Prokaryote Systematics: The Evolution of a Science

CARL R. WOESE

Introduction
The editors of The Prokaryotes are taking the bold and scientifically proper step of organizing this
second edition along phylogenetic lines. The idea of classifying bacteria in this way, according to their
“natural” relationships, is by no means new; it is, in fact, as old as bacteriology itself. What is new is our
capacity to do so. Before the advent of molecular sequencing—particularly of nucleic acids—the
microbiologist simply did not have the tools with which to generate the types of data required to
construct a reliable bacterial phylogeny. Now the microbiologist does. This edition of The Prokaryotes
thus marks a major turning point in the history of bacteriology; the familiar order of the old
determinative classification (with its misleading phylogenetic overtones) is giving way to the meaningful
order of a phylogenetic system. Replacing the old determinative classification with a phylogenetically
valid one may not at first sight appear to be a radical or even important departure for the field of
microbiology. Yet it is; and hopefully this will become apparent as the present chapter unfolds and as
the reader derives insights and other benefits from the succeeding chapters in this phylogenetically
organized edition of The Prokaryotes.

Microbiology—the Science Without a Past

Organisms are in essence historical documents; their structure at all levels reflects (is determined by
and records) their evolutionary history. For this reason a knowledge of evolution and of evolutionary
relationships is an integral part of explanation and understanding in almost all aspects of biology. Unlike
zoology and botany, microbiology developed without this historical dimension, without knowledge of the
phylogenetic relationships among the organisms it studied. It is impossible to say exactly what effect
this has had on the science of microbiology. However, there can be little doubt that knowing the
phylogeny of bacteria would have profoundly altered the course not only of microbiology, but of biology
as a whole.

Consider as an example the role phylogenetic classification plays in zoology: A new beetle is
discovered. It is found to represent a novel genus within the Coleoptera. The biologist, therefore, knows
many things about this discovery that would not otherwise be known, and has explanations for many of
the insect's features that come only from knowing the evolutionary history, the comparative anatomy,
of beetles. This knowledge strongly influences the biologist's scientific orientation, the interpretation of
experimental results, etc.

Contrast this to the microbiologist's classification of a new bacterial isolate. Placing the bacterium in a
determinative system is helpful when it provides precise identification, as when the isolate is found to be
identical (or closely related) to some known species. In this case preexisting knowledge can be invoked
in studying or otherwise dealing with a new isolate. However, if the isolate is sufficiently unusual that it
can be placed only within one of the higher taxa in the deterministic order, the organism's classification
can actually work against understanding the new species, unless that taxon chances to have
phylogenetic validity. The assumption that this familiar order is actually a meaningful order leads to
confusion, not enlightenment. The determinative system presented in the 8th edition of Bergey's Manual
(1974) is full of higher level groupings of this nature—all polyphyletic scramblings, familiar orders
conveying the semblance of understanding without its substance. Examples are the gliding bacteria, the
sheathed bacteria, the appendaged bacteria, the spiral and curved bacteria, the rickettsiae,
Flavobacterium, and, of course, the classic Pseudomonas. We often read statements about some
property of the “pseudomonads,” in which the author fails to identify the particular species of
Pseudomonas possessing that property, on the

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mistaken assumption that the genus Pseudomonas (which means “false unit”!) is a truly
monophyletic grouping, of which this particular strain must, therefore, be representative.

The microbiology that developed in the absence of an evolutionary framework is a science strong on the
applied side; it has also been a rich mine for the biochemist (who treats organisms merely as bags of
enzymes), and one bacterium in particular, Escherichia coli, has proven a most convenient and
productive source of genetic and molecular understanding. However, bacteria hold a special place in the
global ecology: they are the bases of food chains and/or the main mechanism for recycling organic
material. They are agents of mineral deposition and the source of our oxygen atmosphere. (The role of
plants here is not being overlooked; their photosynthetic capacity is of bacterial origin, however.)
Bacteria have ex-isted for at least three-quarters of the earth's history, nearly 10 times as long as the
metazoans, upon which the biologist bases the concept of evolution. Yet the microbiology that could
properly conceptualize and develop these aspects of bacteria never came into existence. Only now that a
phylogenetically oriented microbiology exists can we begin to relate the history of life on this planet to
concomitant geologic changes (i.e., relate biochemistry to geochemistry), to develop a deep
understanding of bacterial ecology and to advance the frontiers of evolution.

Early Attempts to Determine the Natural Relationships Among Bacteria

The 19th century witnessed the transformation of the Linnean classification system into a phylogenetic
systematics (albeit somewhat imperfect) for the metazoa. The reason this was possible and the reason
for the system's success lay in the morphological complexity of animals and plants, the ontogenetic
recapitulation of the phylogenetic sequence, and the existing knowledge of the fossil record. Early
microbiologists recognized the benefits of similarly classifying the bacteria:

… the only truly scientific foundation of classification is to be found in appreciation of the available facts from a
phylogenetic point of view. Only in this way can the natural interrelationships of the various bacteria be properly
understood … it cannot be denied that the studies in comparative morphology made by botanists and zoologists
have made phylogeny a reality. Under these circumstances it seems appropriate to accept the phylogenetic
principle also in bacteriological classification (Kluyver and van Niel, 1936).

However, the facts that bacteria are morphologically very simple, that they do not have meaningful
developmental stages, and that bacterial fossils (which are phylogenetically uninformative in any case)
had yet to be discovered, meant that attempts to develop a natural classification system for the bacteria
were doomed from the start, and would even adversely affect the development of the science of
microbiology.

