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FEMS Microbiology Reviews 24 (2000) 225^249
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The roots of microbiology and the in£uence of Ferdinand Cohn on
microbiology of the 19th century
Gerhart Drews *
Institute of Biology 2, Microbiology, Schaenzlestr. 1, D-79104 Freiburg, Germany
Received 9 June 1999; received in revised form 5 January 2000; accepted 6 January 2000
Abstract
The beginning of modern microbiology can be traced back to the 1870s, and it was based on the development of new concepts that
originated during the two preceding centuries on the role of microorganisms, new experimental methods, and discoveries in chemistry,
physics, and evolutionary cell biology. The crucial progress was the isolation and growth on solid media of clone cultures arising from single
cells and the demonstration that these pure cultures have specific, inheritable characteristics and metabolic capacities. The doctrine of the
spontaneous generation of microorganisms, which stimulated research for a century, lost its role as an important concept. Microorganisms
were discovered to be causative agents of infectious diseases and of specific metabolic processes. Microscopy techniques advanced studies on
microorganisms. The discovery of sexuality and development in microorganisms and Darwin's theory of evolution contributed to the
founding of microbiology as a science. Ferdinand Cohn (1828^1898), a pioneer in the developmental biology of lower plants, considerably
promoted the taxonomy and physiology of bacteria, discovered the heat-resistant endospores of bacilli, and was active in applied
microbiology. ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
Keywords : Concepts in microbiology ; Infectious disease ; Spontaneous generation ; Inheritable feature; Taxonomy of bacteria ; Physiological diversity ;
Bacillus endospore ; Ferdinand Cohn
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The roots of modern science originated in the 17th and 18th centuries . . . .
The progress of biology in the 19th century . . . . . . . . . . . . . . . . . . . . . . . .
3.1. The progress in chemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2. Anatomy, microscopy, developmental cell biology, and sexuality . . . . .
3.3. The development of the evolutionary view in biology . . . . . . . . . . . . . .
The discovery of microorganisms and their ¢rst classi¢cation . . . . . . . . . . .
4.1. The bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2. The fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3. The protozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The concepts of taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1. The species problem in bacteriology and new concepts for classi¢cation
Spontaneous generation vs. evolution of microorganisms . . . . . . . . . . . . . .
The concepts of biological diversity of bacteria . . . . . . . . . . . . . . . . . . . . .
7.1. The organismic and chemical theories of fermentation . . . . . . . . . . . . .
7.2. Autotrophy, chemolithotrophy, and phototrophy . . . . . . . . . . . . . . . . .
7.3. Putrefaction and pathogenicity of bacteria, and immunology . . . . . . . .
The achievements of Ferdinand Cohn . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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* Tel. : +49 (761) 2032607; Fax: +49 (761) 2032779; E-mail : [email protected]
0168-6445 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 6 4 4 5 ( 0 0 ) 0 0 0 2 6 - 7
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1. Introduction
Progress in science has never been a continuous process.
Discoveries, revolutionary ideas, and new concepts were
very often neglected, misunderstood, or attacked if they
did not follow the mainstream of the time. Although bacteria were discovered by observation under the microscope
in the 17th century, they were believed to generate spontaneously and to be transformed into other morphological
and physiological types (pleomorphism). It was not clear
whether bacteria and other infusoria were the cause or the
products of biological or chemical processes. Discussions
on controversial concepts initiated experimental work to
prove or disprove theories. Rational empiricism slowly
overcame speculative reasoning.
2. The roots of modern science originated in the 17th and
18th centuries
In the 17th century, people began to trust the testimony
of nature more than the testimony of human ideas. A
scientist proceeds from the evidence of his own observation, but also from the basis of human written authority.
Modern empiricism was borne on the concept that proper
knowledge ought to be derived from a direct sensory experience of reality in nature. The inductive method for
scienti¢c work in which the conclusion is based on observations and measurements was proposed by Francis Bacon (1561^1626). The classical method of deduction,
which solved scienti¢c problems by sharp reasoning, was
still in use then, but empirical research was favored. Renë
Descartes (1596^1650) propagated that conclusions were
only valid if they could be mathematically proven (in Principles of Philosophy, published in 1644). It was still a long
road to the modern ideas that there is no absolute truth in
biology and that a working hypothesis disproved by experimental evidence has to be replaced by a new hypothesis.
Galileo Galilei's Discourse Concerning Two New Sciences (1620), Robert Boyle's Excellence and Grounds of the
Mechanical Hypothesis (1666), and Isaac Newton's (1643^
1727) Mathematical Principles of Natural Philosophy
(1687) introduced a mechanistic view of nature. Physical
forces were put forth as the cause of biological processes.
There was no dissonance between reductive causal explanation, the omnipresence of God and his part in the vital
principle, and mathematical abstraction. In addition to the
material world, the spiritual world was stressed by Baruch
Spinoza (1632^1677).
Gottfried Wilhelm Leibniz (1646^1716), who reacted
positively to the discovery of the world of microorganisms,
tried to harmonize religious belief with the aspects of the
new science. The animalcules were designated as a very
low order of monads. The philosophers of that time found
in the revelations of the microscope a way to combine the
natural and supernatural worlds and to place the knowledge of nature within theological space [1]. The mechanistic-materialistic view was supported and extended by
Georges Louis Leclerc Comte de Bu¡on (1707^1788),
who published a universal history of nature with descriptions from minerals up to humans (Histoire Naturelle,
Gënëral et Particulie©re, 1749^1804, 54 volumes, completed
by Etienne de Lacëpe©de after Bu¡on's death). Bu¡on
stressed the importance of fossils as witnesses of earlier
periods of life on earth, but he denied the descent of extant
organisms from those of earlier periods because bastards
are sterile and evidence of intermediates between present
and extinct forms was lacking. He believed the Newtonian
concept that organic molecules from the decomposition of
organisms generate or can be incorporated into a new
organism [2]. In his work both the inductive method and
the deductive method were used. By the end of the 17th
century, even those naturalists and philosophers in£uenced
by the mechanical perception of nature doubted Descartes'
e¡ort to derive the generation of animals from a mechanistic nature [3].
Scientists who preferred the inductive method were confronted with problems such as how precarious instrumentally mediated experience could be and how much work
was required to declare observations as reliable. Another
problem accompanying the more modern use of individual
sensory experience was the evaluation of traditionally established knowledge [1,3^5].
Although the inductive method was used more and
more in research, philosophers and many scientists, in£uenced by philosophical ideas, believed until far into the
19th century that they could solve biological problems
by reasoning and explain physiological functions by unclearly de¢ned abstract terms like `vital forces'. Immanuel
Kant (1724^1804) believed that in our thoughts we pass
from a mechanistic view of the parts to a teleological view
of the whole, and we cannot separate these classes of view;
there is a hidden basic principle of nature which unites the
mechanistic and teleological views. Georg Christoph Lichtenberg (1742^1799), a mathematician and physicist in
Go«ttingen, should be mentioned because he personi¢ed
the experimenter who was critical and skeptical of his
own results and rejected any speculative philosophy. He
represented an example of the English empiricism in the
age of enlightenment.
3. The progress of biology in the 19th century
In the 19th century, many biologists made an imperfect
fusion of the Kantian scheme with materialism, as for
example by the `Naturphilosophen' such as Lorenz Oken
(1779^1851), who contributed considerably to embryology, but who tried to construct a biology that could re£ect
the action of the human mind in the animal kingdom and
who considered `natural sciences as the science of the eter-
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nal transubstantiation of God in the world' (1848); Gottfried D. Nees von Esenbeck (1776^1858); and Carl Gustav
Carus (1789^1869), who made careful comparative studies
in di¡erent ¢elds, but tried to explain biological phenomena by teleological principles. These men proposed `ideal
forms' and linked them with the conception of the purpose
that is inherent in living things. The ideas of Naturphilosophie, which dominated in the ¢rst half of the 19th century, especially in Germany, were replaced by the unifying
idea of natural sciences in order to discover the laws of
nature and to rule humanity. One exponent of this thinking was the German pathologist and anthropologist Rudolf Virchow (1821^1902) [5,6].
3.1. The progress in chemistry
In addition to the mechanistic view of biological processes, the beginning of chemical analysis was important
for the progress in biological research. Antoine Laurent
Lavoisier (1743^1794) disproved the phlogiston theory of
Georg Ernst Stahl (1660^1734) by determining the weights
of products from chemical reactions. Oxygen, dinitrogen,
and carbon dioxide were discovered as components of air.
Joseph Gay-Lussac (1778^1850) isolated the metals of the
alkaline-earth group and formulated the law of combining
volumes of gases. In 1811, Amadeo Avogadro described
the distinction between molecules and atoms and proposed
the concept that equal volumes of di¡erent gases contain
the same number of particles under the same physical
conditions. The modern system of chemical symbols and
formulas was developed and many new elements were discovered by Jo«ns Berzelius (1779^1848). He also coined the
term `catalysis' for a process in which a compound a¡ects
the velocity of a chemical reaction, but remains unchanged
and does not contribute to the substrate or products of the
reaction. Friedrich Wo«hler (1800^1882) and Justus von
Liebig (1803^1873) strongly in£uenced biology through
their analysis and synthesis of organic compounds and
by disproving the role of a vital power in the synthesis
of organic compounds. They refuted, however, the role
of microorganisms in fermentation and putrefaction and
proposed, instead of `the metamorphosis' by an organic
product of decomposition, the `ferment'.
Although bioenergetics and thermodynamics were not
included in textbooks until late in the 19th century and
thermodynamic calculations were not considered for metabolic processes, the unde¢ned and obscure term `vital
force' was replaced by the understanding that activities
of living things require the performance of work, whether
chemical, mechanical, osmotic, or electric [7]. The theory
of heat and conservation and the correlation of energy was
proposed by Julius Robert Mayer in 1845 and the law of
the conservation of energy and the calculation of heat
units were proposed by Hermann L. Helmholtz in 1846
and James Prescott Joule in 1843. Scientists slowly became
aware that energy is supplied by metabolism, respiration,
227
fermentation, and photosynthesis, but the problem of energy coupling, i.e. the linkage between energy-yielding and
energy-consuming processes, was not resolved before the
1940s and 1960s.
3.2. Anatomy, microscopy, developmental cell biology, and
sexuality
In the 16th to 18th centuries, the great diversity of
plants and animals was recognized and the anatomy of
humans, animals, and plants was described in numerous
comprehensive articles.
