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INTERNATIONAL JOURNAL O F
SYSTEMATIC BACTERIOLOGY
Vol. 20, No. 4
October 1970
Copyright 1970, Iowa State University P r e s s
pp. 541-550
ARE SOME CHARACTERS MORE EQUAL THAN OTHERS?
S.T. Cowan
ABSTRACT. I n d e c i d i n g o n t h e i m p o r t a n c e o f m i c r o b i a l
c h a r a c t e r s much depends on the meaning attached to
t h e word important, and this was discussed in relation
t o t h e s u b o r d i n a t i o n of c h a r a c t e r s , a n o l d t a x o n o m i c
p r i n c i p l e i n w h i c h d i f f e r e n t k i n d s of c h a r a c t e r w e r e
associated with different category levels.
In a symposium such a s this it i s a l l too easy to accept one feature
(in this c a s e cell wall) a s the most important character of an organism;
t h i s is not mental laziness but the effect of brain-washing. F o r two days
we have listened to experts expounding on the wonders of cell walls which
a r e credited with yielding useful taxonomic information in t e r m s of
anatomy, chemistry and serology; the claims made r i v a l those made for
DNA by molecular biologists. I use the t e r m brain-washed advisedly,
for we have been exposed to concentrated cell walls-and nothing but cell
walls-and a s t r a n g e r in our midst could be excused for believing that
bacteria a r e made up entirely of cell walls and their appendages. It i s
my mission t o t r y to r e d r e s s the balance (for it i s not t r u e that bacteria
a r e entirely made up of cell walls) and, a s a general taxonomist, t r y t o
evaluate what we have heard and, m o r e particularly, put it in proper
perspective relative to the many other features that go to make up the
ba ct e r ium
The problem divides itself into t h r e e p a r t s : (i) to l i s t the kinds of
c h a r a c t e r that a r e used in taxonomic work, (ii) to t r y to pick out those
that a r e most informative about the inherent nature of the organism and
i t s relationship to others, and (iii) discuss what we mean by the word
important when we use it in taxonomy. Some of this I have done before
(Cowan 196 8 ) .
.
Kinds of Characters
Morphology h a s not been discussed in detail in this symposium, although the cell wall undoubtedly makes the major contribution t o the shape
of any microorganism. Most of us limit our morphological studies to the
crude shape (I recognize only three, spheres, rods and s p i r a l s ) , a r r a n g e ment (clumps, packets, and chains), presence o r absence of motility
( f r o m which we predict whether the organism i s o r i s not flagellated),
s p o r e s and capsules. Dr. Kageage h a s warned us that electron m i c r o scopy may add to our confusion, but fimbriae (also called pili) a r e difficult to detect except by i t s use. We may however, use indirect methods
such a s the adsorption of r e d cells to a s s u m e their presence. These fimbriae a l s o have something to do with sex, but this i s a subject which i s
outside the laboratory experience of the microbial taxonomist. Bound up
with morphology a r e the staining reactions of the microbial cell, and
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these depend both on the permeability of the cell membranes to the stain
and stain complexes, and to the reactivity of the cell s t r u c t u r e s with the
particular stain.
T h e r e i s a well-known taxonomic principle, the subordination of
c h a r a c t e r s , which we can apply t o our problem. This means that c e r tain kinds of character a r e used for the definition of taxa of one category
and other kinds a r e used for higher o r lower categories. We cannot
deny the importance of morphological c h a r a c t e r s ; in fact, the highest
categories (or ranks) of bacteria a r e usually based on morphological
features. We distinguish between branched and unbranched rods, between those that have rigid and those that have flexible cells, between
those in which t h e cell i s s p i r a l shaped and those in which it i s not;
these a r e the kinds of character that we use to define bacteria in the
categories we call Order and Family (Table 1).