During the lifetime of Louis Pasteur and Ferdinand Cohn (mid- to late 19th century) a natural system of
bacterial classification was not very important. Bacteriologists then were wrestling with the basic
question of the nature of a bacterium, with problems such as the apparently pleomorphic nature of
bacteria (the result of working with impure cultures), the difficulty of their isolation and cultivation, and
the search for a sufficient number of characters by which to make useful distinctions among them. Thus,
it was relatively unimportant whether bacteria were related to plants (as Cohn believed) or were the
Monera of Haeckel's new third (protist) kingdom; or whether or not bacteria and blue-green algae were
truly related. Cohn's original “form-genera” classification of bacteria, a simple system based upon shape
and behavior, gave the microbiologist a useful start on the problem.

By the turn of the century, however, the evolution of bacteria (and so a natural system of classification)
had become an important consideration, as witnessed by the above quote from Kluyver and van Niel.
Bacteriologists debated the proper criteria upon which to base a natural system, as well as the
appropriate assumptions to make regarding bacterial evolution. Emulating metazoan taxonomists, most
early microbiologists assumed the morphological characters were the fundamental ones: “It is self-
evident that the shape of the cells is of outstanding importance for determining the place of a bacterium
in any phylogenetic system” (Kluyver and van Niel, 1936). And in defining the higher taxa there could be
“no doubt that in this respect morphology remains the first and most reliable guide.” (Kluyver and van
Niel, 1936). Physiological characters were suspect “because of the wide range of adaptation which is
manifested in bacteria” (Kluyver and van Niel, 1936) and such characters were thus definitely secondary.
Prévot (1933), among others, felt that physiological characters were reliable only in making the lowest
level, interspecies distinctions. Their use as primary (high-level taxonomic) characters was so at
variance with conventional wisdom in the first part of this century that Kluyver and van Niel (1936)
judged “Orla-Jensen's

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contribution to systematics—the prominent place assigned to rightly evaluated physiological

characters— … a milestone in the development of bacterial taxonomy.” Still, van Niel a decade later
cautioned that “… we cannot yet use physiological or biochemical characters as a sound guide for the
development of a ‘natural system’ of classification for bacteria” (van Niel, 1946).

By the 1940s, a number of “natural,” albeit procrustean, bacterial classifications had been devised —
e.g., by Migula (1907), Pringsheim (1923), Buchanan (1925) (the beginnings of Bergey's Manual),
Kluyver and van Niel (1936) (later emended by Stanier and van Niel [1941]), and Prévot (1940)—all
based primarily on morphology, and so all basically similar.

The original Kluyver and van Niel (1936) system serves as a good example of these efforts and the
assumptions underlying them: the primary assumption—given that morphology reigned—was that the
simplest shape, the sphere, was the original shape. In keeping with Oparin's (1938) primitive ocean
theory, bacterial metabolism was seen as initially heterotrophic . More implicity embodied in the
scheme was the notion—taken again from metazoan experience—of an evolutionary development;
evolution proceeded toward increasingly intricate forms, toward more complex life cycles, “in the
direction from unicellularity to multicellularity” (van Niel, 1946). The postulated ancestral coccoid
eubacterium was seen as developing along four lines: in the family Micrococcaceae, the cell shape
remained spherical, but a progression from single cells, through tetrads, to cells grouped in packets
(sarcinae) occurred, culminating in “the highest developmental stage … the cocci able to form
endospores” (Kluyver and van Niel, 1936). The fact that “motility occurs … sporadically among the cocci
… indicates that also the flagellated rods find their origin in this primitive group, the more so since the
two typical modes of flagellation are already encountered” (Kluyver and van Niel, 1936). Here then is the
origin of the Pseudomonadaceae, “cephalotrichous (and related immotile) rod-shaped bacteria,” spiral,
curved or straight, but largely Gram-negative; and the Bacteriaceae, “peritrichous (and related immotile)
rod-shaped bacteria,” either sporeforming or not, but in the main, Gram-positive. The final family, the
Mycobacteriaceae, arises from a lineage that “leads via the streptoccoci to the short Gram-positive rods
in the group of lactic acid bacteria and corynebacteria. The further development of these universally
immotile bacteria can have given rise to the mycobacteria which apparently form the connecting link
with the simpler actinomycetes” (Kuyver and van Niel, 1936). Although (purple and green)
photosynthetic bacteria were enfolded into the various categories of this scheme (their morphologies
were typical and their physiologies incidental) the emphasis on morphological characters forced the
exclusion of the spirochetes, myxobacteria, and blue-green algae.

Stainer and van Niel (1941) later completed (and emended) the scheme, using the Kingdom Monera to
include all the prokaryotes within two divisions, the Myxophyta (blue-green algae) and the
Schizomycetae (bacteria). The division of schizomycetes contained three classes “of polyphyletic
origin” (Stainer and van Niel, 1941 ) Eubacteriae, Myxobacteriae, and Spirochaetae. At this time the
photosynthetic bacteria were also separated from their nonphotosynthetic counterparts in a separate
order Rhodobacteriales; showing that the microbiologist had now developed greater confidence in
physiological characters.

The Dream Ends

These early bacteriologists cannot be faulted for their efforts at phylogenetic classification. They
followed scientific principles and were generally temperate and tentative in their conclusions and
pronouncements. Their goal was to create a framework that would generate understanding and
successfully guide bacteriology into the future. However, they dealt with a vast array of facts— shapes,
sizes, arrangement and behavior of cells, flagellar patterns, spore characteristics, Gram stain, fixation
and staining artifacts, pigmentation, colony characteristics, nutritional requirements, catabolic
properties, and so on—that were ill-defined; and the relationships among these facts were confusing.
Moreover, the majority of their facts represented relatively superficial properties of bacteria. This hazy,
unsortable continuum from useful to meaningless facts and relationships did not become the basis for
building a useful natural classification of bacteria, but rather served as a convenient and powerful
device by which prejudices could be laundered into scientifically respectable pronouncements.
Bacteriologists of the day readily justified their view that blue-green algae are not really bacteria; “…
pigmentation does not afford any indication of relationship between Bacteria and Myxophyceae …”
(Pringsheim, 1949). They just as readily put certain bacteria, e.g., Beggiatoa and Thiothrix, together with
the blue-green algae, because “representatives of … [these] genera show such unmistakable
morphological affinities with the Cyanophyceae that in our opinion they must be considered as
colourless derivatives of the genera

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Oscillatoria, Phormidium and Schizothrix. …” (Kluyver and van Niel, 1936).