The ¢rst microscopes consisting of one or two optical
lenses were build by Johannes and Zacharias Janssen
about 1590. The propagation of light and its re£ection
and refraction by an optical lens has been known since
the work of Christian Huygens (1629^1695). He constructed simple microscopes and telescopes. The magni¢cation of these microscopes was low, and the pictures of
objects were a¡ected by the chromatic and spherical aberration of their lenses because the light rays of various
wavelengths do not focus in the same plane. It is remarkable that Marcello Malpighi (1628^1694), Nehemiah Grew
(1628^1711), Antonie van Leeuwenhoek (1632^1723), and
Robert Hooke (1635^1703) observed and described bacteria, protozoa, fungi, spermatozoa, erythrocytes, and tissues of plants and animals in ¢ne detail using these primitive instruments. Leonhard Euler (1707^1783) postulated
and several scientists such as G.B. Amici and A. Chevalier
constructed the ¢rst achromatic lenses by combining lenses
of di¡erent refraction indices. The objectives and oculars
of the commercially produced microscopes were, until late
in the 19th century, of variable quality because they were
produced by empirical methods of trial and error. A progressive step was taken when the physicist Ernst Abbe
(1840^1905) developed a theory of the image formation
in the light microscope and constructed, in cooperation
with the mechanic Carl Zeiss (1816^1905) and the producer of optical glass Friedrich Otto Schott (1851^1935),
oil-immersion lenses with a high numerical aperture and
the Abbe condenser for optimal illumination of the specimen ¢eld. The problem of spherical aberration, which
caused blurred ¢gures in the periphery of the microscope
¢eld of view, was solved by a combination of di¡erent
lenses. These new improved microscopes were made popular in the cell biology and microbiology institutes about
1877^1878 by Ferdinand Cohn and Robert Koch, who
tested these objectives and Abbe's condenser [8,9]. Since
then, microscopes ¢tted with oil-immersion lenses that
bring about a maximal resolution of 0.2 Wm have been
available. The documentation of bacteria was decisively
improved by Robert Koch (1843^1910). He developed
the method of staining smears in cooperation with C.
Weigert [10] and the method of ¢xation of bacteria on
cover slips, and introduced microphotography [11,12] using a heliostat for illumination [11^14]. The di¤cult prob-
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
lems in the preparation of microphotographs were vividly
described by Heymann [13].
The cells as building stones of tissues and organisms
were described by C.F. Wol¡. The great period of cell
biology began in the 1840s with the availability of an
improved microscope, the knowledge of comparative histology increased, and new thoughts on the role of cells
grew [15]. Johannes E. Purkinje (1787^1869) was the ¢rst
to use the term protoplasm [16] and proposed the idea of
the similarity of animal and plant cells. Hugo von Mohl
(1805^1872) and Matthias J. Schleiden (1804^1881) were
recognized as the founders of the cell theory; they considered the cell as an independent living entity of all organisms [17^19]. Initially the protoplasm was considered as a
very simple mucous material. In the 1880s, the nucleus was
shown to be an indispensable constituent of animal and
plant cells, and mitotic cell division was described by E.
Strasburger, Francis Balfour, L. Auerbach, and W. Flemming.
Microorganisms were believed to be very variable (pleomorphic) and to generate spontaneously. In the period of
£ourishing cell biology around 1840, many scientists began
to study the developmental history of lower algae, fungi,
and protozoa, and later of bacteria. Ferdinand Cohn
(1828^1898) investigated the unicellular algae Protococcus
pluvialis Ku«tzing and Stephanosphaera pluvialis and elucidated the di¡erent stages of development and the di¡erence between vegetative and generative multiplication of
swarm cells (macrogonidia and isogametes) [20^24]. About
the same time, but independently, the sexuality of algae
was discovered in 1854 by Gustave Thuret in Fucus, of
Vaucheria in 1855 by Nathanael Pringsheim (1824^1894),
and of Sphaeroplea annulina and Oedogonium in 1855/1856
by Cohn [22,24]. The fecundation of the egg cell in the
oogonium by the spermatozoids or the fusion of isogametes in cryptogamae, algae, and fungi was carefully
studied by Cohn, Heinrich Anton de Bary, Thuret, Pringsheim, and others [19]. It was concluded that sexuality is a
peculiarity not only of higher but also of lower organisms.
The discovery by Cohn [25,26] of the complex developmental cycle, functional di¡erentiation, and sexual reproduction of Volvox globator and many other microorganisms was not only interesting from the point of cell
biology, but also important for modern taxonomy and
physiology. The concept that shape and function of each
higher organism is based on a special plan was developed
by the comparative anatomy studies in the 17th and 18th
centuries. The progress in chemistry and comparative cell
biology extended this concept to cells as the building
stones of all organisms which are structurally and functionally di¡erentiated during the development of the organism.
3.3. The development of the evolutionary view in biology
Several scientists of the 17th and 18th centuries became
aware that extant life forms were organized di¡erently
than those of earlier periods of the Earth's history. It
was also realized that most organisms live in restricted
areas, in natural habitats. The question of the origin of
species was realized and the descent of species from common ancestors was discussed, but the static view of nature
and the belief that all organisms could be traced back to
creation or di¡erent forms of spontaneous generation,
such as abiogenesis or heterogenesis, dominated
[3,27,28]. Species were believed to be invariable.
Jean Baptiste Antoine de Monet Chevalier de Lamarck
(1744^1828) was one of the ¢rst to explain the multiplicity
of forms of organization and their gradation from primitive to highly developed species by a process of evolution
[28,29]. Impressed by the comprehensive comparative
studies of fossils and living organisms, he postulated that
the fossil species are ancestors of the living species. Lamarck proposed that the environmental conditions
changed over long periods and that low to high complexity evolved by an inherent potential and by adaptation to
the changed environmental conditions. He believed that
the acquired properties were transmitted to the next generation. Although he did not explain the mechanism, his
theory of evolutionary change replaced the static view of
nature.
Georges Lëopold Cuvier (1769^1832) contributed to the
theory of evolution with comprehensive comparative studies on the anatomy of vertebrates and invertebrates and
with paleontological studies, but continued to believe the
constancy of species. He and the geologist Charles Lyell
believed that extinction of species was caused by changes
in environmental conditions during geological periods and
that new species originated discontinuously by creation,
spontaneous generation, or sudden changes.
Charles Robert Darwin (1809^1882) founded his theory
of the evolution on the basis of his own studies and the
numerous published observations of comparative anatomy
of living and fossil organisms [30]. He concluded that all
organisms have a common origin. Darwin assumed a continuous formation of a large and inexhaustible supply of
genetic, i.e. inheritable, variations. In subpopulations of
species, living in a separate habitat, natural selection
caused diversity even within a species. Individuals and
populations formed that changed their features slowly
from that of the original species. New species originate
from varieties. Natural selection was, in the view of Darwin and Alfred Russel Wallace (1823^1913), not an accidental process, but was caused by di¡erential success in
reproduction and competition within the population of the
organisms and was determined by the interactions with the
speci¢c physical, chemical, and biological conditions of its
habitat. New varieties optimally adapted to their surroundings survived and dominated in their habitat; less
adapted varieties disappeared [28,30,31]. The principles
of natural selection, evolution, and origin of species were
not accepted immediately by the scienti¢c community of
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the 19th century, and the concept of spontaneous generation by abiogenesis was revived to explain the formation
of the ¢rst organisms on Earth [6,27].
4. The discovery of microorganisms and their ¢rst
classi¢cation
4.1. The bacteria
The supposition that various diseases are caused by microorganisms was expressed several times in the early literature [29]. In 36 BC, Marcus Terentius Varro wrote that
animals (animalia quaedam minuta) that cannot be followed by the eye were transferred through the air to other
persons and caused serious diseases. It is clear from his
publication that he described malaria, which is caused by
the sporozoon Plasmodium and is spread by the mosquito
Anopheles [32]. Girolamo Fracastoro (1478^1553) studied
the `French disease' syphilis and wrote in 1546 that the
`contagion is an infection that passes from one thing to
another' by direct contact between two persons, by contaminated material, or over long distances. He also described the pathology of a contagious disease, presumably
spotted fever caused by Rickettsiae [29,33]. Athanasius
Kircher (1602^1680) studied infectious diseases caused by
a contagium animatum. In contrast to the medical doctors
of his time, who believed that diseases are caused by putrefaction of the body humor or miasma, he observed
`vermes' in the blood or lymph nodes of people su¡ering
from bubonic plague caused by Yersinia pestis. Presumably he did not see the bacteria, but rather particles in
the tissues.
The ¢rst clear evidence for the existence of bacteria was
given by Leeuwenhoek. He was an optician by hobby and
constructed, as did many contemporaries, numerous microscopes. The important step forward came from his very
careful and imaginative style of observation. In more than
200 letters to the Royal Society in London, which were
published in the Transactions of the Royal Society, and in
letters to Robert Hooke, he described di¡erent forms of
bacteria, yeasts, and protozoa [1,4,34^36]. He also performed some simple experiments, e.g. he studied the in£uence of acetic acid on the mobility of bacteria, which he
called animalcules, beesjes, or cleijne schepsels. The detailed description of bacteria from tooth plaque, water
samples, and hay infusion is remarkable considering the
low magni¢cation and resolution of his simple instruments. The bacteria he saw were documented by drawings.
The size of the bacteria was determined by comparison
with grains of sand or erythrocytes. The movement of
bacteria was described in detail. The new knowledge on
the animalcules or vermes quickly circulated and initiated
many microscopy studies in order to ¢nd infusoria in organic material or tissues from sick people [36]. The development of the idea of the contagium animatum up to the
229
causal analysis of infectious diseases will be dealt with in
Section 7.3.
Carl von Linnë classi¢ed the microscopic organisms in
the genus `chaos' (1773^1776). Otto Friedrich Mu«ller
(1730^1784) criticized the scientists of this epoch for contemplating the infusoria without any critical characterization and classi¢cation. In his book Animalcula infusoria
£uviatilia et marina, he classi¢ed the infusoria by morphological and biological criteria, such as movement, habitat,
and formation of aggregates. From the 18 genera he proposed, only several characteristic types, especially Flagellata and Ciliata, can be identi¢ed. Bacteria, but also Protozoa, appear under the taxa Monas and Vibrio. He
described 10 species of Monas and 31 species of Vibrio.
The description of the infusoria was documented by ¢gures [37]. The knowledge of the larger forms of infusoria,
the protozoa and unicellular algae, was improved in the
following decades, but the studies on bacteria concentrated on the question of their origin (see Section 6).
Christian Gottfried Ehrenberg used an improved microscope, ¢tted with achromatic combinations of lenses, to
study the `Infusionsthierchen als vollkommene Organismen' (infusoria-animalcules as complete organisms) [38].
The largest part of this book was devoted to the protozoa.
The most simple organisms he observed were classi¢ed as
Monadina and Vibrionia. The tail-less, lip-less, eye-less,
most simple monadina were subdivided into sphere monads and rod monads. The genera Monas, Bacterium, Vibrio, Spirillum, Spirochaeta, and Spirodiscus were described, but the species were less well characterized.
Fëlix Dujardin subdivided the bacteria, combined in the
family Vibrioniens, into the genera Bacterium, Vibrio, and
Spirillum [39]. Four species of Bacterium ^ B. termo, B.
catenula, B. punctum, and B. triloculare ^ were described.