Differences in stainability a r e m o r e r e s t r i c t e d and, in bacteria, a r e
limited to the reactions to two staining methods, G r a m and Ziehl-Neelsen;
both methods a r e useful but, a s they a r e affected by extraneous f a c t o r s
such a s pH, age of the culture, and the nature of the medium in which
the culture i s grown, they must be interpreted with caution. While the
shape of the bacterium depends on the intact cell wall, its staining c h a r a c t e r i s t i c s depend on i t s permeability and chemical nature. Dr. Doetsch
h a s reminded us that the site of insertion of flagella i s not random but
depends on the s t r u c t u r e of the cell wall. We should, perhaps, reconsider our modern neglect of the type of flagellation.
We do not limit our characterization t o shape and surface s t r u c t u r e ;
we observe c h a r a c t e r s such a s inclusions of fat and other ('metachromatic')
bodies, and the nuclear m a t e r i a l of the bacterium, though t h i s l a s t i s often
considered to be a feature of m o r e i n t e r e s t to the biochemist than t o the
cytologist o r to the taxonomist.
The chemical nature of the different p a r t s of t h e bacterial cell, insofar
a s we know it, s t a r t s with the cell wall and cell membrane. In the basal
mucopeptide component of the wall a r e amino sugars and amino acids and
the presence o r absence of these wall polymers may be related t o the
taxonomy of the bacteria. In some bacteria the cell walls contain teichoic
acids, and different teichoic acids may be associated with different species. However, both Drs. Work and Gooder have expressed doubts about
the usefulness of the wall polymers in taxonomy. The correlation of the
chemistry and the taxonomy depends on accurate identification and good
classification, a s was shown many y e a r s ago when Cummins and H a r r i s
(1956) found some unexpected discrepancies; in their examination of cell
wall extracts of Corynebacterium
pyogenes the chromatogram was differ--ent f r o m that of a l l the other corynebacteria and, indeed,closely r e s e m bled that of streptococci. A check by c l a s s i c a l taxonomic methods indicated that C. pyogenes was a misfit in that genus and that c h a r a c t e r i s t i c s
of a s t r e p t & o m been overlooked. Thus the taxonomic indication
given by the cell wall hydrolysate was m o r e accurate than the 'placing'
by intuitive methods, and provided evidence that cell wall chemistry was
a significant tool which, for Gram-positive bacteria a t least, demarcated
taxa that w e r e 'good' genera.
The cell wall chemistry of Gram-negative bacteria h a s been studied in
other ways; t h e r e has been much m o r e intensive work on the serology of
the 0 antigens of Gram-negative than of Gram-positive bacteria, and
D r . Nikaido h a s summarized f o r us the r e s u l t s of Westphal and his
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543
Table 1. Morphological and cytological c h a r a c t e r s available to the
taxonomist.
Size of c e l l
Shape of c e l l
-sphere
\ spiral
Movement
Capsule
active
\;:::
Appendages
Inclusions
spores
\nucleus
Cell wall
Staining
reactions
Gram
\ Ziehl-Neelsen
colleagues on the sugar components of 'chemotypes,' which, even if they
do not show exact correlations, show a remarkable similarity in the
kinds of enteric bacteria they group together. F o r example, Salmonella
--adelaide, Arizona serotype 20, and Escherichia coli serotype 111: €34 a l l
c r o s s - r e a c t serologically by virtue of similar 0 antigens, and they a l s o
have the s a m e sugar pattern of their 0 antigens (Table 2).
Polysaccharide antigens a r e found in capsules, and in pneumococci
a r e responsible for the type specificity of the organism.
Flagella a r e protein in nature, and the protein flagellin h a s a charact e r i s t i c composition of 14 amino acids. Stocker (1956) h a s suggested
that the multiplicity of H antigens found in the enteric bacteria i s d e t e r mined by different arrangements of the amino acids. Dr. Pine s e e m s to
think that bacterial phylogeny i s revealed by biochemistry, but i f that i s
the accepted view of the biochemist, it i s not one s h a r e d by the microbial
taxonomist
To s u m m a r i z e this section: the chemical nature of the cell surface i s
taxonomically significant and operates a t t h r e e levels:
.
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( i) genus: amino acids and amino sugars of the wall.