Eventually, most microbiologyists came to realize the futility of these attempts to construct a
phylogenetic systematics for the bacteria. Van Niel put his rejection of the whole program (the end of
his dream of a natural system for bacteria) this way in 1955:
What made Winogradsky (1952) grant that the systematics of plants and animals on the basis of the Linnean
system is defensible, while contending that a similar classification of bacteria is out of the question? The answer
must be obvious to those who recognize in the former an increasingly successful attempt at reconstructing a
phylogenetic history of the higher plants and animals, based upon comparative-anatomical, embryological,
distributional, ecological, and paleontological studies and who feel that comparable efforts in the realm of the
bacteria (and bluegreen algae) are doomed to failure because it does not appear likely that criteria of truly
phylogenetic significance can be devised for these organisms (van Niel, 1955).

This became microbiology's new catechism:

For [most] major biological groups [including the bacteria], the general course of evolution will probably never be
known, and there is simply not enough objective evidence to base their classification on phylogenetic grounds.
For these and other reasons, most modern taxonomists have explicitly abandoned the phylogenetic approach. …
(Stanier et al. 1970).

It was one thing to recognize the impossibility of classifying bacteria phylogenetically by the existing
criteria. It was quite another to conclude that they could never be so classified. Yet, this indeed is what
the field of microbiology had done—clinching this scientific exorcism by adopting the attitude that,
determinable or not, knowing the phylogenetic relationships among bacteria was not important in any
case—an attitude that seems to have been held from the start by the “realists” who had “… been
impatient with idealists … [for] unjustified speculations regarding relationships between … bacteria”
(Breed, 1939), and who evinced little cognizance of evolution. Where were the “idealists” now, who
understood that “… the mere fact that a particular phylogenetic scheme has been shown to be unsound
by later work is not a valid reason for total rejection of the phylogenetic approach” (Stanier and van Niel,
1941)?

Henceforth, speculation concerning bacterial evolution became solely an extracurricular activity, best
done over a glass of port; classification would be solely determinative; and criticism of the system
would center merely upon its organization, which “… based on the Linnean approach, not only is
unjustifiably pretentious, but also impedes the best utilization of established characteristics because
they are employed for the construction of mutually exclusive combinations” (van Niel, 1955).

The outcome of all this was an atavistic replacement of the concern with natural relationships by the
still-unsettled problem of what a bacterium (a prokaryote) actually is:
… the biological nature and relationships of the bacteria have been subjects of perennial discussion. Why have
these questions obsessed some members of each succeeding generation of microbiologists? There can be no
doubt about the principal reason. Any good biologist finds it intellectually distressing to devote his life to the
study of a group that cannot be readily and satisfactorily defined in biological terms; and the abiding intellectual
scandal of bacteriology has been the absence of a clear concept of a bacterium. … Our first joint attempt to deal
with this problem … 20 years ago … was framed in an elaborate taxonomic proposal, which neither of us cares
any longer to defend. But even though we have become sceptical about the value of developing formal taxonomic
systems for bacteria …, the problem of defining these organisms … in terms of their biological organization is
clearly still of great importance … [italics added] (Stanier and van Niel, 1962).

While great progress would be made in characterizing and defining the prokaryotic cell, a
fundamental answer to this new/old question of bacterial organization nevertheless rested upon
having a natural classification for bacteria; to fully interpret that historical document the cell,
comparative analysis in the context of a phylogenetic framework is essential.

The Molecular Revolution

The historical irony here is that as the interest in determining bacterial phylogenies waned, as the
enterprise became increasingly distrusted, discredited, and disregarded, the tools for generating a valid
phylogenetic classification for bacteria were being developed by molecular characterizations of the cell.
The reason why this would make possible what seemed impossible is obvious: on the molecular level,
prokaryotes are just as complex, just as stable, and just as easily and clearly defined, as eukaryotes are.

In their seminal article “Molecules as documents of evolutionary history,” Zuckerkandl and Pauling
(1965) emphasized the considerable historical information contained in macromolecular sequences.

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relatively simple to interpret), they are perfectly well defined and generally comprise hundreds to
thousands of more-or-less-independent characters (amino acids or nucleotides). The number of
different possible sequences is enormous. Thus (extensive) similarity always signifies evolutionary
relatedness; convergence ceases to be a consideration. Or, as Zuckerkandl and Pauling (1965) put it: “…
a recognition of many differences between two [sequences] does not preclude the recognition of their
similarity.”

From the extent (and nature) of the differences among sequences that correspond in different
organisms to the same function, one can reconstruct molecular genealogies, build evolutionary trees
for the organisms (Fitch and Margoliash, 1967; Fitch 1971; Felsenstein, 1982; Olsen, 1988).

The initial molecular approaches used to characterize bacteria gave less precise, less reliable, and more
restricted phylogenetic information than the underlying full sequences later would—however, these
were a far cry from the ill-defined, ambiguous, and misleading phenotypic characterizations previously
available. Genetic studies, nucleic acid hybridizations, and immunological cross-reactivities all helped
to provide a phylogenetic basis for a variety of bacterial genera. DNA base ratios provided a widely
accepted and useful (but generally overvalued) phylogenetic measure as well. Molecular analyses of the
bacterial cell wall brought meaningful order to the “high GC” Gram-positive bacteria (Schleifer and
Kandler, 1972). And full sequences were even determined for a few cytochromes (Ambler et al., 1979a
and b) and ferredoxins (see George et al., 1985). It was not until the late 1970s, however, after the
partial sequencing method known as oligonucleotide cataloging had been extensively applied to
bacterial ribosomal RNAs, that the full panoply of bacterial phylogeny was finally glimpsed (Fox et al.,
1980).