The species Vibrio lineola, V. rugula, V. serpens, and V.
bacillus were distinguished from Spirillum undula, S. volutans, and S. plicatile by their shape and movement. The
organisms described by both authors cannot easily be
identi¢ed by present taxonomic characteristics. The work
of Maximilian Perty [40] did not improve the taxonomy.
He confused the characterization by mixing up developmental stages with species. He subdivided the so-called
animal-plants or Phytozoidia, into Filigera, Sporozoidia,
and Lampozoidia, and further subdivided the latter into
Vibrionida, Spirillina, and Bacterina. Allied to the Spirillina, the species Spirochaeta plicatilis, Spirillum volutans,
Spirillum undula, and Spirillum rufum were mentioned.
The Bacterina were subdivided into Vibrio, Bacterium,
Metallacter and Sporonema.
4.2. The fungi
The large fruiting bodies of basidiomycetes and ascomycetes, conspicuous to the unaided eye, may have been
known to man since primitive times. Humans have used
fungi, often unknowingly, for fermentation in wine, beer,
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and bread making. Fungi were also used as food, drugs, or
poison.
In the 16th and 17th centuries, the shape, appearance,
and usefulness for man of numerous fungi were described,
for example, by Charles de L'Ecluse (Clusius ; 1526^1609)
[41]. Gaspard Bauhin (1560^1624) was the ¢rst to discern
genera and species in his detailed and illustrated description of plants. In his book, 2700 species of plants and 100
species of fungi were described. The fungi were separated
into esculentii, noxii, and perniciosi [42]. Joseph Pitton de
Tournefort (1656^1708) presented a hierarchical ordered
system with detailed descriptions of genera [43]. Fungi
were separated into six groups: (1) centrally stalked with
cap; (2) centrally stalked without cap; (3) laterally
stalked ; (4) globose without stalk, including myxomycetes; (5) subterranean forms; and (6) corraloid forms.
Developmental stages, e.g. teleutospores of rust or mycelium of fungi, as described by Robert Hooke, were not
included.
How fungi propagated was not known, and they were
believed to originate from decaying substances. The revolutionary idea that all plants produce seeds was proposed
by Porta in 1590. He described spores, which he called
seeds, isolated from numerous fungi. M. Malpighi pictured in his book of the anatomy of plants [44] sporophores, sterigmata, and spores, and speculated whether
spores were units of propagation. Pier Antonio Micheli
(1679^1737), although he never received an academic degree, made great progress in the description of cryptogamae. He introduced the names of many generic names,
such as Mucor, Aspergillus, and Polyporus, and his descriptions of species are so detailed that they can be identi¢ed today. With a primitive microscope, he observed
seeds (spores) and sporophores in many groups of fungi,
and he cultured certain molds on pieces of fruit. He followed the germination of spores and the growth and development of fungi up to the fruiting bodies, and concluded that each fungus formed its own seeds and is
reproduced only by its own kind [45]. Carl von Linnë
(1707^1778) included the described fungi as a class of their
own in his book on species plantarum [46], where he established the binomial system of nomenclature. He did
not, however, contribute to a better understanding of fungi.
In the second part of the 18th century, many detailed
descriptions of fungi were published and illustrated with
excellent drawings [47]. Phenomena of infected plants had
been known since the classical period. Phytopathology,
based on empirical research, was initiated by Mathieu Tillet (1714^1791). He studied loose smuts and hard smut of
wheat and showed that they are infectious diseases. He
observed that seeds (spores) from smutted kernels produce
smutty wheat [48]. In 1767, Giovanni Targioni-Tozzetti, a
disciple of Micheli, described the infection of plants by
germinating rust spores. He observed the penetration of
the epidermis through the stomata by germ tubes and the
development of the fungus inside the wheat plant [49]. In
the same year, Felice Fontana published the results of his
microscopy studies on the rust of grain. Bënëdict Prëvost
(1755^1819), who was not familiar with these important
observations, published in 1807 his detailed and careful
studies on the germination of bunt or smut spores and
the infection and development of the fungus in wheat
plants. He observed that copper sulfate inhibits the germination of spores, and he demonstrated by ¢eld experiments that the disease can be controlled by soaking the
wheat seeds in a solution of copper sulfate [50]. Although
this method was not widely accepted at that time, it was a
precursor of the Bordeaux mixture, introduced by Pierre
Millardet in 1885, which became in combination with the
lime-sulfur solution the world's outstanding preventive
fungicide, used at ¢rst to ¢ght downy mildew on vine
leaves caused by Plasmopara viticola [51].
A new period of research in mycology began with Heinrich Anton de Bary (1831^1888). He and many of his
students and coworkers, such as O. Brefeld, E. Fischer,
A. Meyer, P. Millardet, and M. Woronin, published important papers in the ¢eld of sexual and asexual reproduction, development, and parasitism of fungi [52^55,60]. In
1893, Pierre Dangeard observed nuclear fusion in the teleutospores of a rust fungus, and in 1894 in Peziza. He
interpreted this process correctly as a fecundation. This
progress in developmental biology was the basis of a modern taxonomy of fungi. Ferdinand Cohn studied the development of the zygomycete Pilobolus crystallinus and of the
entomophthoracea Empusa muscae [56,57].
Johann Scho«nlein in 1839 and David Gruby in 1841
described Trichophyton and Candida albicans as infectious
fungal parasites of man and founded the ¢eld of medical
mycology [29].
The ¢rst systematics of fungi was published by Christian
Persoon [58]. He understood that mushrooms are only
fruiting bodies and are not the whole plant. He recognized
two types of fruiting bodies: those in which the hymenium
is uncovered during maturation of the spores and those in
which the hymenium is enclosed, e.g. the pu¡ball (bovist).
He established a herbarium containing the type species.
The fungi known at that time were divided into 71 genera.
Other systematic treatments of fungi were published by
Elias Magnus Fries [59], and in 1837^1854 by August
Corda [29]. These early systematic studies were based exclusively on morphological data. De Bary emphasized the
importance of the developmental history and of the sexuality for classi¢cation of fungi [53].
Nutritional physiology and the development of exact
methods to analyze growth and nutrition of fungi were
founded by Jules Raulin, who elucidated the mineral requirements of Aspergillus niger [61]. The growth of fungi
on a mineral medium completed with an organic carbon
source was introduced by Louis Pasteur, but Raulin was
the ¢rst to determine quantitatively the growth of fungi
and the consumption of the nutrients. He recognized that
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besides the macroelements and one organic carbon source,
trace elements were essential for the growth of Aspergillus,
but their exact analysis required improved methods for
puri¢cation, which were not available at that time.
4.3. The protozoa
The protozoa, called `infusoria', have been described in
many monographs since the 17th century. Christian Gottfried Ehrenberg (1795^1876) was well known for his detailed and comprehensive description of more than 500
species [38]. He observed that the small animals take up
particles of carmin or indigo into vesicle-like structures,
which he called stomach. He proposed the concept that
protozoa have complex internal structures similar to those
of higher organisms. Felix Dujardin (1801^1862), who
stressed the importance of the work of Ehrenberg, rejected
this hypothesis as most of his contemporaries did. Dujardin improved the systematics of protozoa and observed
that sodium phosphate, ammonium oxalate, sodium bicarbonate, and ammonium nitrate were used by the infusoria
as nutrients [39].
5. The concepts of taxonomy
The comparative anatomy studies in the 17th and 18th
centuries brought together a comprehensive knowledge of
the shape, structure, and organization of organisms. The
great diversity in the world of living beings, the purely
practical need to bring order into the richness of life,
and the desire to investigate the perfect harmony of nature
and its diversity were motives to study systematics. In
the era of Linnaeus, systematics had enormous prestige
and dominated all other contemporary research. Linnaeus
and his contemporaries believed that genera and higher
taxa are creations of God and that therefore his systematics represented a natural system. This systematics
was based on essential properties and originated from
creationist thinking in the absence of an evolutionary
theory (essentialism). The principle of logical downward
division is based on the similarity of organisms and £owed
from the higher to the lower taxa using the method
of dichotomy. It was a purely descriptive work, but it
was a rich source of information. Linnë not only introduced binary nomenclature, he also completed the species
description by adding remarks on the habitats of the
species.
The quite di¡erent systems which originated in the 17th
and 18th centuries were in£uenced by the choice of the
characteristics used for the ¢rst division [28]. Even within
a system, the type of characteristic was changed, e.g. from
fructi¢cation to vegetative growth, or from morphological
to physiological features. It was discussed whether one
should use only a single key characteristic or multiple
characteristics; whether one could use characteristics other
231
than morphological characteristics for classi¢cation, e.g.
physiological and ecological features; and whether the
characters should be weighted. The re¢ned and extended
knowledge of organisms living in di¡erent parts of the
world and the revolution in philosophical thinking made
the downward classi¢cation of essentialism unsuitable for
classi¢cation. Practical considerations led to the adaptation of an upward classi¢cation of empirical grouping using numerous characteristics. This method started with the
characterization of species, followed by sorting of species
into groups of similar ones, and combining these groups
into a hierarchy of higher taxa [28]. In 1772, Adanson
introduced the use of multiple characteristics for classi¢cation. He recognized that di¡erent characteristics have
di¡erent taxonomic signi¢cance.
Taxonomy was revolutionized in the 19th century by
Charles Darwin, the founder of evolutionary taxonomy.
Darwin explained why groups of species are related to
each other. In the thirteenth chapter of The Origin of
Species [30], he developed the theory of classi¢cation.
His theory of common descent provided reasons for the
degrees of similarity among organisms and an explanation
for the hierarchy and for the homogeneity of taxa in a
natural classi¢cation. Darwin also discussed methods
and di¤culties of classi¢cation. He stressed that true classi¢cation is genealogical and, therefore, the taxonomical
value of all characters has to be weighted. Similarities due
to descent have to be separated from similarities due to
convergence. However, the Darwinian revolution had only
a minor impact on the methodology of classi¢cation. Upward classi¢cation had already been introduced before
Darwin [28].
The classi¢cation of microorganisms, especially of higher taxa, was improved in the 19th century by the discovery
of sexuality and of the development of fungi, lower algae,
and protozoa. In earlier times, very often di¡erent stages
in the life cycle or zoospores were described as di¡erent
species or interpreted as polymorphy. The discovery of the
ascus and the basidium and their role as meiosporangia
was decisive for the grouping of ascomycetes and basidiomycetes.
5.1. The species problem in bacteriology and new concepts
for classi¢cation
Bacteria have been known since the early observations
of Leeuwenhoek, and many studies were published after
that time which describe `small animals' or `infusoria' as
contagion (Jakob Henle (1809^1885), contagium vivum
[62]) or as `ferment' of butyric acid fermentation [63,64].
Unfortunately, no scientist carefully isolated the particular
microorganisms and studied them in their environment.
The bacterial forms observed with the microscope were
described as a new species without consideration of the
forerunner. The work of Ehrenberg and Dujardin was
an exception, but they did not characterize the species
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su¤ciently. The problem of the origin of bacteria and of
independent, distinct species was still not solved by 1850.