(ii) species: teichoic acids of the wall,
(iii) subspecies or serotype: polysaccharides of capsules, amino
acids of flagella.
Chemical and serological make-up of c e l l characters
Table 2.
Cell wall
amino acids
amino sugars
teichoic acids
po ly saccharides
Capsule
polysacchatides
Nucleus
DNA
P
0 antigens
,
We cannot leave the chemistry of the cell without brief mention of the
cytoplasm and cell contents, which, of course, include the nuclear mater i a l . The relations between DNA homology and cell wall structure have
been discussed by Dr. Johnson, who s t r e s s e d the importance of nucleotide sequence. This naturally leads on t o a consideration of hybridization
among bacteria, which i s probably only successful when both p a r t n e r s
belong t o the s a m e genus; so-called intergeneric hybridizations a r e suspect and suggest the need for us t o re-examine our generic circumscriptions. DNA homology, o r lack of it, can justify o r discredit a genus,
and t h i s i s well seen in Neisseria, some species of which s e e m to be
badly located when p l a c e m g e n u s (Bavre 1967, Kingsbury 1967).
Table 3.
Nineteenth century characters used by taxonomists
Colony form
Change in medium
bleaching of indicator
indicator colour change
Growth i n broth
Action on milk
acid formation + c l o t
digestioa of clot
rennet clot formation
Gelatin stab
Pigment production
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SYSTEMATIC
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545
What I c a l l Nineteenth Century C h a r a c t e r s consist of those f e a t u r e s
that can be described and recorded; collectively they a r e a l s o known a s
cultural c h a r a c t e r s but t h i s t e r m is a s vague a s 'taxonomic c h a r a c t e r '
since a l l c h a r a c t e r s a r e both cultural (in the sense that they a r e o b s e r vations on cultures) and taxonomic (since each c h a r a c t e r contributes t o
the description of the organism). To c a l l them Nineteenth Century Chara c t e r s i s explanatory of their place in taxonomy, for in the l a s t century
they w e r e t h e c h a r a c t e r s on which taxonomists depended and the only
ones, a p a r t f r o m morphology, that could be used to describe bacteria.
They include such features a s colony f o r m (size, elevation, surface, edge,
consistency, pigmentation), haemolysis on blood agar, appearance of
growth i n broth, ty-pe of growth in gelatin s t a b cultures, change of indicator in milk and in sugar solutions, clotting and digestion of clot i n
milk, and liquefaction of inspissated s e r u m , Many of t h e s e c h a r a c t e r s
a r e subjective (e. g. in the description of a colour) and a l l a r e influenced
by t e m p e r a t u r e and duration of incubation, and t h e nutritional qualities
of t h e b a s a l medium; in other words, they a r e variable because many of
t h e f a c t o r s that affect them a r e difficult to control. (Table 3).
Table 4.
Physiological characters
Growth requirements
Atmosphere
a i r , oxygen, C02
C and N sources
organic, inorganic
Essential growth
factors
haemin, co-enzyme I
Trace elements
Temperature
Inhibitors
range, optimum
antibiotics
chemical
An extension of the l a s t group of c h a r a c t e r s i s seen i n what a r e des c r i b e d a s the growth requirements and the physiology of bacteria. It is
still useful to know what media encourage and what discourage growth;
what substances a r e essential and which inhibit growth. A refinement of
t h i s listing of media and stimulating/inhibiting substances i s t o study the
actual growth requirements of bacteria; instead of using infusions of
meat we p r e p a r e defined media (often incorrectly called synthetic) so that
we can e x p r e s s the minimal nutritional needs in t e r m s of amino acids,
s u g a r s , salts, and so on. We a r e much m o r e scientific than our foreb e a r s , but we should not be too self-satisfied for not a l l bacteria a r e
accommodating and s e v e r a l pathogens demand animal t i s s u e in which t o
multiply. But if we avoid the difficult organisms (and biochemists always
do) we can describe our bacteria very prettily by naming the carbon and
nitrogen s o u r c e s that can be utilized, and list the t r a e elements and
e s s e n t i a l growth factors that a r e required. Antagonists a r e taxonomically a s interesting a s growth stimulants, and the description of a
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bacterium i s seldom complete without reference to a l i s t of antibiotics
to which it i s susceptible, and another l i s t of those to which it i s r e s i s tant. Some bacteria produce bactericidal substances, bacteriocins, but
production of these may be a s t r a i n characteristic so that this ability
may not be taxonomically significant.