The Nature of Molecular Chronometers

The “evolutionary clock” (Kimura, 1983) is one of the great discoveries of the 20th century: The fact
that in different organisms different (but clearly related) molecular sequences correspond to what
appears to be the very same molecular function implies that most of the (net) changes that become
fixed over time in any given molecular sequence are selectively neutral; they are of no phenotypic
consequence (Kimura, 1983). Such changes must happen more or less randomly in time, and so can
be used to measure time in a relative sense. In other words, on the genotypic level a more-or-less
steady pace of evolutionary change occurs that is quasi -independent of the sporadic “real”
evolutionary changes happening in the overlying phenotype. This independent “evolutionary clock”
embedded in the genotype gives the biologist the capacity to infer evolutionary histories and
relationships (Woese, 1987); and it has also freed the bacteriologist from the phenotypic quagmire of
ill-defined, confusing, or conflicting, and generally phylogenetically uninterpretable morphological
and physiological characters.

Not all molecular chronometers are equally useful for reconstructing genealogies, however (Woese,
1987): Some are more accurate than others. Some are restricted to particular taxonomic levels and/or
particular bacterial groups. Others give distorted answers because they have undergone (subtle)
functional, i.e., selected, changes. The most reliable molecular chronometers might seem to be those
free of direct connections with the overlying phenotype, such as parts of introns, pseudogenes, “junk
DNA.” Changes in their sequence would necessarily happen randomly, and so would be interpretable in
a straightforward way. However, changes become fixed so rapidly in these sequences that the range of
organisms over which they provide phylogenetically useful information is extremely narrow (Kimura,
1983; Woese, 1987).

The most useful molecular chronometers actually are molecules like the ribosomal RNAs— molecules
with universal, constant, and highly constrained functions that were established at early stages in
evolution, functions that are not affected by changes in the organism's environment (except for changes
in basic physical parameters such as intracellular pH and temperature). (A strong indicator of the
constancy of rRNA function is the near constancy of the molecule's secondary structure within each of
the primary kingdoms, and the approximate constancy that holds even between kingdoms [Gutell et al.,
1985]). Because rRNAs are large molecules, they contain considerable information; their size also makes
them less erratic chronometers than smaller molecules (Woese, 1987). Moreover, rRNAs are easy to
isolate in relatively large quantities; they seem not to be subject to lateral gene transfer; and they can be
sequenced directly (without resort to gene cloning).

The fact that a precisely functioning molecule such as RNA is under strict functional constraints is

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both an advantage and a disadvantage. The advantage lies in the constancy of the constraints on the
various positions in the sequence and the fact that some positions change far more slowly than others;
this last makes the molecule like a clock that includes both a second hand and a calendar —i.e., it can
measure a wide range of time intervals. The disadvantage is that the stringent constraints lead to more
(local) sequence convergence than otherwise, and the vast differential in rates at which positions
change makes analysis more problematic than it would be for a uniform rate situation. (Another of its
advantages would appear to be that RNA is a “nonlinear” chronometer and so is potentially capable of
distinguishing rapidly vs. slowly evolving lineages, and, therefore, localizing the root of a tree without
the need to resort to the use of outgroup sequences [Woese, 1987]).

Construction of Phylogenetic Trees from Sequence Data

The initial step in extracting phylogenetic information from molecular sequences is to align them. An
ideal alignment procedure places all the homologous positions in a set of sequences in
correspondence. We generally equate statistically significant sequence similarity with homology, the
retention of ancestral attributes, and so align sequences by maximizing their similarity. However,
sequence similarity is a somewhat inaccurate indicator of homology (especially the “maximized”
similarities generated by some of the computer algorithms now in use). The issue of what constitutes
sequence homology is not as straightforward as it initially seems, but it is inappropriate to discuss this
in detail here. Suffice it to say that homologous sequence positions are often difficult to identify (as
sequence similarities) in the absence of knowledge of higher order structural (and functional)
homology—especially when sequences span the vast evolutionary distances they do in the microbial
realm. (Recall that genes under no phenotypic constraint change composition very rapidly on an
evolutionary time scale [Kimura, 1983]), Thus, significant higher order structural similarity is generally
taken to mean homology, and in turn is used together with sequence similarity in attempts to construct
sequence alignments that maximize homology (Woese et al., 1983).

Two main types of analysis are used today to infer phylogenetic trees from sequence alignments,
evolutionary distance analysis (Fitch and Margoliash, 1967; Felsenstein, 1982) and maximum parsimony
analysis (Fitch, 1971; Felsenstein, 1982). The former takes into account only the number of positions that
differ in composition between pairs of sequences—this pair-wise difference being formally a distance.
The latter looks at the quality of the difference between sequences, i.e., at which positions have different
compositions in different sequences and the nature of these differences. Evolutionary distance analysis
uses less of the information in an alignment than does maximum parsimony analysis. A crude analogy
that to some extent captures the distinction between the two is that of a person arriving at a city from
some far-away place, having traveled by some arbitrarily chosen circuitous route. A distance
measurement would concern itself only with how far the person has traveled, not the route, the travel
time or where the traveler began. A parsimony analysis attempts to reconstruct the actual route taken.

With the evolutionary distance method, the observed number of differences between two sequences is
an underestimate of the actual number of differences, because more than one change will have taken
place at some positions; and in some instances these will appear to be no change. The greater the
actual distance between two sequences, the greater their observed difference underestimates it.
Consequently, sequence distance measurements make distantly related lineages seem relatively closer
than they actually are—often making them appear specifically related, when indeed they are not
(Felsenstein, 1982; Olsen, 1988) . Fortunately, this underestimate of distances can be corrected
statistically, at least to some extent (Jukes and Cantor, 1969; Olsen, 1988).