Ferdinand Cohn (1828^1898) stressed that in the ¢eld of
bacteriological systematics, one has to start at point zero
[65,66]. His taxonomic studies were based on an excellent
knowledge of the unicellular algae, lower fungi, protozoa,
and bacteria. He noticed that the cellular organization and
other structural details of bacteria could not be resolved,
even when the bacteria were observed with the strongest
oil-immersion objective of the microscope (the methods of
phase-contrast microscopy and staining of bacteria were
still not discovered) [65,66]. Only a few characteristics
were available for classi¢cation, and it was not known
whether they are stable and species-speci¢c stages of development, or variations caused by environmental conditions. Sexual reproduction of bacteria was unknown.
The isolation of single cell clones and the pure culture
technique were slowly developed from the cultivation on
solid media and enrichment cultures. The growth of colored bacteria on starch-containing food was described by
Herrmann Ho¡mann ([36], p. 110). Joseph Schroeter, a
coworker of Cohn, transferred colonies of pigmented bacteria, grown on slices of cooked potato, to another piece
of solid food to separate the colored from the colorless
bacteria [67]. Clone cultures of fungi were obtained in the
laboratories of de Bary and Brefeld by sowing single
spores on solid media ([54], pp. 2 and 5; [60,68]). Scientists
became rapidly acquainted with the culture of bacteria on
solid media and the technique was used in the laboratories
of Cohn and Koch starting in about 1875 [36]. The separation of single cells by streaking bacteria on solidi¢ed
gelatin was introduced by Koch in 1877 [12] and the use
of plates with gelatin was introduced by Koch [12,14,69]
and Esmarch [70,71]. Frankland [72] and Petri [73] developed a small, practical culture chamber, the Petri dish, to
keep the cultures free of contamination through the air.
The introduction of agar as a solidifying agent greatly
improved the isolation and culture of bacteria because
agar is inert for most bacteria and is still solid at 37³C,
the temperature at which most pathogenic bacteria were
cultivated [74,75].
Cohn noticed that species and genera of bacteria have
meanings di¡erent than those of higher organisms, because generative propagation was not known. The classi¢cation of bacteria had to start from the characterization
of `form-genera' and `form-species'. The question whether
these species are related to each other in their develop-
ment, chemical features, and descent could only be answered in the future when new chemical methods became
available [65,66,76]. From the beginning of his studies,
Cohn was convinced that the kingdom of bacteria consisted of species with inherent characters. He defended
this concept against Theodor Billroth (1829^1894) and
many other contemporaries who believed that all spherical
bacterial forms and all rod-shaped bacterial forms each
belong to only one species of plants and have `only one
form of life' (`eine einzige Lebensform') which can adapt
to di¡erent conditions of the environment and change
their form accordingly (pleomorphy): Micro-, Meso-,
Megacoccus and Micro-, Meso-, and Megabacteria. Billroth combined all genera proposed by Cohn in the polymorphic species Coccobacteria septica, except for Spirillum and Spirochaete, which he did not consider [77,78].
Joseph Lister defended the idea that bacteria are generated
from conidia of fungi and that they change their morphology during culture on di¡erent media [76,79]. From the
description of his experiments, it seems clear that he transferred a mixture of di¡erent organisms to new media and
that speci¢c microorganisms were selected during growth.
During this time, several pathologists described microorganisms in di¡erent diseased tissues, but they did not isolate and characterize the bacteria [36]. Although they
speculated that these organisms cause the illness, no experiments were undertaken to identify the organisms and
to study their e¡ect on the human body.
During a period of about 20 years Cohn and coworkers
studied numerous distinctive characteristics of bacteria,
such as cytological details, movement, growth under various conditions in mineral media substituted with one carbon source or on complex media, appearance of pigments,
and the formation and germination of endospores (Fig. 1).
The structure of £agella and the swarming phenomenon
were detected, and the function of £agella was correctly
interpreted [66,67,76,80]. On the basis of these investigations and his being impressed by Darwin's theory of origin, evolution, and selection of species, Cohn developed a
new concept of bacterial classi¢cation. Bacteria were de¢ned as mostly pigment-free cells of characteristic shape
that multiply by cross division and live as single cells,
¢lamentous cell chains, or cell aggregates. They contain
a plasma membrane and sometimes refractile granules.
They form a distinct kingdom of microorganisms that
are discernible by heritable characteristics that allow the
classi¢cation into distinct species with typical character-
C
Fig. 1. Di¡erent bacteria, drawn by Cohn. A: (Table V in [66]). 8) Cladothrix dichotoma, described on p. 185 in [66], similar to Scytonema, false
branching; 9) Bacillus anthracis, from blood of a cow which died from anthrax; 10) mobile bacteria with endospores from rennet ; 11) bacilli with endospores from butyric acid fermentation; 12) Micrococcus and spores from rennet ; 13) Micrococcus bombycis from silkworm, sick from £accid disease.
B: (Table VI in [66]). 9, 10) Lamprocystis (Clathrocystis) roseopersicina ; 11) Chromatium (Monas) warmingii ; 12) Chromatium (Monas) okenii; 13) Chromatium vinosum (Monas vinosa); 14) Rhabdomonas rosea containing sulfur globules, pink colored; 15) Ophidomonas (Spirillum) sanguinea, large, red colored with light-scattering granules (Thiospirillum jenense?); 16) Spirochaete Obermeieri, Borrelia recurrentis with red blood cells; 17) Bacillus ruber
Frank (p. 181 in [66]), red colored, growing on cooked rice; 18) Myxococcus (Micrococcus) fulvus, red colored colonies.
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
istics, which are transmitted to the following generation
when bacteria multiply. Cohn proposed that within the
species, varieties originate, which transmit their new features to the next generation. He was convinced that bacteria belong to the plant kingdom and that they are related
to algae [66,76,80^82]. From his studies on development,
he concluded that bacteria are closely related to the Phycochromaceae (Rabenhorst 1865), which were also known
as Myxophyceae (Wallroth 1833), Schizophyceae, or Cyanophyceae (Sachs 1874); today they are named cyanobacteria ([83], p. 1711). Schizophyceae and Schizomyceae
(bacteria) were combined in the group of Schizophyta (¢ssion plants) [76,80,84,85]. The close relationship between
bacteria and Schizophyceae was exempli¢ed by comparison of the chlorophyll- and phycocyan-containing Oscillatoria with the colorless Beggiatoa (Fig. 2). These two genera have the same shape and cellular organization and the
same type of movement, which is a combination of gliding
forwards and backwards, a rotation around the longitudinal axis, and a vivid bending of the trichomes. The Chroococcaceae were compared with Micrococcus and Bacterium, Merismopedia with Sarcina, and Spirulina with
Spirillum. A relationship between groups of bacteria, phycochromaceen, £orideen (red algae), and lichen was deduced mainly on the basis of the pigments chlorophyll,
phycocyan, and phycoerythrin and the type of cell division, movement, and reproduction [84,85]. Cohn supposed
that the Phycochromaceae were early inhabitants of the
earth because of their ability to grow in extreme habitats,
their simple way of reproduction, and their fossil record.
The fungi were considered as a group of microorganisms
not related to the bacteria and phycochromaceen [76,86].
Cohn classi¢ed the bacteria into: (I) Sphaerobacteria
(sphere-shaped) with the genus Micrococcus, (II) Microbacteria (rod-like) with the genus Bacterium, (III) Desmobacteria (¢lamentous bacteria) with the genera Bacillus
and Vibrio, and (IV) Spirobacteria (screw-like bacteria)
with the genera Spirillum and Spirochaeta [76,80,81]. Micrococcus was divided into three groups of species based
on the characteristics chromogen (pigmented), zymogen
(fermenting), and contagion (pathogen). Bacterium termo
was speci¢ed as the cause of putrefaction. Contagion and
putrefaction were discerned as speci¢c features. In the description of the screw-like bacteria, Cohn followed the
names proposed by Ehrenberg : Spirochaeta plicatilis, Spirillum volutans, S. tenue, and S. undula. The bacteria were
cultivated on synthetic media with various carbon sources
or on complex media. The inheritance of features, e.g.
pigmentation, was supported by their stability in following
generations. The pigments were di¡erentiated by solubility
or insolubility in water and their color and were analyzed
by simple chromatographic, spectroscopic, and chemical
methods. The genus Sarcina [66,76] was determined by
the occurrence of division in three perpendicular planes.
The principles of Cohn's bacterial taxonomy were not
generally accepted. H. Karsten, A. Wiegand, Estor, Win-
Fig. 2. Beggiatoa species, from Cohn, F. (1866) Hedwigia 5, 161^166.
ternitz, and others still believed that bacteria originated
from decaying plant and animal tissues ([36], p. 130) or
spontaneously [27,76]. E. Hallier supported the germ
theory of infectious diseases, but he believed that the micrococci he isolated from pathogenic material were transformed into fungi [87]. The fungus theory of Hallier was
strongly refuted by de Bary because of Hallier's faulty
experiments [88]. Hallier considered the succession of different organisms that he observed in his culture apparatus
as stages of the same organism, which he regarded as
genetically connected [87]. Billroth, Lister, Na«geli [89],
and other contemporaries defended the opinion that the
morphological and physiological di¡erences between the
species are caused by nutrition and other growth conditions [35,36]. T.A. Edwin Klebs (1834^1913), a pathologist, agreed with the hypothesis that bacteria can be classi¢ed into di¡erent species, and he defended the germ
theory of infectious diseases ; in addition to micrococci
and bacilli, he proposed microsporines and monadines
[90,91]. Ray Lankester observed enrichments of purple
bacteria in decaying organic material and named the pig-
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ment bacteriopurpurin and the bacterium Bacterium rubescens [92]. He thought that all the bacteria that contained
bacteriopurpurin but which had di¡erent shapes were
phases of one and the same organism (pleomorphism)
[93]. Cohn, Ehrenberg, Engelmann, Warming, N. Winogradsky, and Zopf described many species of purple bacteria (the name was coined by Engelmann) mainly on the
basis of their morphology, pigmentation, physiology, and
cell inclusions (Fig. 1) [38,76,80,81].
An important achievement of Cohn was the species concept, founded on the hypothesis that distinct species-speci¢c populations have several inheritable characteristics in
common, which di¡erentiate them from other species. The
concept was solidi¢ed as soon as pure cultures of bacteria
were isolated which had stable markers such as pathogenicity, e.g. Bacillus anthracis [94], or nitri¢cation, e.g. Nitrosomonas [95^97]. The principle of upward classi¢cation
based on invariable, multiple characteristics remained the
method of choice for decades. The progress in methods to
study bacteria and the increasing knowledge of the physiological and biochemical features of bacteria led not only
to the identi¢cation of new species, but also to grouping of
the species into higher taxa. The concept of bacteria as an
independent group of microorganisms with di¡erent inheritable characteristics and their relationship to the Schizophyceae (Cyanobacteria) was con¢rmed and extended by
R. Stanier and C.B. van Niel [98], who proposed the term
prokaryotic cell organization, which di¡ered from the
organization of eukaryotic cells. This fruitful concept
was quickly accepted by the scienti¢c community and later
extended by the discovery of archaebacteria as an independent group of prokaryotes distinct from eubacteria and
cyanobacteria [99,100].
