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Despite challenges, microbial taxonomy is on solid footing because of
international cooperation and widening uses of modern analytic tools
Hans G. Trüper
hree international agreements, the
International Codes on Botanical,
Zoological, and Prokaryote Nomenclature, provide a basis for effective
practices in bacterial taxonomy. Although these agreements were long in coming,
steadily improving means of communication
should make it easier to move toward a unified
nomenclature code for all biological taxa, which
will provide an even stronger basis for future
biodiversity and taxonomy research.
Taxonomy originates in our desire to differentiate among living beings, providing humans
a better means for understanding life around
us. Our very early ancestors, who surely encountered unexpected environmental conditions while
they roamed the continents, needed to determine which animals or plants they could safely
eat, which they had to fear, which they could
T
International agreements provide the current
basis for effective taxonomic practices in biology.
Unlike the Botanical and Zoological Codes the
International Code of Nomenclature of Prokaryotes is based on living type strains that carry
the species names.
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Initial efforts to classify microorganisms depended on the 19th century Botanical Code where
rivalries led to a cross-Atlantic split in approaches
until about 1930, when a new system for microbes
based on living cultures was developed.
Y
Ribosomal gene-based and broader genomicsbased and polyphasic approaches to classifying
microbes suggest a bright and more incisive future
for taxonomics.
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domesticate or cultivate, and which were otherwise valuable to them. Those practical classification schemes were an early form of taxonomy.
Ancient Philosophers and Major Religions
Saw Taxonomy as Stable
The Greek philosopher Aristotle (384 –322 BC)
was among the first to conceptualize the signal
differences between animals and plants while
building a more refined means for classifying
species. In recognizing that there are (at least)
two principally different groups of living beings,
Aristotle characterized the motile ones as animals and the nonmotile as plants. Within the
animals, he assigned individual species to higher
and lower orders, while his student Theophrastos (371–287 BC) started a descriptive botany.
Their classical view of biology prevailed for
many centuries, and was embraced by medieval scholars such as Thomas Aquinus
(died 1274) and Albertus Magnus (died
1280).
Aristotle and other Greeks believed in
spontaneous generation, considering it a
genuine property of nature and one that did
not require involvement of the gods. They
also believed in the constancy of species
without evolution, despite believing that
spontaneous generation continued to happen. In this era, as Judaism and then Christianity spread into Europe, the biblical creation story, in which God produced all
living species within a six-day period about
4,000 BC, came to replace ancient Greek
views about the origins of living beings.
These religious dogmas further strengthened the concept of the constancy of species.
Perspective
International Perspectives on Taxonomy:
from the Past to the Future
Hans G. Trüper is
an Emeritus Professor of Microbiology
at the University of
Bonn, Germany. He
is Chairman of the
Judicial Commission of the International Committee
on Systematics of
Prokaryotes, and a
former president of
the Federation of
European Microbiological Societies
(FEMS). This article
is adapted from a
lecture presented
at the 2004 ASM
General Meeting in
New Orleans, La.
Volume 71, Number 6, 2005 / ASM News Y 273
A more detailed view of biology developed
during the Renaissance when scholars rediscovered the works of the Greek philosophers, and
these efforts continued through the following
period of humanism. Scientists, then called natural philosophers, began to collect and to describe in detail many different plants, animals,
and also fossils, recording their findings mainly
in Latin, which provided a valuable degree of
internationality to these early efforts in the natural sciences.
Microorganisms and, Later, Latin
Nomenclature Enter the Picture
These efforts expanded into another dimension following the development in 1660 by the
Dutchman Antonie van Leeuwenhoek (1632–
1726) of what came to be called the microscope.
He began describing very small but previously
unrecognized living beings that are invisible
to the naked eye. Because of their motility, he
called them “animalcula,” meaning little animals. Some of these animalcula were later recognized to be bacteria.