Under the general heading of physiology we a r e concerned with growth
a s it i s affected by extraneous influences acting simultaneously; these
may be (i) physical factors such a s temperature and humidity, (ii) chemical factors such a s the atmosphere in which growth occurs, whether
oxygen can o r cannot be used, and so on. The third group (iii) of factors
a r e physico-chemical, such a s pH value of the medium, and the molarity
of salts in the medium (Table 4).
It would be foolish of m e to say that these nutritional factors a r e m o r e
o r l e s s important than any other kind of feature, but it i s quite obvious t o
the unbiased that, say, compared with morphological c h a r a c t e r s , the two
kinds of feature a r e not only different in themselves but that they a r e
expressing different differences ( o r divisions).
What a r e often called the biochemical c h a r a c t e r s a r e those we d e t e r mine by simple biochemical t e s t s which give us some idea of the enzymatic make-up of a n organism. Within recent y e a r s attention h a s been
focussed on respiration, o r the katabolism of carbohydrate which may be
broken down and utilized by anaerobic fermentation o r by oxidation
(which provides twenty t i m e s a s much energy a s fermentation), o r by a
combination of both methods. Fortunately, there a r e simple t e s t s by
which t h e kind of respiration can be discovered, and many bacteriologists
have chosen this character a s a linch-pin about which a l l taxonomic
problems revolve, thus giving i t a n importance that may be challenged
(Table 5).
Table 5.
Metabolic characters
Enzyme systems -constitutive
inducible
Metabolic products
acids
\pharmacologically
active
A bacterium that is a pathogen
i s much l e s s likely t o be misidentified
than a nonpathogen; the fact that it was isolated f r o m a sick animal o r a
wilting plant i s a pointer t o i t s c o r r e c t identification. But the pathogenicity of a bacterium for an animal, plant, o r even another bacterium,
should not render it any m o r e meritorious in the eyes of the taxonomic
beholder. Unfortunately, the economic and epidemiological significance
of a pathogen h a s made i t s recognition a m a t t e r of concern t o veterinary,
medical, horticultural, and agricultural i n t e r e s t s and increased i t s
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SYSTEMATIC BACTERIOLOGY
Table 6.
547
Other kinds of character available to taxonomists
Pathogenicity
Na t u r a1
animals
plants
Experimental-
infection
'intoxication
Bacteriophage
lysogeny
susceptibility
importance t o the word a t large, with the r e s u l t that outside p r e s s u r e
h a s enhanced the value of this one character out of a l l proportion to i t s
worth in taxonomy. In the host pathogenicity i s often an assumption, and
although a logical one, it can only be proved by infection of another m e m ber of the host species (Table 6 ) .
Finally, we come to the taxonomic relations between the bacteriophage and the host bacterium, which may be of one of two kinds; either
the bacterium c a r r i e s a phage t o which it i s not susceptible (this i s lysogeny), o r the bacterium may be susceptible to one o r m o r e phages, and
the pattern of susceptibility may be characteristic. In either event, the
taxonomic level of the bacterium that is determined by the phage i s a
low one,
Importance ?
In this brief discussion of the kinds of c h a r a c t e r we use in bacterial
taxonomy I have s e v e r a l t i m e s used the words important, valuable, o r
significant, and it is now t i m e to consider what we mean by t h e s e t e r m s .
I have used the t e r m s synonymously, a s a f o r m of what Fowler calls
'elegant variation,' s o h e r e we need discuss only one of them, and I will
take &he simplest of the words, the one most easily understood, important.
Important surely needs some qualification; important for what? Here we
a r e thinking in relatively narrow t e r m s ; we a r e dealing with important
( o r importance) a s i t concerns the taxonomist, and, narrowing it s t i l l
further, a s it concerns him in his evaluation of microbial c h a r a c t e r s .