The concept of a bacterial species, however, is still open
to discussion. Since prokaryotes do not have the same
form of sexuality as higher organisms, of which species
are de¢ned as groups of interbreeding natural populations
that are reproductively isolated, a bacterial species has
been regarded as ``a collection of strains that share
many features in common and di¡er considerably from
other strains'' [101]. This de¢nition is unsatisfactory because it remains in the opinion of the taxonomist to de¢ne
a new species. It is known that bacteria can exchange
genetic material even over large phylogenetic distances,
but the extent to which homologous recombination between host and foreign DNA takes place di¡ers strongly.
In modern bacterial taxonomy, morphological characteristics, which dominated the classi¢cation in the past century, are of minor importance. The weight of the genomic
characterization has increased over that of the chemical
composition of cell constituents, e.g. the components of
the cell wall and metabolic products and pathways. It is
recommended that strains which share at least approximately 70% nucleotide sequence identity and a di¡erence
of less than 5³C in the melting point of DNA/DNA duplexes belong to the same species [102]. This level of sim-
235
ilarity leaves room for genomic and phenotypic di¡erences
due to the di¡erent life history of the strains, but simultaneously allows the combination of these strains in a species, which has for practical purposes enough common
features. There are several reasons for not changing the
present classi¢cation of prokaryotes on the basis of a rigorous use of this species de¢nition: (i) not enough data on
strain diversity and interspecies relationships are available,
(ii) di¡erent criteria have been applied to identify species,
(iii) very closely related strains are for diagnostic purposes
still separate species, e.g. in the group of enteric bacteria,
and (iv) evolutionary systematics, as proposed by C. Darwin, is the only way to come to a `true natural system' of
bacteria.
An increasingly robust map of evolutionary diversi¢cation has been compiled, and the progress in the construction of phylogenetic trees on the basis of true DNA/DNA
homologies is impressive. The recognition of Archaea as a
distinct kingdom of organisms has in£uenced thoughts on
the evolutionary relationships among living organisms.
This phylogenetic classi¢cation will be the ¢nal objective
of systematics, although at present there is no general
agreement about the domain concepts of C.R. Woese
(Bacteria, Archaea, Eukarya), the ¢ve-kingdom classi¢cation of L. Margulis (Prokaryotes [Monera], Eukaryotes
[Plants, Animals, Fungi, Protists]), or the division of prokaryotes in Monodermata, having a single `cell membrane'
(Gram-positive) and Didermata, having two `cell membranes' (Gram-negative) [103]. The important role of prokaryotes in the evolution of life seems to be evident, but
the origin of the di¡erent groups of eukaryotic and prokaryotic organisms and their evolutionary relationship remains open to further studies. The same is true for the
species concept for bacteria. A phylogenetic classi¢cation
is the ¢nal goal, but an arti¢cial classi¢cation is still in use,
even though we know that markers such as phototrophy,
autotrophy, pathogenicity, and methanogenesis are not
characteristic for a phylogenetic group [102,103].
6. Spontaneous generation vs. evolution of microorganisms
The hypothesis of spontaneous generation of living
beings from the elements or from putrefaction, decaying
organic matter, and humidity was an old belief described
by Aristotle and other philosophers and poets of antiquity
that occupied the attention of many scientists over the
centuries and adhered to a wide spectrum of philosophical
views until modern times [1,3,4,27,29,35,104]. All proponents of spontaneous generation believed that living entities can arise suddenly by chance from inorganic matter
(abiogenesis) or from organic matter, which was itself derived from organisms (heterogenesis), independently of
any parents. Vitalists deny any possibility of abiogenesis
by chance, while others, following the universality of
strictly deterministic natural laws in the mechanistic phi-
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losophy of R. Descartes, believed in the abiogenetic way
of spontaneous generation. The doctrine of spontaneous
generation has long been considered as an inhibitor of
scienti¢c progress. It will be shown here by a few examples
that the controversial discussion on this theory became
¢nally a driving force of scienti¢c progress because it initiated numerous experiments and resulted in new concepts
and experiments [27].
The extensive studies on the anatomy of higher and
lower plants and animals in the 17th century revealed
that animals and plants developed from eggs and semen.
Francesco Redi (1626^1697) discovered that putrefying
matter is not the material from which animals generate,
but a substrate on which animals deposit their eggs. He
observed that £ies lay their eggs on £esh and that maggots
generate from eggs, and £ies from maggots. Leeuwenhoek
was convinced that no living things came from putrefaction, but that they derived from those created in the beginning [4]. He studied the development of insects and
vermes from eggs. From his results the following questions
arose: (1) is air needed to support life?, (2) do all animals
come from eggs?, and (3) can seeds and eggs survive for
inde¢nitely long periods? [1,4].
Leeuwenhoek rejected the idea of spontaneous generation also for the microscopic organisms and believed that
the animalcules were distributed by air in the form of
seeds or germs, but he did not prove this hypothesis [4].
The distribution of germs by air was a controversial issue
in the 19th century. Louis Joblot (1645^1723) also denied
the doctrine of spontaneous generation, and this standing
was considered to be contrary to all reason and religion.
He experimented with heated infusions to see whether they
could produce animalcules. He boiled fresh hay and distributed the infusion into two vessels, one of which was
closed and the other was left open. After a considerable
time he observed animalcules only in the open vessel [105].
Like Leeuwenhoek, he believed that the eggs of animalcules were carried by air into the uncovered vessel. John
Turberville Needham (1713^1781) performed similar experiments, but he used closed and open vessels in which
he heated meat extract. In both vessels a dense population
of organisms was observed after several days of incubation. Needham repeatedly observed that after heating different kind of infusions and careful closing to avoid contamination from air, innumerable ¢laments swelled from
an internal force and became perfect zoophytes or microscopic animalcules [106]. He and also Bu¡on concluded
that in each living material is a vegetative force ^ a universal semen that can initiate new life in any organic substance. Bu¡on developed the idea that vitality is an indestructible property of living things [107].
Abbë Lazzaro Spallanzani (1729^1799) observed in infusions a sequence of di¡erent animalcules. In numerous
experiments, he showed that heating prevents the appearance of animalcules in infusions if the £asks are sealed
hermetically and the air in the bottle did not contain ani-
malcules. He found that the heating period required to
render an infusion sterile is variable, and he concluded
that Needham's infusions were contaminated by air
[108]. Needham commented that in Spallanzani's experiments, the prolonged heating destroyed the vegetative
force and modi¢ed the air. In response to Needham's objections, Spallanzani repeated his experiments and concluded that animalcules developed in £asks that were
corked, but not in hermetically sealed £asks that were
heated for 0.5^2 h. He also did experiments with £asks
having capillary necks to avoid diminishing the `elasticity
of the air', as accused by Needham. Two types of animalcules were described : those of superior order, which were
easily destroyed in 30 s at 100³C, and the other exceedingly minute organisms that sometimes survived boiling
for 30 min. He also showed that boiling water is much
more e¡ective in sterilization than hot air and that boiling
media for long periods did not prevent growth of animalcula [108,109].
The opposition to Spallanzani and like-minded people
rested on the adherence to the traditional 18th century
mechanistic concept of spontaneous generation. Opponents of spontaneous generation were faced with the problem of the generalization of an experimental result: the
statements that all organisms arise from parents or that
no organism arises spontaneously from matter can be disproved for one organism, but neither can be proven with
absolute certainty. Moreover, Spallanzani had several limitations; most importantly, his microscope was insu¤cient
to see bacterium-sized objects. He attacked the doctrine of
spontaneous generation from an a priori belief in the hypothesis that all living things arise from parents. Thus, the
experiments of Spallanzani and the critical thoughts of
Leeuwenhoek did not convince the adherents to the doctrine of spontaneous generation of animalcules, and the
doctrine remained a widely held belief and was supported
by many biologists, such as O.F. Mu«ller, Treviranus, Lamarck, Ku«tzing, and Dujardin far into the 19th century
[27,35,36]. Although cell biologists and histologists provided more and more examples of organisms that arise
from parents and argued by analogy that all living things
were produced in the same way, the doctrine survived in a
transformed view. Lamarck believed that spontaneous
generation is necessary in order to understand the discontinuities in fossil records and the evolution from the lower
forms on the escalator of life to the more complex higher
organisms [104].
The spreading of microorganisms through the air was
very often thought to be a source of contamination. F.
Schulze [110] gassed heat-sterilized infusions with air
sucked through concentrated sulfuric acid. No growth of
organisms was observed until the vessel with the infusion
was exposed to open air. Felix-Archime©de Pouchet and
Hughes Bennet, however, observed growth in the apparatus described by Schulze. J. Tyndall (1820^1893) noticed
that the air has to pass slowly through the sulfuric acid;
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otherwise, the gas bubbles could transfer microorganisms.
Theodor Schwann (1810^1882) designed an apparatus
consisting of a £ask that contained an infusion sterilized
by boiling. Air was conducted through a heated glass tube
before reaching the infusion. Such £asks kept for 6 weeks
did not show any growth of microorganisms, but after
opening the £ask, the infusion became putrid. Schwann
concluded that the germs or seeds of infusoria in the air
were destroyed by heat. In the same apparatus, the £asks
were ¢lled with boiled sugar solution and yeast. In £asks
with unheated air, the sugar was degraded, alcohol was
formed, and the yeast cells grew ([35], pp. 86^87). A new
principle of air sterilization was introduced by H.
Schro«der and T. von Dusch [111]. They ¢ltered air
through cotton-wool before passing it through the infusion. The ¢lter trapped the germs, and no growth was
observed in the heated infusion. Although these and other
scientists showed experimentally that no animalcules developed in boiled infusions and therefore no spontaneous
generation occurs if the air is free of germs, the number of
opponents did not decrease.
One of the opponents was F.A. Pouchet (1800^1872),
who began his experiments with the aim of proving spontaneous generation. He believed that life was generated by
a vital force coming from pre-existing living matter (heterogenesis [27,112]). According to his theory, the main
factors of heterogenesis are organic matter, water, access
of air, and a suitable temperature. He repeated the experiments of Schwann and Schulze, but obtained contrasting
results. At this time, Louis Pasteur (1822^1895) extracted
germs from the cotton-wool after ¢ltration of air and observed them under the microscope, thereby demonstrating
that germs are distributed through air [63]. The presence
and distribution of microorganisms in the air was also
studied in Cohn's laboratory. In a simple set-up, air was
sucked through a previously sterilized medium. The aerated medium was incubated at di¡erent temperatures, and
the growing fungi and bacteria were studied microscopically [113]. Mi£et showed that the number and type of
microorganisms growing in the aerated media were dependent on the source of air (laboratory, garden, or open
¢eld). Similar experiments were performed by Pasteur
and coworkers, who showed that air in the mountain region of the Alps at 2000 m altitude contained far fewer
germs than air in locales in Paris [63,104,114]. Pasteur also
concluded that alkaline infusions required a higher temperature or prolonged periods of boiling to destroy the
germs than acidic infusions [104,114,115]. In order to
avoid contamination, but to allow access of air to the
infusion, he used £asks with a neck that had been heated
and pulled out into a capillary and bent several times: the
boiled infusion in these £asks remained sterile. The spontaneous-generation proponent Pouchet did not give up. He
conducted an extensive series of experiments similar to
Pasteur's, but again came up with contrasting results. Finally, a commission of the Academy of Sciences, which
237
was prejudiced, decided the discussion in favor of Pasteur.