Large tracts containing botanical and zoological names and descriptions were compiled for
several centuries. To regulate the naming of
biological species, the Swedish physician and
biologist Carolus Linnaeus (1707–1778; also
Carl von Linné) in his Systema Naturae (1735,
with many updates) proposed a binomial Latin
system for naming genera and species. This prerequisite for a meaningful taxonomy became the
basis for our uniform biological nomenclature.
Linnaeus, who strictly adhered to the concept
of the constancy of species, devised systems
for categorizing plants, animals, and—today
it looks strange—minerals. Within the two recognized kingdoms of animals and plants, he
differentiated only four levels: class, order, genus, and species. Of these, he considered genus
the most important level. Strictly on the basis of
morphology, Linnaeus classified and named as
many plants and animals as he could obtain. He
did not accept the classification system, devised
in 1764 by Michel Adanson, that relied on
many different traits and included microscopic
species. Indeed, Linnaeus doubted the value of
microscopy and, citing their “lack of morphological characters,” refused to classify the animalcules described by van Leeuwenhoek and his
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followers. Instead, he placed them in a class of
invertebrate animals that he called “Chaos.”
Although the Linnaean proposals were widely
accepted, that acceptance came amid continuing
strict adherence to the notion that any species,
once created, maintained its constancy. With
this new Latin nomenclature to provide structure and consistency, efforts to classify plants—
including fungi—and animals based purely on
their morphological descriptions increased
enormously.
Ideas about evolution began to take shape
during the early part of the 19th century
through the investigations of Friedrich T. Kützing and Jean-Baptiste Lamarck. A few decades
later, the publication of Charles Darwin’s Origin of Species in 1859 led to a major upheaval in
biology and long-held notions about species
constancy. By now, biologists accept evolution
as the explanation for how new species arise.
By Mid-19th Century, Biology Becomes an
International Enterprise
Even while such fundamental changes were under way, biologists began to convene international conferences to amend and augment the
Linnaeus-based nomenclature systems then at
hand. For instance, the first International Code
of Zoological Nomenclature was approved in
1901 and published in 1903.
Although microscopists meticulously described numerous infusion “animalcules” in the
17th and 18th century, for a long time they did
not attempt to classify them. However, later
during the 19th century, the formal naming of
fungi and bacteria fell under the Botanical Code.
Its early version, called “Laws of Botanical Nomenclature,” was published in 1867 following
the Second International Botanical Congress in
Paris. Despite those efforts, however, national
and personal rivalries split the world community of botanists. Thus, a renegade group several
decades later proposed an alternative naming
system, the “American Code of Botanical Nomenclature,” that included innovations such as
the type rule. These alternative approaches were
not reconciled until 1930 during the International Congress in Cambridge.
Further developments in bacterial taxonomy
came early during the 20th century (see box, p.
275). For instance, during the first half of the
century, neither the fungal nature of bacteria
nor the algal nature of blue-green algae
were held in doubt because both were seen
as part of the botanical system. Bacterial
names that still end with the suffix –myces
remind us that these species were named
according to the rules of that earlier botanical system. Moreover, the myxobacteria
were originally considered to be fungi and
retained that status until the American
mycologist Roland Thaxter (1858 –1932)
recognized their bacterial nature.
Ferdinand Cohn in 1872 described Bacillus anthracis not long after Robert Koch
(1843–1910) identified it as the cause of
the infectious disease anthrax. The very first
pure cultures of bacteria—a new concept—
came from Koch’s laboratory in Germany
and that of Joseph Lister (1827–1912) in
Britain during the 1870s, leading to a burst
in such research, particularly from Louis
Pasteur (1822–1895) and collaborators in
Paris and Koch in Berlin. Between 1880
and 1950 there was a decline of interest in
phylogenetic problems in bacteriology. After 1950, Peter H. A. Sneath in Britain and
R. R. Sokal in Kansas developed phenetic
taxonomy, also known as numerical taxonomy, while W. Hennig in Urbana, Ill., developed cladistic taxonomy around 1966.