The maximum parsimony method assumes that evolution proceeds by a “least action” principle, i.e.,
that in generating sequence B from sequence A, the evolutionary process tends to make the minimum
number of changes required to do so. Thus the “correct” tree (evolutionary branching order) is
assumed to be the one that allows the minimum number of changes in going from some (assumed)
ancestral sequence to the collection of its descendant sequences (being considered). As with the
(uncorrected) evolutionary distance method, maximum parsimony analysis fails to take multiple
changes at a given position in an alignment into account, and so shows a strong tendency to cluster
distant lineages, whether or not they are specifically related to one another (Felsenstein, 1982).

All methods of phylogenetic tree inference are imperfect, due to the effects just mentioned, as well as
others (Felsenstein, 1982; Olsen, 1988; Jin & Nei, 1990). They perform particularly badly when

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dealing with lineages that evolve at different rates and with sequence alignments wherein the different
positions change composition at vastly different rates. Unfortunately, these are the real-world
conditions. If nothing else, it is important to confine analyses of a sequence alignment to those
positions that are the most “phylogenetically informative”, i.e., those that have not changed
composition frequently during the time span covered by the alignment (Felsenstein, 1982; Olsen, 1988;
Achenbach-Richter et al., 1988).

The construction of phylogenetic trees has become an arcane art, and most biologists are unable to
assess the validity of such trees. A major part of the problem here lies with the practitioners of the art,
who feel no responsibility to present their methods and conclusions to the broader scientific community
in intelligible forms; in some cases it is even impossible to reconstruct a particular analysis from its
published account. To make matters worse, different experts using different methods usually disagree
about the correct branching orders. However, it appears (based largely upon the consistency of the
rRNA trees derived under different conditions, from alignments of varying compositions, etc.) that most
phylogenetic trees now being inferred from bacterial sequence data by the standard methods are at least
first approximations to the correct trees.

Since bacterial relationships so far are based almost exclusively upon a single molecule, the 16S rRNA
(or the functionally related but far-smaller 5S rRNA), it remains an assumption (yet a reasonable one)
that the phylogenies so inferred represent the organism as a whole. It would seem, therefore, that the
scientifically proper stance for the microbiologist to take at this juncture would be to treat these
phylogenies as hypotheses, and test them using other molecules, phenotypic characteristics of the
organisms, and so on. When the same or very similar relationships are given by different molecular
systems or when new phenotypic similarities consistent with the projected phylogeny turn up, then that
(general) phylogeny can be confidently accepted. A few such tests have already been done, and the
results have almost always confirmes the major taxa inferred from ribosomal RNA sequence analysis.
For example, a large structural idiosyncrasy in an ATPase sequence common only to the (true)
flavobacteria and the bacteroides (Amann et al., 1988) confirms a relationship that was suggested solely
on the basis of the analysis of 16S rRNA.

Prokaryotes and Eukaryotes

So long as their phylogeny remained an unresolved, confused matter, and their nature was so little
understood, the relationship of bacteria to eukaryotes was not a fruitful subject for discussion.
Although there was little doubt that eukaryotes were a monophyletic group (because it seemed unlikely
that such a complex cell would arise twice), the same could not be said of bacteria. Microbiologists
disagreed as to whether the bacteria were distant relatives of plants (Cohn's view), whether some (the
blue-green algae) were plant-like and others not, whether they belonged to Haeckel's kingdom of
protists, and so on; but there was general agreement that bacteria were not necessarily all related to
one another. This could be seen in the strong distinction made between blue-green algae and bacteria,
and in the reluctance to include myxobacteria and spirochetes, for example, in the usual bacterial
taxonomic schemes (Pringsheim, 1949; Stainer and van Niel,
1941). There was just too much morphological and physiological diversity among them for the
(premolecular) bacteriologists to feel comfortable with the concept that bacteria were a
monophyletic group.

In the 1930s, Chatton (1937) attempted to bring order into this confusion by placing all living systems
into one of two categories, defined on the basis of fundamental cytological distinctions:
“Eukaryotes” were those organisms whose cells contained a membrane-bounded nucleus and
certain organelles; “prokaryotes” lacked these features.

Bacteriologists were not initially attracted to Chatton's suggestion, because it defined prokaryotes in a
completely negative way and thus did nothing to address the bacteriologists' concerns about the
nature of bacteria and their relationships.
The entirely negative characteristics upon which this group is based should be noted, and the possibility of …
convergent evolution.… be seriously considered (Pringsheim, 1949).

… the bacteria and blue-green algae encompass a number of distinct major groups, which do not now appear to be
closely related to one another; their only common character is that they are procaryotic. It thus appears that the
procaryotic cell has provided a structural framework for the evolutionary development of a wide variety of
microorganisms. (Stanier and van Niel, 1962)

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The matter was further confused by suggestions (based upon artifacts and misinterpretations) that
some bacteria might actually have cytological structures similar to those that were considered unique to
eukaryotes (DeLamater, 1952; Tulasne, 1947).

However, with the advent of the electron microscope and other molecular tools, the prokaryote (as well
as the eukaryote) began to take on a well-defined submicroscopic and molecular character of its own. It
was now possible to define and distinguish prokaryote from eukaryote in comparable terms, e.g., the
differences in ribosome structure ( Woese, 1970; Woese and Fox, 1977a). These detailed studies
strongly reinforced the notion that “prokaryote” was a monophyletic unit. Yet, the ready acceptance of
this conclusion was strange, for despite the above-cited reservations of some bacteriologists and the
warnings of others:
… there are remarkably few comparative studies. The result is that the application of the newer adjuncts of
morphology for taxonomic purposes entails generalization from limited cases (Murray, 1962),

the “characteristic” features of prokaryotes were derived from very few examples thereof.
Escherichia coli was the only prokaryote to be extensively studied. This can only mean that the
monophyletic nature of prokaryotes was assumed a priori by those interested in their molecular
characterization.