To estimate what he means in this context by the word important, we
want to h o w what he does with the c h a r a c t e r s , and, in particular, if he
g r a d e s t h e m and a r r a n g e s them in some order. T h e r e a r e two questions
h e r e which should be separated.
(1) What does the taxonomist do with c h a r a c t e r s ? He u s e s them to
describe bacteria, for it i s f r o m the description that he obtains a mental
picture of the organism, and by the description p a s s e s on that picture to
others. Whether the organism i s previously known o r unknown, the
taxonomist uses the description (or c h a r a c t e r s ) so that he (and others)
will know when he has two o r m o r e of a s i m i l a r kind, and he recognizes
the similarity by the number of c h a r a c t e r s shared by the individuals, the
g r e a t e r the number of shared c h a r a c t e r s the g r e a t e r i s the similarity
and when (if ever) a l l the c h a r a c t e r s a r e alike the organisms being compared a r e known to be identical. The taxonomist u s e s c h a r a c t e r s to find
likenesses o r similarities.
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( 2 ) Does the taxonomist grade c h a r a c t e r s , o r a r r a n g e them in some
o r d e r of m e r i t ? It i s a n unconscious habit to make comparisons, and
the taxonomist i s no exception when h e compares different c h a r a c t e r s
and weighs their usefulness to him. Let us suppose that a taxonomist
has cultures of the species we know a s Escherichia coli and Chromobact e r i u m violaceum; quickly he can distinguish t h e m b F h e pigment p r o duced by one of them, but when he stains films by G r a m ' s method he
cannot distinguish t h e m for they a r e both Gram-negative rods without any
distinctive features. Clearly, h e thinks, pigment production i s m o r e
valuable than the G r a m reaction, and h e r a t e s (or grades) it m o r e highly.
C. -lividum and he had
But if his two cultures had been C. violaceum and observed only the s a m e two c h a r a c t e r s , he would not have rated pigmentation any higher (because both species produce a violet pigment) than
the G r a m reaction. These examples show that two c h a r a c t e r s will be
evaluated differently a t different t i m e s , o r when t h e r e i s a different
r e a s o n for making the comparison. The important word in that sentence
i s different, and it d e s e r v e s i t s repitition; it i s perhaps, a clumsy way
of rephrasing the old saw 'every c a s e must be dealt with on i t s own
m e r i t s . ' In this instance the taxonomist, in making his comparisons, i s
looking for differences that will enable h i m to distinguish between different bacteria; h e i s looking for differentiae, and when he finds c h a r a c t e r s
that a r e of different values to h i m he grades them.
The answers t o our two questions cannow be considered together; to
question ( l ) , what does he do with c h a r a c t e r s ? , we found that he was
using them to group s i m i l a r organisms together, in other words, he was
pigeon-holing, sorting, o r classifying. The answer t o question ( 2 ) , does
he grade c h a r a c t e r s ? , is that h e consciously o r unconsciously a r r a n g e s
his c h a r a c t e r s according t o t h e i r value in what he i s doing-this t i m e
separating different organisms, o r identifying them with known ones. An
important difference i n t h e s e activities i s that in sorting o r classifying
he i s comparing s e v e r a l c h a r a c t e r s a t one time,whereas in picking out,
o r identifying, h e i s m o r e likely t o be using one o r two c h a r a c t e r s a t a
time, and he l e a r n s f r o m experience that, for the purpose he has on hand
and with t h e kinds of bacteria he i s dealing with, some c h a r a c t e r s will be
m o r e informative (and therefore useful o r important) than others. As
with c h a r a c t e r s , so with t e s t s for showing c h a r a c t e r s ; some t e s t s will be
m o r e valuable (because they a r e m o r e selective) than others in making
a n identification.