Modern Microbial Taxonomy Practices
Emerge
Enormous progress in microbiology occurred as researchers in Europe continued
to isolate and describe new microbal species
of all metabolic categories. These included
the Dutch group led by Martinus W. Beijerinck 1851–1931) and the Russian group led
by Sergei N. Winogradsky (1856 –1953).
Their efforts and contributions from many
others were included in the first edition of
Bergey’s Manual, whose publication was
strongly supported by the International
Committee for Systematic Bacteriology (ICSB),
which was founded in 1930. Bergey’s Manual
eventually outcompeted two rival systems for
classifying microorganisms, one led by François
Prévot in France and the other by Nikolai A.
Krassilnikov in the Soviet Union until the 1950s.
During the first International Congress of
Microbiology, held in Paris during 1930, the
founders of the ICSB concluded that the prevail-
Partial Chronology of Taxonomy, Systematics
for Prokaryotes
Earliest taxonomic descriptions
O. F. Müller, Denmark 1786 (posthumous): genera Monas and
Vibrio.
F. T. Kützing , Germany 1833: Micraloa rosea (syn: Lamprocystis roseopersicina).
C. G. Ehrenberg, Germany 1838: Spirillum volutans, Spirochaeta
plicatilis, Ophidomonas jenensis (syn. Thiospirillum jenense) and
Monas (syn. Chromatium) okenii.
V. Trevisan, Italy 1842: Beggiatoa punctata and Beggiatoa leptomitiformis.
Systematics
O. F. Müller, Denmark 1773–1774: Based on morphology only;
lacked clear distinction between bacteria and protozoa.
F. Cohn, Germany 1872 and 1875: First purely bacterial system,
still based on morphology only. Genera: Micrococcus, Bacterium, Vibrio, Spirillum, Bacillus and Spirochaeta, forming the
higher taxon Schizomycetes, i. e., “fungi dividing by splitting”
(binary fission). First to realize their similarity with certain “bluegreen algae” which he named Schizophycetes, i.e., “algae dividing by splitting.”
K. B. Neumann and R. Lehmann, Germany 1896: Based on
morphology, Atlas of Bacteria.
W. Migula, Germany 1897: Still based on morphology, System of
the Bacteria.
S. Orla-Jensen, Denmark 1909: Predominant use of physiological
criteria to describe bacterial species, The main lines of the natural
system of bacteria.
D. H. Bergey, United States 1923: Bergey’s Manual of Determinative Bacteriology, 1st edition, combined morphology and
physiology and compiled most of the hitherto described species.
ing Botanical Code was no longer adequate
for handling microbial taxonomy. Hence, they
called for establishing an international commission to develop an international code of nomenclature for bacteria. From this commission the
International Union of Microbiological Societies (IUMS)-affiliated ICSB (now the International Committee for Systematics of Prokaryotes, or ICSP) arose.
Volume 71, Number 6, 2005 / ASM News Y 275
Future Critical Tasks in Prokaryote Taxonomy
Keep isolating new species, increase teaching of systematics. At least 3 million prokaryote species may someday be
characterized, named, and classified. A prerequisite for understanding and exploiting this biodiversity is to
continue educating microbiologists to understand taxonomy and systematics, including the international rules of
nomenclature, and to continue to advance the art of isolating and culturing microbes.
Improve taxonomic practices by including genomics and proteomics. Microbial taxonomists need to develop a
better understanding of phylogeny by intensively making full use of genomics and proteomics. For example,
multilocus sequence analyses of genomes should allow taxonomists to identify genetically stable “housekeeping
genes” that will help them to understand internal structures of species and to overcome the species definition
dilemma. Genome-based comparisons could turn out to be a better tool than are ribosomal RNA comparisons for
resolving the key unsettled questions about “Bacteria versus Archaea.”
Include the Cyanophyceae, or Cyanobacteria, under the ICNP. The taxonomy of the Cyanobacteria remains
unsettled, with botanists classifying them as algae (Cyanophyceae, Myxophyceae) under the Botanical Code of
Nomenclature, together with eukaryotic algae, all other plants, and fungi. Yet these organisms are bacteria and
should be classified under the ICNP, following its key principle of preserving living type cultures.