By the late 1960s the prokaryote-eukaryote dichotomy had become dogma; and the critics had
become converts:
There is little doubt … that biologists can accept the division of cellular life … into two groupings at the
highest level expressing the encompassing characters of procaryotic and eucaryotic cellular organization.
(Murray, 1974)

All organism except viruses can be assigned to one of two primary groups, readily distinguishable by
differences in cellular organization.… The definition of bacteria and blue-green algae in terms of positive
rather than negative characters had to await the revolution in our knowledge of cell structure which followed the
introduction of the electron microscope as a tool in biological research.… These differences [between
prokaryotes and eukaryotes] are now so widely recognized that descriptions of them can be found in the
better textbooks of general biology …, a sure indication that they have acquired the status of truisms (Stanier,
1970).

The strength of the eukaryote-prokaryote dogma was convincingly demonstrated by the incredulity
expressed by many, perhaps the majority, of biologists at the discovery of the archaea (archaebacteria),
almost all of it unpublished, unfortunately. Biologists could no longer even imagine that a class of
prokaryotes could exist that were no more related to other prokaryotes than they were to eukaryotes!

The prokaryote-eukaryote distinction did much to focus and refine the biologist's concept of the primary
phylogenetic relationships. However, in an important sense it was wrong and so, wrongly shaped the
biologist's thinking, with the result that it impeded as much as it fostered scientific progress. The
seductive symmetry of this simplistic dichotomy is almost certainly the source of the problem:
monophyletic eukaryotes (the one side of the equation) imply monophyletic prokaryotes (the other).
(One wonders how long the discovery of the archaea was delayed by this all-too-simple catechism).

The concept has an even more pernicious aspect, however. The prefix pro- in prokaryote connotes three
interrelated things: 1) prokaryotes are older than eukaryotes; 2) prokaryotes are simpler and more
primitive than eukaryotes; and 3) prokaryotes are an ancestral stage in the evolution of eukaryotes. A
clear example of these assumptions can be seen in the works of L. Margulis (e.g., 1988). A constant
theme, readily apprehended in her diagrams, is the aboriginal cell that gives rise to an ancestral
bacterium, that in turn spawns a cascade of sublineages, certain ones of which go on to form various
aspects of the ancestral chimeric eukaryotic cell (through endosymbiotic interactions). The
mycoplasmas (“aphragmabacteria” in her terminology) provide the body of the eukaryotic cell (the
“host” component), whose mitochondria are derived from the “omnibacteria” (a group vaguely
reminiscent of the purple bacteria); cyanobacteria become the ancestral chloroplasts, spirochetes the
ancestral flagella, and so on.

The microbial phylogenies based upon molecular sequence comparisons fail to support this picture and
its underlying assumptions (Fox et al., 1980; Woese, 1987). The eukaryotes seem as ancient a group as
the bacteria; the basic eukaryotic cell (its organelles aside) does not appear to have arisen from either
prokaryotic group; and the notion that the eukaryotic cell was a prokaryote that evolved to become more
“advanced” is no more than anthropocentric bias. (In any case, the fact that we now know two disparate
types of prokaryotic organization exist casts any presumed prokaryotic stage in the evolution of the
eukaryotic [host] cell in a whole new light).

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Prokaryotic Evolution

How Valid Were the Old Phylogenies?

The bacterial phylogeny that emerges from molecular sequence comparisons has little in common with
our preconceptions. The old microbiologists' worst fears concerning the phylogenetic validity of the
phenotypic characters that they had to deal with have been fully realized. Morphology is not the guiding
principle they once took it to be; most, if not all bacterial morphological characters are just too simple
not to have evolved independently numerous times. Cocci generally arise as degenerate variants of
less simple shapes, as in the cases of Micrococcus, Staphylococcus, Leuconostoc, Paracoccus, and
other genera the reader will encounter throughout this volume. It is doubtful that patterns of cell
aggregation are useful phylogenetic characters even for making species distinctions. Bacterial
appendages, particular modes of motility or division, and flagellar patterns all show a scattered,
polyphyletic distribution (Fox et al., 1980; Woese, 1987). A few of the more complex morphological
traits, such as endospore formation, have some phylogenetic validity; but what is a phylogenetically
meaningful morphological character cannot be assessed a priori.

The traditional physiological characters fare no better, though far less had been expected of them.
Autotrophy and heterotrophy, and oxidation and reduction of the same compounds, can be found
within different species in the same genus or family, and occasionally even in the same organism
(Fox et al., 1980; Woese, 1987). Phylogenetic sense has yet to be made of the catabolic patterns in
groups such as the clostridia. The most phylogenetically consistent physiological trait is
photosynthesis (Woese, 1987): each of the five known variations of chlorophyll-based
photosynthesis represents a different bacterial phylum (division).

Phenotypic characters, both morphological and physiological, tend to define incomplete (paraphyletic)
groupings; close relatives lacking the trait in question almost always occur (Woese, 1987). For
instance, nonsporeforming relatives of spore formers are common, and “colorless” relatives often
outnumber the photosynthetic bacteria in a number of taxa. (Ironically, however, none of the bacteria
that the early bacteriologist felt certain were colorless relatives of the blue-green algae [see above]
turned out to be so.

It is clear that the microbiologists who would now construct a new (phylogenetic) taxonomy for bacteria
must take as open minded and creative an approach to developing the new system as possible. It will
not do unthinkingly to apply the old Linnean formula, to continue merely to use only the old criteria for
defining and naming taxa, or to make the new system a chimera of old and new concepts and categories
(Stackebrandt et al., 1988).