It was not seriously considered that Pasteur worked with
yeast extract or other de¢ned media, while Pouchet used
hay infusions. Pasteur refuted the doctrine of spontaneous
generation not only because of the results of his sterilization experiments, but also because of preconceived ideas
that speci¢c fermentations, such as butyric, alcoholic or
lactic acid fermentation, are caused by speci¢c microorganisms even when no oxygen is present and because of
his anti-materialistic belief in a Creator God [63,64,104,
114^117].
The heterogenists and others continued to carry out
di¡erent types of experiments to prove or disprove spontaneous generation [1,27,29,35,104]. Charlton Bastian
(1837^1915) was not convinced that germs were transferred through the atmosphere, and he opposed the theory
that diseases are caused by parasites. His experiments
showed that some germs may be much more thermoresistant than had been previously supposed. The practice of
heating liquids to 115^120³C for sterilization was introduced by Pasteur and Chamberland. Chamberland developed the autoclave and in 1884, a ¢lter made of porous
porcelain to remove all microbes from water [27,35].
John Tyndall (1820^1893), a great experimenter and ingenious thinker, was an opponent of spontaneous generation. He developed a method to make particles in air
visible using light scattering and compared the infectiousness of the particle density in air with the growth density
in the culture vessels in his apparatus. He observed that
the `power of air' to develop life in sterile media paralleled
its capacity to scatter light. Air from which all particles
were sedimented was shown to be sterile [118]. He concluded that air is a carrier of germs. Tyndall observed, as
W. Roberts [119], F. Cohn [76,82], and Eidam [120] did,
that neutralized hay infusion withstands long-term boiling.
He concluded that bacteria have phases of development ^
one phase is relatively thermolabile and is destroyed by
heating at 100³C in 5 min, whereas the other phase, which
was regarded as the germ of the bacterium, is thermoresistant to boiling temperatures [121]. F. Cohn discovered
in the same year that the heat-resistant phase in the development of the hay bacillus is the endospore (Fig. 1). He
described the whole life cycle of Bacillus subtilis and the
formation and germination of endospores by detailed microscopy studies [82]. On the basis of his results, Tyndall
elaborated the important method of fractional sterilization, known today as tyndallization [121]. By this method,
vegetative and heat-sensitive stages of bacteria are killed
by boiling of the suspension. After a certain period, which
is necessary for the heat-resistant germ to pass into a heatsensitive state, the infusion was boiled a second time. Tyndall determined the time for the interval and the number
of repetitions necessary for complete sterilization. The results of Cohn and Tyndall explained many of the controversial results of the advocates and opponents of the doctrine of spontaneous generation, especially the observation
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that hay infusion, which very often contains heat-resistant
spores, resists boiling.
If infusoria are not generated spontaneously from organic matter, how are they originated and propagated ?
After publication of Darwin's The Origin of Species in
1859 and the increasing evidence of earlier periods of life
on earth, the concept that organisms share a common
origin and subsequently diverged through time was slowly
adopted by scientists. However, Darwinism revived the
discussion on spontaneous generation, although it was restricted to the question of the beginning of life and the
origin of microorganisms. In France, Darwinian evolution
was regarded as a doctrine allied with the forces that
threatened church and state [104]. Ray Lankester in England believed that abiogenesis was a necessary and integral
part of the universal evolution theory [27]. The discussion
on how the archetype of organisms originated on Earth is
still open.
Ernst Haeckel, one of the early propagandists of Darwin's theory, constructed various phylogenetic trees of organisms [31]. Phylogeny, a term coined by Haeckel, is the
attempt to reconstruct the evolutionary history of life.
Haeckel divided the organisms into three main groups:
animals, plants, and protists. Since the knowledge about
bacteria at this time was very meager, Haeckel included
them in the collective term infusoria. Cohn, who likewise
was convinced of the theory of evolution, speculated that
the ¢rst living germs arrived from other planets and that
all organisms evolved from these primitive organisms ^
new heritable varieties originated and were separated in
speci¢c habitats by natural selection. He proposed that
the phycochromaceen were early inhabitants of the Earth
because of their ability to adapt to extreme habitats, their
simple way of reproduction, and the fossil records [76,79^
81,84,85].
Over much of the next century, biologists' interest in
phylogeny was minimal, but it was rekindled with the
accumulation of new phylogenetic data from the ¢eld of
molecular biology. The development of DNA and RNA
sequence technology and of mathematical methods to
compare conserved sequences in rRNA and proteins revolutionized evolutionary and phylogenetic biology, especially of bacteria, which developed from an area receiving
little attention to one playing a central role in the phylogenetic tree ¢rst proposed by Carl Woese and coworkers
[99,100]. The concept of the prokaryotes and the eukaryotes as two groups of organisms, each of which comprises
a large evolutionary diversi¢cation [99], was largely con¢rmed and later extended to a tripartite classi¢cation of
Bacteria, Archaea, and Eukarya [99,100]. The concept of
Cohn [76,84,86] that cyanophyceae (now cyanobacteria)
are related to bacteria was supported by the concept of
the prokaryotic cell [98]. Cyanobacteria were recognized as
one of the nearly 20 main lines of descent in the domain of
Bacteria [101]. The phylum cyanobacteria and the chloroplasts, which were proposed to derive from endosymbiotic
cyanobacteria, have a complex phylogenetic structure
[122]. The three groups of organisms ^ eubacteria, archaebacteria, and eukaryotes ^ are now generally accepted as
major phylogenetic branches of the tree of life. Woese and
Fox [99] proposed the progenote as a primitive hypothetical ancestor of prokaryotes and eukaryotes. However, the
unraveling of the true evolutionary relationships of the
three kingdoms remains a matter of speculation and further studies [123^126].
Archaebacteria have, besides their own typical features,
markers which are characteristic of eukaryotes or eubacteria [103,126,127]. It has been discussed whether they are
polyphyletic and relatives of Gram-positive bacteria [103].
Some physiological attributes, e.g. molecules of the photosynthetic apparatus, are distributed throughout taxa that
are phylogenetically not closely related. However, the photosynthetic apparatus seems to have evolved only once
[128^130]; the genetic information for their components
possibly spread by lateral transfer to di¡erent phylogenetic
groups. Anoxygenic photosynthesis ¢rst developed about
3.5 Gyr ago; oxygenic photosynthesis dominated about
2 Gyr ago [128,129]. For recent literature on the evolution
of microorganisms, see [103,126,131^135].
7. The concepts of biological diversity of bacteria
The end products of metabolic processes, such as alcohol or lactic acid, have been known since ancient times,
but they were not traced back to the activities of microbes.
In the 19th century, the understanding increased that not
unde¢ned vital forces, but organisms can metabolize organic and inorganic substrates. This insight was based
mainly on the progress in chemical analysis and the observation under the microscope of microorganisms in fermenting, putrefying, and infectious organic material, and
was also supported by an increase in rational experimental
analysis in biology.
7.1. The organismic and chemical theories of fermentation
For a long time, chemists dominated who proposed that
fermentation is caused by a spontaneous internal transformation of organic material ([29], p. 23) or by a `ferment'
(`Ga«hrungssto¡') [136,137]. Lavoisier quantitatively
studied alcoholic fermentation. He concluded that the sugar was split into an oxidized portion (carbon dioxide) and
a reduced portion (alcohol) [138]. Gay-Lussac observed
that oxygen is necessary to start fermentation, but not
for its continuation [139]. The hypothesis that fermentation, putrefaction, and contagiousness are the result of
some spontaneous chemical change in the organic matter
or tissues (microzymas) and that microorganisms are just a
product but not the causative agent of disease and fermentation [35] was proposed by Liebig [136,137] and Bëchamp
[140].
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Yeast was considered by Berzelius as a catalyst, like
platinum, which was not transformed during fermentation.
Liebig postulated that the `ferment' is produced from
`Kleber' (gluten) by oxidation with the oxygen from water
[136,137]. G.V.M. Fabbroni [141] suggested that the decomposition of sugar during fermentation is caused, in
absence of oxygen, by a vegetative-albumenoid substance.
Caniard de la Tour (1777^1859), Theodor A.H.
Schwann (1810^1882) and Traugott Ku«tzing (1807^1893)
were the ¢rst to propose independently of each other that
alcoholic fermentation is a biological process and that
yeast is a reproducing, living thing (sugar fungus, Saccharomyces) [142^144]. Schwann and Ku«tzing described yeast
in detail. Liebig and Wo«hler anonymously published a
persi£age of the theory of fermentation caused by living
cells [Annalen der Pharmazie 24 (1839) 100]. In a serious
article, Liebig [137] described fermentation, putrefaction,
and decomposition as processes attributed to the instability of certain substances, which are able to communicate
their instability to other substances in succession. He
called these unstable, nitrogen-containing substances `ferment', which he believed arose as a modi¢cation of a
vegetable saccharine solution exposed to air; the fermentation continued in the absence of air. The chemist Mitcherlich concluded from his own observation that yeast is
essential for fermentation, but acts by contact, following
the catalytic theory of Berzelius [145].
Louis Pasteur (1822^1885) took a great step forward in
research on fermentation by studying not only the substrate and the products of growth and fermentation, but
also the organisms in the fermentation broth. He investigated the formation of lactic, butyric, acetic, and tartaric
acids and of alcohol [64,114^117] and observed anaerobic
life by butyric acid fermentation [64]. In the book Etudes
sur la Bie©re [116], Pasteur summarized and extended his
work on fermentation and life without oxygen. The modern view that yeast might ferment sugar through the production of a soluble ferment or enzyme was proposed as
early as 1858 by Moritz Traube [146]. Finally in 1897,
Eduard Buchner (1860^1907) isolated `zymase' from yeast
juice which catalyzed the formation of alcohol from sugar
[147]. He opened the door to the fruitful studies of the
biochemistry of enzymes, cofactors, and enzymatic processes in the 20th century.
This short overview on the history of fermentation
shows that the concepts of catalysis and species-speci¢c
metabolic capacities of microorganisms, experimentally
proved by new analytical and microbiological methods,
paved the way for modern research of this ¢eld. The multitude of theories, their controversial discussion, and new
experimental approaches accelerated the progress.