Complete the unified biocode for all species of living and extinct beings. For the sake of biodiversity research,
international taxonomists should continue to develop a unified “biocode,” to ensure that names for biological taxa
are properly assigned. For instance, some eucaryotic genera now carry bacterial names, such as the green walking
stick insect that is named Bacillus and the blind cave amphibium called Proteus. A prerequisite for such a biocode
is to compile a list of all valid names for living and extinct beings.
Ensure access to type strains and their taxonomic data. Prokaryote taxonomy is based on living type strains as
stipulated by the ICNP. It also requires that type strains are deposited in two internationally acknowledged culture
collections in different countries. Regardless of intellectual property considerations, access to type strains must be
ensured for doing comparative taxonomic and other scholarly studies.
Delayed by World War II, the first edition of
the International Code of Nomenclature of Bacteria appeared in 1948. It declared that bacteria
would be described under its rules and no longer
under those of the Botanical Code. The key
principle that distinguishes this code from those
of botany and zoology is that it is based upon
living type strains deposited in type culture collections.
These efforts led to publication in 1966 of
The Index Bergeyana, which was compiled by
Robert E. Buchanan and coworkers. It and later
supplements collected all extent names for bacteria to establish the Approved Lists of
Names. In 1980 the ICSB abandoned those
names that were not represented by a living type
strain. This rigorous ICSB policy put prokaryote
taxonomy on a basis that remains the envy of
botanists and zoologists. The Approved Lists
are continued as Validation Lists in every issue
of the International Journal of Systematic and
Evolutionary Microbiology (IJSEM). Names do
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not have standing in nomenclature unless they
have been included in those Lists. A fourth edition of the Code, is scheduled to appear later this
year during the IUMS Congress in San Francisco.
Meanwhile, the French biologist Emile Chatton in 1937 introduced the terms eukaryotes
and prokaryotes. Taxonomists who specialize
in classifying eukaryotes often have claimed the
species concept for themselves, arguing philosophically that prokaryote species do not exist.
Bacterial taxonomists indeed remain aware of
the less-than-satisfying definition of prokaryote
species. Nonetheless, they have continued to
name prokaryotes as species ever since microbiology enabled them to do so.
In 1968 British taxonomist S. T. Cowan humorously wrote: “a bacterial species is a group
of organisms defined more or less subjectively by
the criteria chosen by the taxonomist to
show—to best advantage as far as possible and
putting into practice— his individual concept,
what a species is.” Rita Colwell and several
collaborators reformulated the bacterial species
concept about a decade ago: “A prokaryote
species is a group of strains that show a high
degree of overall similarity and differs considerably from related strain groups with respect to
many independent characteristics.”
In 1962, Roger Stanier and Cornelis van Niel
published The Concept of a Bacterium, lamenting the state of bacterial systematics but declaring faith in developments that appeared favorable for its future. They said that bacteria are
prokaryotes and vice versa and included the
blue-green algae in this category.
Meanwhile, George Fox, Carl Woese, Erko
Stackebrandt, and others championed the se-
quencing of ribosomal RNA molecules and, later,
genes encoding those molecules as a way of establishing the phylogeny of prokaryotes. Subsequent
classification methods helped to show that rRNA
sequences alone cannot meet this challenge. Today, a majority of taxonomists seem to adhere
to a “polyphasic” approach that Rita Colwell
proposed initially in 1970 and that the Belgian
Peter Vandamme refined in 1996. This approach
calls for combining phenotypic and genotypic
markers as a way of classifying microbial species.
Of course, genomic sequencing is now a powerful tool that is becoming a part of our continuing, cooperative, and international taxonomic
efforts. Those efforts appear to have a bright
future (see box, page 276).
Volume 71, Number 6, 2005 / ASM News Y 277