The Scope of Prokaryote Phylogeny

The ability to determine bacterial phylogenetic relationships, which culminated in the discovery of the
archaea (Woese and Fox, 1977b), has had three important consequences: 1) it has permitted the
construction of a comprehensive phylogenetic tree that relates all living systems (see Fig. 1);
2) it provides the basis for a proper understanding of the relationship between prokaryotes and
eukaryotes; and 3) it gives us a framework within which to begin developing a meaningful concept of
the universal ancestor of all life on this planet.

Fig. 1. An unrooted universal phylogenetic tree. The tree was produced from an evolutionary distance matrix
derived from an alignment of small subunit rRNA sequences. Only those positions in the alignment judged to be
homologous among all three domains were used in the calculation. Detailed descriptions of these procedures can
be found in Woese (1987) or references cited therein.

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In dealing with prokaryotic evolution, one has to think on an entirely different time scale than when
dealing with classical (metazoan) evolution: the plant/animal/fungal branchings in Fig. 1 are relatively
superficial by comparison to some of the prokaryotic branchings (or, for that matter, to the protist
branchings on the eukaryotic lineage itself). Yet in defining microbial taxa we err in the opposite
direction, grossly underclassifying them relative to the metazoa: the human and the frog, two different
classes of animals, are separated by less evolutionary distance—about 5% in rRNA sequence terms—
than separates most species of the genus Bacillus. This taxonomic “double standard” undoubtedly
contributes to our mistaken (or at least exaggerated) impression that microbial evolution has a far more
protean quality than metazoan evolution.

The Two Prokaryotic Kingdoms

In general, the (eu)bacteria and archaea present rather different evolutionary pictures. The archaea are a
small but diverse collection of phenotypes—the methanogens, the extreme halophiles, the extreme
thermophiles, and the sulfate-reducing species (Balch et al., 1979; Jones et al., 1987 ; Stetter et al., 1987).
They differ in this respect from the bacteria, whose greater phenotypic variety appears at the same time
more connected, more interrelated. The tree shown in Fig. 1 can be interpreted to suggest that the
archaea in general evolve more slowly than bacteria do. While the majority of the bacterial phyla arise in
such a tight radiation that their exact order of
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branching has yet to be resolved, branching order among the major archaeal groups is readily
discernible. Photosynthesis is distributed among the bacteria in such a way as to suggest that it is a
fundamental bacterial characteristic, either being present in the ancestor common to all bacteria, or
arising very early in bacterial history (Woese, 1987). Archaeal photosynthesis, on the other hand, which
is based upon an entirely different mechanism than is bacterial photosynthesis (involving bacterial
rhodopsin [Stoeckenius, 1985]), appears to have arisen in, and is confined to, one relatively superficial
subline (Woese and Olsen, 1986). Aerobic phenotypes are plentiful among the bacteria, rare among
archaea (Woese, 1987). Thermophilic species, especially extreme thermophiles, are so numerous among
archaea that they are considered characteristic of the group; the majority of bacteria are mesophilic
(Woese, 1987).

The differences between archaea and bacteria run deep. Each has its own characteristic version of the
ribosomal RNAs, almost as different from one another as either is from eukaryotic rRNAs. And in their
ribosomal proteins the archaeal and bacterial versions tend to resemble one another less than the
former do the corresponding eukaryotic versions. Indeed, some archaeal ribosomal proteins do not even
have homologs among the bacteria; yet they do among the eukaryotes. Archaeal DNA-dependent RNA
polymerase finds its closest relative in one of the three eukaryotic polymerases (pol II), rather than in the
bacterial RNA polymerase, which is only distantly related to these two. This same story repeats itself in
most molecular systems studied in the archaea—in the ATPases, where archaeal and eukaryotic
versions are definitely more alike than either is like the bacterial version, in certain key factors involved
in the translation process, and in some DNA-associated proteins. To all this can be added the ways that
archaea are unique, such as their ether-linked lipids, methanogenic metabolism and the modifications
they make to certain bases in their tRNAs.

By comparing sequences of genes that appear to have been duplicated (and functionally diverged
somewhat) in the universal ancestral state, i.e., before any of the three major lineages emerged, it has
been possible to locate the root of the universal tree (Iwabe et al., 1989 ). The root occurs on the
bacterial branch of the tree (below the bacteria proper) shown in Fig. 1. If true, this means that archaea
are specific relatives of (and possibly resemble ancestral forms of) the eukaryotes!

By now, the reader is well aware that the unfamiliar term “archaea” is being used in lieu of the customary
term “archaebacteria” (and that “bacteria” is used instead of “eubacteria”). The term archaebacteria
incorrectly connotes a relationship to (eu)bacteria. Both are prokaryotes, but, as we have seen, this
reflects only cytological resemblance, not kinship. To view archaea as “just bacteria” in any sense is not
to appreciate their uniqueness. Therefore, specifically to overcome the misleading connotation of the
term “archaebacteria” and generally to bring formal taxonomy into line with the natural system emerging
from molecular data, a new formal system of organisms has been proposed (Woese et al., 1990 ), in
which at the highest taxonomic level all life is divided into three “domains”—the Bacteria, the Archaea,
and the Eucarya. Within each domain, there are two or more kingdoms (for example, the Animalia and
Plantae within the Eucarya).

A detailed phylogenetic tree for the Archaea is shown in Fig. 2 (Woese and Olsen, 1986; Woese,
1987; Achenbach-Richter et al., 1987b). The root of the tree divides the Archaea into two main
lineages. One, the kingdom Crenarchaeota (Woese et al., 1990) is a phenotypically pure collection
of extreme thermophiles. The other, the kingdom Euryarchaeota (Woese et al., 1990) is a diverse
collection of lineages that collectively embrace all four of the major archaeal phenotypes
(Achenbach-Richter et al., 1988). On this latter, cosmopolitan branch of the tree a group of typical
extreme thermophiles, members of the genus Thermococcus, provides the deepest branching,
which is succeeded by the branching of the sulfate reducers (the genus Archaeoglobus). The three
methanogen branchings then follow, the Methanococcales being the deepest branching among
them. This branching pattern suggests that methanogenic metabolism somehow arose from the
sulfur-reducing thermophilic metabolism of Thermococcus-like entities (perhaps through the
intermediary of a sulfate-reducing metabolism) and that the biochemistry of the extreme
halophiles originated in methanogenic biochemistry.