7.2. Autotrophy, chemolithotrophy, and phototrophy
Autotrophy, i.e. growth of organisms with carbon dioxide as the only carbon source, was discovered in green
239
plants by Jan Ingenhousz (1730^1799) and Nicolas Thëodore de Saussure (1767^1845) [148^150]. The term autotrophy was introduced by Wilhelm Pfe¡er [7]. Ingenhousz
showed that plants in the presence of light absorb carbon
dioxide and liberate oxygen and that the CO2 is used for
nutrition [148,149]. Saussure determined quantitatively the
increase of the plant dry weight and the decrease of CO2
during the day in correlation with the light intensity, and
he observed that during the night, oxygen is consumed
and CO2 is released [150]. Liebig, Boussinggault, and
Sachs studied the nutritional physiology of plants grown
in a pure mineral solution [19,151]. The term photosynthesis for the light-induced assimilation of CO2 was coined
late in the 19th century. Research on oxygenic (oxygenproducing) photosynthesis increased very slowly, yielding
some important results in the middle of the last century
(e.g. chloroplasts as the site of photosynthesis, and starch
as the product [151]), and culminated in the 1960s with the
discovery of the CO2 -¢xation cycle, the water-splitting system in photosystem II, and the generation of the protonmotive force by light-driven electron transport [152]. After
the discovery of photosynthetic CO2 ¢xation, it was believed that oxygen is generated by the splitting of CO2 ; the
origin of oxygen from water was not discovered before
1941 [153].
Autotrophy and photosynthesis were discovered much
later in bacteria than in plants and algae. For many decades, CO2 ¢xation was assumed to be restricted to plants
[76]. Pigmented, bacteriochlorophyll (bacteriopurpurin)containing bacteria have been described since the 1830s
by Cohn, Ehrenberg, Esmarch, Perty, Warming, Winogradsky, Zopf and others [38,76,81,92,154^157]. Wilhelm
Engelmann (1843^1909) investigated the in£uence of
the quantity and quality of light on the movement (photokinesis) and phototaxis of these bacteria [155^157]. He
was the ¢rst to conclude from growth experiments with
these bacteria under anoxic conditions in the light that
the `purple schizomycetes' assimilate CO2 like the green
plants and that they are able to transform the absorbed
light energy into chemical energy [157]. Twenty years
passed before the anoxygenic type of bacterial photosynthesis was con¢rmed by Molisch [154]. Engelmann was not
sure because he had contradictory results and was possibly
convinced that oxygen liberation is connected with CO2
assimilation.
In 1877, T. Schloesing and A. Mu«ntz observed the bacterial oxidation of ammonia to nitrite and nitrate. R. Warington found that this is a two-step process. Nikolaevitch
Winogradsky (1856^1953) isolated the nitrifying bacteria
and discovered that the oxidation of ammonia to nitrite by
Nitrosomonas and the oxidation of nitrite to nitrate by
Nitrobacter yielded free chemical energy, a process which
has been named chemolithotrophy [95^97]. He also observed that these bacteria can grow with CO2 as the
only carbon source. Thus, these bacteria are chemolithoautotrophs.
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Cohn described the presence of hydrogen sul¢de in stagnant water bodies and the formation and degradation of
sulfur droplets in Beggiatoa (Fig. 2). Erroneously he concluded that Beggiatoa is responsible for the synthesis of
H2 S [66]. The oxidation of hydrogen sul¢de to sulfur and
sulfuric acid under microaerophilic conditions in Beggiatoa was demonstrated by Winogradsky [158]. The reduction of sulfate to sul¢de by Bacterium desulfuricans was
¢rst described by M. Beijerinck [159].
In 1885, H. Hellriegel (1831^1895) and H. Wilfarth discovered the ¢xation of dinitrogen in root nodules of leguminous plants, and they showed that the combined nitrogen compounds formed in the nodules were supplied to
the plants. The causative bacteria were isolated and described by Beijerinck [160]. The reduction of N2 to ammonia by the free-living, aerobic bacterium Azotobacter
chroococcum was shown by Beijerinck and van Delden
[161,162], and dinitrogen ¢xation by the anaerobic bacterium Clostridium pasteurianum was discovered by Winogradsky [163]. Dinitrogen ¢xation by phototrophic bacteria
was detected in cyanobacteria by G.E. Fogg in 1942 and
in purple bacteria by H. Gest in 1950. These important
results and the progress in the analysis of fermentation
and oxidation/reduction processes led to modern concepts
of metabolism in the 20th century, e.g. the unifying theory
of microbial metabolism proposed by Albert J. Kluyver
[164,165].
7.3. Putrefaction and pathogenicity of bacteria, and
immunology
Putrefaction was always observed as a process of decay
of organic material, a source of unpleasant odor, and a
possible cause of disease in man and animals. The exact
nature of the putrid process was, however, for a long time
a matter of speculation because no experimental approach
was available [1,14,35,36,166]. In the second part of the
19th century, growth experiments using selected and de¢ned media with cultures of microorganisms enriched in
one species revealed that microorganisms have speci¢c,
inheritable features for the production of pigments or fermentation products or for the oxidation of inorganic compounds. Putrefaction was traced back to the activity of
bacteria able to decompose nitrogen-containing organic
material. The standpoint of Liebig, that putrefaction is a
rearrangement of molecules, was refuted [76,116]. Four
possibilities for the mechanism of putrefaction were discussed by Cohn [76]: (i) bacteria assimilate proteins and
transform them into their own cell material ; (ii) bacteria
produce and excrete a ferment-like compound which solubilizes and decomposes protein (like barley grains, which
produce diastase, which splits starch into sugar); and (iii
and iv) bacteria oxidize or reduce protein enzymatically
with oxidizing or reducing ferments. It was concluded
that pigmented bacteria or other bacteria split protein
molecules after uptake directly or by excreted ferments
into ammonia and other compounds and assimilate ammonia as nitrogen source [76].
7.3.1. Bacteria as contagion
The process of putridity was more and more associated
with the idea of sepsis as a cause of septicemia, pyemia,
and putrid infection. B. Gaspard administered putrid material to experimental animals and observed the development of symptoms. The nature of pyemia and septicemia,
however, remained a mystery [35]. The pathological e¡ects
of putrid infections on the cellular level were described by
Virchow [167]. He and other scientists studied the e¡ect of
dose on the symptoms of septic shock, intoxication, abscesses, and cytopathic modi¢cations of tissues [36,166^
168]. Koch [14,69] investigated the histology of infected
tissues, and he examined with a microscope ¢tted with
an oil-immersion lens system and an Abbe condenser the
germs in slide preparations stained with aniline colors. He
stressed that each type of infection resulted in a characteristic histological picture caused by the microorganisms
speci¢c for the illness; the bacterial causative agent had
to be isolated from the tissue [14]. Several scientists, such
as E.v. Bergmann (1868), Hiller (1879), and Blumberg
(1885), were opponents of the germ theory of putrefaction
and proposed that putrefaction is caused by toxic compounds [35,36]. The observation of vibriones (Treponema
pallidum) in syphilitic pus and Trichomonas vaginalis in the
vagina by Donnë, the detection of the anthrax bacillus by
C.J. Davaine [169], the description of a mold, called Botrytis bassiana (Beauveria) as a causative agent of a silkworm disease by A.M. Bassi [170], and other observations
motivated Jacob Henle (1840) to reactivate the germ
theory of disease and to study infectious diseases [62].
This was at about the same time that Pasteur's studies
revealed speci¢c microorganisms as the causative agents
of di¡erent fermentations.
The numerous cholera epidemics, the observations of
Davaine on anthrax, of Traube (1864) and E.K. Klebs
(1869) on urethritis and nephritis, of Rind£eisch (1869)
on a¡ections in the heart muscle, the demonstration of
Borrelia recurrentis only during an attack of fever in the
blood of patients su¡ering from relapsing fever by
O. Obermeier [171], and other observations on infected
tissues [172] stimulated E. Hallier (1831^1904) to isolate
and cultivate germs from infected tissues in his culture
glass [173,174]. Unfortunately he interpreted the germs,
isolated from humans and animals infected by cholera,
typhus, gonorrhea, diphtheria, and pox virus, as forms
of fungi (polymorphism). This incorrect interpretation
was rejected by the mycologists de Bary and Brefeld and
bacteriologists such as Cohn, Rind£eisch, and BurdonSanderson [35,36]. In spite of the inconsistent results of
the numerous observations, the view that bacteria and
other microorganisms may be the causative agents of the
diseases received increasing consent ([36], pp. 86^103).
The crucial experiments showing that one distinctive
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species causes a speci¢c infectious disease were performed
by Robert Koch (1843^1910). The decision to select anthrax for the ¢rst series of experiments was fortunate because the infected tissues contain numerous bacilli (Bacillus anthracis). Koch isolated the bacteria from an animal
that died of anthrax and set up cultures in a moist chamber, where the growth, division, and sporulation of the
bacilli were observed with the microscope and documented
by microphotography, which was developed by Koch [12].
In the decisive experiment, it was shown that B. anthracis,
isolated from the diseased animal, and not Bacillus subtilis,
caused anthrax in mice. Koch wrote to Cohn, who was at
this time an internationally recognized authority in bacteriology, that he would like to demonstrate his results in
Cohn's laboratory. The demonstration of his decisive results in Cohn's laboratory in Breslau in the presence of
Julius Cohnheim and Carl Weigert, both pathologists in
Breslau, was an important step in the progress of infectious biology and the ¢rst proof that distinct bacterial
species can cause a disease with typical symptoms. The
results were published [94] after Cohn's article on the sporulation of B. subtilis [82] in the journal Beitra«ge zur Biologie der P£anzen, founded by Cohn. The experimental
proof of infectious disease, later described as Koch's postulates, was the beginning of modern medical microbiology [13,35,36]. The postulates comprise the isolation of the
microorganism from the infected tissues, the growth of the
microorganism in pure culture using the plate and slide
technique [69,175], the improved methods of observation
using microscopy, staining and documentation of the bacteria [10,12,175], the achievement of the typical symptoms
of the disease by inoculation of the isolated bacteria into a
sensitive host [176^178], and the isolation of the same
microorganism from the newly infected host. The ¢rst
success was followed by the discovery of Mycobacterium
tuberculosis as the causative agent of tuberculosis
[177,178]; of Corynebacterium diphtheriae, which causes
the toxigenic disease diphtheria [179]; and of Vibrio cholerae, which causes cholera [180]. A. Ogston, using Koch's
technique to isolate and determine the number of micrococci in pus, cultivated cocci in glass cells with Cohn's or
Pasteur's £uid under oxic or anoxic conditions and concluded that Streptococcus (Rosenbach) and Staphylococcus
cause in£ammation and suppuration [181,182]. Rosenbach
[172] subdivided the genus Staphylococcus into species. In
summary, the development of several new techniques and
the concept that speci¢c infectious diseases are caused by
distinct species of bacteria having inheritable virulence
factors were the prerequisite for placing research on the
etiology of infectious diseases on a valid scienti¢c ground.