To a taxonomist thinking of c h a r a c t e r s , the word important really
means useful o r helpful; in relation t o c h a r a c t e r s he will r e g a r d t h e m as
being of m o r e - o r - l e s s equal importance for sorting ( o r classifying), but
for identification o r for picking out one of a known kind he. will find that
c h a r a c t e r s vary in their usefulness, and he will grade t h e m according to
their value t o him for that particular purpose. But we should recognize
that even in classifi'cation t h e r e i s an apparent grading; this i s because
t h e r e i s not one universal classification of bacteria, but many different
classifications, some general, some specialized, but each having a different purpose and therefore a different emphasis. These classifications
will differ f r o m each other in the divisions and subdivisions that a r e
made, and these differences will be reflected in the c r i t e r i a ( c h a r a c t e r s )
chosen t o bring them out most clearly. This selection of c h a r a c t e r s for
a special purpose may appear to be s t r e s s i n g those c h a r a c t e r s , but in
fact it is not a weighting, but a r e - a r r a n g e m e n t of c h a r a c t e r s , s o that
different ones become the distinguishing c h a r a c t e r s .
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549
So, a s a general taxonomic principle, we can say that c h a r a c t e r s a r e
of equal importance in classification, but of unequal importance in identification; to answer the question posed by the title of this paper ( a r e
some c h a r a c t e r s more equal than o t h e r s ? ) , we need to look a t the c i r cumstances (identification) in which c h a r a c t e r s do have different values
which (when and w h e r e ? ) a r e most important t o u s .
The TODTen
Historians of the future will be able to judge the present e r a f r o m the
r e s u l t s of ballots, polls, and l i s t s of 'top tens,' for the 1960s have been
characterized by gradings of people and things, f r o m the sale of pop
r e c o r d s to the popularity of politicians. Consequently, it will be in the
modern idiom to grade c h a r a c t e r s in the order of their importance to us,
but we should specify our reason( s) for doing so, for t h e s e lists will vary
with the purpose specified a s much a s l i s t s of popular film s t a r s o r footballers based on polls made in Europe and in the United States. The
analogy with popularity polls i s an apt one, for football fans on the two
continents will be choosing f r o m different t e a m s of players, and bacteriologists working in one discipline will use c h a r a c t e r s (or t e s t s ) not
used by colleagues in other disciplines. Even if we limit ourselves to
identification, t h e r e will be need for different l i s t s for diagnosticians
doing different kinds of work. Most identification work i s done by applied
bacteriologists not greatly concerned with taxonomy, and it will be obvious that, to a sanitary bacteriologist, the pathogenicity of a bacterium
for a plant is not worthy of even a fleeting thought, which means that, for
him, its value o r importance i s zero.
As this symposium has been concerned with cell walls, it is fitting
that I should end by expressing my opinion of their place in a l i s t of top
t e n c h a r a c t e r s most useful f o r general identification work, Let m e say
at once that c e l l walls will obviously be among that top ten, along with
shape, stainability, GC content of DNA, respiration, nutritional require,
ments, enzymes such a s catalase and oxidase, pathogenicity, and
but I a m getting near the tenth and should pause. F o r different purposes,
the o r d e r of m e r i t will be different and for a general identification scheme
I hesitate to name the sequence. Rather would I commend to your notice
diagnostic tables such a s those prepared by the late Dr. Steel and m e
some y e a r s ago (Cowan and Steel 1961,1965), and beg you to a s s u m e that,
of the top ten, none is m o r e equal than another.
...
Literature
Cited
BBvre, K. 1967. Transformation and DNA base composition in taxonomy,
with special reference to recent studies in Moraxella and Neisseria.
Acta Dath. microbiol. scand. 69:123-144.
Cowan, S. T. 1968. An a s s e s s m e n t of the value of biochemical and s e r o - Chemotaxonomy and
logical techniques in microbial taxonomy. In
Serotaxonomy, ed. J. G. Hawkes, 269-278. London: Academic P r e s s .
and K. J. Steel. 1961. Diagnostic tables for the common medical
bacteria. J. Hyg., Camb. 59:357-372.
and
1965. Manualfor the identification of medical bacteria.
Cambridge: University P r e s s .
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.
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