7.3.2. Control of infectious diseases
While Koch and his coworkers and disciples were concentrating on the isolation and characterization of parasitic and saprophytic bacteria, the French school under the
guidance of Pasteur was directed toward the prevention of
241
infectious diseases. By repeated passages of pathogenic
germs on arti¢cial media at high temperatures (42³C), in
non-host animals, or in speci¢c tissues, they obtained bacteria with attenuated virulence. These attenuated cultures
were used to inoculate animals or humans. The vaccinated
individuals were shown to be resistant to the virulent
strains of fowl cholera, anthrax, swine erysipelas, or rabies
[183^186].
7.3.3. Disinfection
The observation that carbolic acid inhibits growth of
microorganisms and the formation of pus in wounds
[187] and the numerous observations that microorganisms
cause fermentation, putrefaction, and infections stimulated
Joseph Lister (1827^1912) to develop the antiseptic system
[188,189]. He worked out procedures for treating wounds
with phenolic compounds that were generally accepted
and introduced into the medical practice after a long period of uncertainty. Koch and others tested many other
disinfectants [190,191].
7.3.4. Immunology
From studies on the interactions of warm-blooded
bodies with inoculated parasites and the successful ¢ght
against infectious diseases, research in the large ¢eld of
immunology was initiated and the theories of humoral
and cellular immunity were developed [29,35]. E. Metchniko¡ (1845^1916) studied phagocytosis [192], and E. von
Behring (1854^1917) and S. Kitasato (1852^1931) detected
the antitoxins against infections of Clostridium tetani and
Corynebacterium diphtheriae [193]. Paul Ehrlich (1854^
1915) published important articles on toxins and antitoxins and their standardization and on the speci¢city of antibodies against antigens [194,195]. The extreme complexity
of the immune system was revealed at the end of the 19th
century.
8. The achievements of Ferdinand Cohn
Ferdinand Cohn was born on January 24, 1828 in Breslau, now Wroclaw, into a Jewish family. His life-long
interest in history and the classical languages Latin and
Greek was born during his education at the Maria Magdalena Gymnasium (Fig. 3). After the ¢nal examination at
this Gymnasium he began his studies of natural sciences
with the main subject botany in Breslau in 1844 (Fig. 4).
Cohn continued his studies from 1846 to 1849 in Berlin
because his application for admission to the doctoral examination at the university in Breslau was refused because
of his Jewish faith. He received his doctoral degree in
Berlin on November 13, 1847 at the age of 19. In 1849,
Cohn returned to Breslau full of ideas for studying developmental cell biology, especially of lower plants and microorganisms by means of microscopy methods. He completed his Habilitation (second dissertation) in October
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
Fig. 3. Maria-Magdalenen Gymnasium in Breslau at 1867, the high school of Ferdinand Cohn, destroyed during World War II, now replaced by a
hotel opposite the Maria-Magdalenen church. From: Unbekanntes Portra«t einer Stadt, catalogue of an exhibition, by Iwona Binkowska and Marzena
Smolak, translated by Jerzy Pasieka, Muzeum historyczne we Wroclawiu, Ratusz wroclawski 1997.
1850, became a lecturer (auMerplanma«Miger Professor) on
April 2, 1857, and an associate professor on July 30, 1859.
He married Pauline Reichenbach in 1866, and was appointed full professor on April 17, 1872 (Fig. 5). In
1866, he founded the Institute of Plant Physiology and
established a research group (Fig. 6). A new building for
plant physiology, a herbarium, and a museum of botany
were constructed in the botanical garden of the university
and were opened in 1888 (Figs. 7 and 8). Cohn died on
June 25, 1898 (Fig. 9). The details of his career have been
described recently [79,196].
Cohn contributed to a broad ¢eld of topics in biology.
His reserve in self-representation and his modesty may be
the reason why his name is at the present time much less
known than that of Koch and Pasteur. Cohn's major ¢eld
during his studies in Breslau and Berlin was botany. In
Berlin he received a decisive intellectual stimulus for his
subsequent research. His studies on plant cells and on the
Fig. 4. The main building of the university of Breslau (north side), alma mater Viadrina, founded by Leopold III, picture taken about 1867, published
in, see Fig. 3.
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
243
Fig. 5. Letter of appointment of Ferdinand Cohn as full professor. Text translated: Your Honorable is informed by order of the Mr. Minister of Intellectual A¡airs, most devoted, that in instance of the philosophical faculty your Majesty, the emperor and king has signi¢ed his pleasure, to appoint you
as full professor in the philosophical faculty of this university. With my best congratulations, I send herewith the at April 17 by his majesty accomplished appointment, and request you, for the purpose of an imprint, to give the carrier 15 Sgr. You will receive a further order for the suitable increase of your salary. To the royal professor of the university, Mr. Dr. Ferdinand Cohn, right honourable. Transcript of the order is herewith communicated to the philosophical faculty by order of the Mr. Minister of Intellectual A¡airs with regard to the proposal of the 13th March. The royal
curator of the university Con¢dential councillor and president.
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
mental stages of approximately 90 plants should be observed and documented by volunteers throughout the year
at di¡erent places in Silesia. Cohn reported and coordinated the registered changes in the vegetation for many
years [202]. Cohn published important contributions on
the movement of plants induced by external stimuli (light,
chemical, and mechanical) [203^208].
Cohn's comprehensive knowledge in many ¢elds of biology was combined with a deep interest in history and
art. Cohn felt obliged to mediate knowledge of natural
sciences to a wide audience. He was convinced that education in natural sciences was as important as training in
cultural sciences and that scienti¢c thoughts are important
not only for scientists, but also for the general public to
open their minds. He stressed and practised this idea during his entire life. All those who listened to him were impressed by his gifted, clear, rhetorical, and brilliant speech.
His popular description of a broad spectrum of botanical
knowledge was combined in the collected lectures on
plants, which was published in 1882, and in a second,
revised edition in 1897 [209]. The article on `Plants in
the ¢ne arts' [210] presents a retrospect on the description
of plants in art and science during several epochs. In 1856
he gave a lecture in Berlin on the history of gardens.
Fig. 6. The only room with windows of the Institute of Plant Physiology, founded in 1866 by Cohn in an old building of the university. On
the right side in the foreground the sea water aquarium, a kind of enrichment culture, from which many bacteria and protozoa have been
isolated and described; in the background F. Cohn with his coworkers.
From [214].
development and sexuality of algae and fungi established
his early distinction in the scienti¢c community [18,20^
25,56,57,65]. The leading role of Cohn in the evolution
of the principles of modern bacterial taxonomy was described in Sections 4.1 and 5 [66,76,79,81,84^86] and his
comprehensive studies of bacterial physiology were detailed in Section 7 [65,66,76,82,85]. In addition, Cohn
was an important promoter of applied microbiology. He
gave lectures in agricultural botany, advised farmers on
the diagnosis and treatment of plant diseases caused by
fungal infections, became a pioneer in the analysis of
water as one possible source of infectious diseases, and
described in detail the damage to trees by hurricanes
and lightning [80,197^200].
In 1875 on the 50th anniversary of the doctorate of his
mentor Professor Go«ppert, Cohn initiated the work on the
£ora of cryptogams in Silesia and then published the work
in several volumes between 1877 and 1908 [201]. In the
`Schlesische Gesellschaft fu«r Vaterla«ndische Kultur' (the
Silesian Society of National Culture), a type of academy
in which he served as the secretary of the botanical section
for more than 30 years, it was decided that the develop-
Fig. 7. The new Institute of Plant Physiology and Museum of Botany,
opened 29 April 1888. Photographed 25 June 1998.
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
245
One of the postulates that Cohn defended during his
oral doctoral examination was the need for an Institute
of Plant Physiology. During his academic career, he never
neglected this goal, but the realization was impeded by
many obstacles. By his continuous e¡ort, he was allowed
in 1866 to use several empty and dark rooms in the old
convent of the university located in the center of the town
to set up a laboratory of plant physiology (Fig. 6). By
di¤cult and continuous negotiations with the ministers
of agriculture and culture, he received a small amount of
¢nancial support for the costs of the equipment, lighting,
sanitary installation, and the salary of a technician. Very
often, Cohn himself laid out the money and was reimbursed after many months [211^213]. Many students and
scientists came from abroad to study with him and many
of these students later obtained leading positions. The inadequacy of rooms for research and teaching and the need
for a museum of botany ¢nally led, after many years of
planning and discussion, to a successful proposal for a
new building, which was opened with a ceremony on April
29, 1888. The new building, located in the botanical garden, contained the herbarium and the museum, a lecture
room, the Institute of Plant Physiology with laboratories
and the library, the o¤ce for the director of the botanical
garden, and apartments for employees [213]. The building
is still in use (Fig. 7).
Fig. 9. Gravesite of Ferdinand Cohn and his wife Pauline Cohn in the
Jewish Cemetery in Breslau (Wroclaw). The German and Polish texts of
the inscription on the tablet translate as follows: Ferdinand Julius
Cohn, 1828^1898. Botanist and Microbiologist, Pioneer in Modern Microbiology and the Taxonomy of Microorganisms, Founder of the Institute of Plant Physioloy of the University of Breslau (1866), Promoter of
Robert Koch. On the 100th Anniversary of his Death on June 25, 1998
in Breslau. Vereinigung fu«r Allgemeine und Angewandte Mikrobiologie,
Deutsche Gesellschaft fu«r Hygiene und Mikrobiologie, und Gesellschaft
fu«r Virologie, Muzeum Historyczne we Wroclawin.
Fig. 8. Ferdinand Cohn (from [214]).
From the beginning of his career, Cohn communicated
with many of his contemporaries by letter and by personal
contact during meetings and private journeys [214]. During the last decade of his life, when he was no longer at the
forefront of science, he published articles on historical
aspects and overview articles, e.g. on Tabaschir or mandragora [215], the history of botany and botanical gardens
[216^218], Caspar Schwenckfeld [219], and Laurentius
Scholz von Rosenau [220]. Cohn was honored by numerous distinctions from academies, societies, universities, and
his home town Breslau. The German Society of Hygiene
and Microbiology awarded a Ferdinand Cohn medal in
the 1980s. His great personality and his important work
have been illuminated in several articles [35,79,196,212,
221^227].
Cohn was a personality molded by an education in classical art. His Jewish faith and his modesty led him to
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G. Drews / FEMS Microbiology Reviews 24 (2000) 225^249
avoid political activities, although as a student he participated actively in the 1848 revolution in Berlin. His sustained importance in biology was in two ¢elds: the sexuality and development of lower plants and the concept
that bacteria are organisms with distinct, heritable characteristics. He proposed principles of bacterial taxonomy,
knowing that at his time the methodical means to elaborate a modern taxonomy on a phylogenetic basis were not
available. Cohn discovered the development and heat resistance of bacterial endospores.
[23]
[24]
[25]
[26]
[27]
[28]
[29]
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