Fig. 2. Phylogenetic tree for the Archaea. The tree, produced as described in the caption to Fig. 1, was rooted using
outgroup sequences from the other two domains. The positions in the alignment used for the analysis met two
conditions: 1) they were represented by a known nucleotide in all archaeal sequences used; and 2) at least 50% of
the sequences showed the same composition at a given position. The three major methanogen groups are indicated
by roman numerals. Generic abbreviations are: Mc., Methanococcus; Mt., Methanothermus; M., Methanobacterium;
Ms.,

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Methanospirillum; Mp., Methanoplanus; Msa., Methanosarcina; Mth., Methanothrix; H., Halobacterium; T.,
Thermoplasma; A., Archaeoglobus; Tc., Thermococcus; Tp., Thermoproteus; Tf., Thermofilum; P., Pyrodictium; S.,
Sulfolobus; and D., Desulfurococcus.

Fig. 3 provides a comparably detailed look at the bacteria (Woese, 1987). The lowest branching in this
case involves the Thermotogales lineage, a little-studied but very interesting group of thermophiles.
While one or two other branchings from the common stem can be discerned above this, the bulk of the
major bacterial lineages arise in an unresolved radiation. If one accepts that the most ancient
stromatolites (3.5 billion years old [ Walter, 1983]) were produced by photosynthetic bacteria (as
stromatolites are today), then it appears that at least the earliest photosynthetic bacteria (the green
nonsulfur bacterium, Chloroflexus, being an example) had evolved by that time.

Fig. 3. Phylogenetic tree for the Bacteria. The tree was produced as described in the captions of Figs. 1 and 2. The
alignment used comprised one to three representative sequences from each of the 11 recognized bacterial phyla.

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A reasonable argument can be made to the effect that both prokaryotic domains arose from
thermophilic ancestors (Achenbach-Richter et al., 1987a; Woese, 1987). The case is stronger for the
archaea: 1) No mesophilic lineages have been found on the crenarchaeal side of the archaeal tree
although they have been looked for extensively—strongly suggesting that this branch of the
Crenarchaeota has a thermophilic origin; 2) only the extreme thermophile phenotype is found on both
main branches of the archaeal tree; 3) both the Methanococcales and the Methanobacteriales contain
species that grow at very high temperatures; these define the deepest branchings in each group and so
presumably represent the group's ancestral phenotype; and 4) the shortest lineages in the tree are all
associated with thermophilic species of one kind or another. (A short lineage implies that the phenotype
is relatively little changed from some common ancestral phenotype.) The analogous argument for the
bacteria is based upon the fact that on one side of that tree, only thermophilic species are known (the
Thermotogales group), and their lineages are shorter than those of other bacteria, while on the other
side, thermophilic lineages are at least common, particularly among the deeper branching lineages, e.g.,
the green nonsulfur bacteria and the deinococcus-thermus group (Achenbach- Richter et al., 1987a;
Woese, 1987). A thermophilic origin for all prokaryotes is in keeping with the geologist's picture of early
earth, a planet whose biosphere was far warmer than it is today (Walker et al., 1983; Worsley et al.,
1986).

Mechanism of Prokaryotic Evolution: Its Relationship to

Geologic Change
In that prokaryotic evolution spans almost the entire history of this planet, and that prokaryotes have
such an intimate connection with certain types of geologic processes, one of the more interesting
classes of questions the microbiologist faces concerns the relationship between prokaryotic evolution
and geologic change—what geologic events influenced prokaryotic evolution and how they did so; how
prokaryotic evolution in turn effects changes in the biosphere; etc. These are certainly questions for the
future, but the beginnings of understanding seem to be visible in the little we have discovered so far
about prokaryotic evolution.

The strongest correlation emerging from molecular phylogenetic measurements of prokaryotes is that
the rate of evolution measured at the genotypic (i.e., sequence) level is in some way
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connected with the types of change that occur at the overlying phenotypic level; The more rapid the
rate of evolution at the genotypic level (one manifestation of which is a lineage on a phylogenetic tree
that is abnormally long), the more unusual and atypical are the resulting phenotypic changes. Such a
“tempo-mode” relationship has been observed, extensively documented, and discussed on the
metazoan level in paleontological terms for many years (Mayr, 1942; Simpson, 1944). It is only recently
that what appears to be its counterpart on the cellular and molecular level has been encountered in the
prokaryotic world (Woese et al. 1985; Woese, 1987).

It is by no means a straightforward matter to identify an “unusual” or “atypical” prokaryotic phenotype.

Different organisms tend to be characterized in different noncomparable ways; and the judgement
“atypical” is subjective in any case. A useful direction to develop here may be the comparison of
genotypic classification of species (based upon some chronometer such as rRNA) to their numerical
taxonomic classification (where the latter does not include molecular sequence data). Those organisms
whose phenotypes are “unusual” compared to their relatives should tend to show a discrepancy
between their genotypic and phenotypic (numerical taxonomic) classifications. On a cruder level this can
already be seen when species that actually belong to one genus are placed instead in some new genus.

The clearest examples of the tempo-mode relationship so far encountered are the mycoplasmas.
Phenotypically, mycoplasmas constitute a separate bacterial class; their uniqueness includes not only
lack of a cell wall, but also the small size of their genomes and certain biochemical and cytological
idiosyncrasies (Razin, 1978). Some biologists have gone so far as to declare them to be primitive forms
of life, unrelated specifically to bacteria (Wallace and Morowitz, 1973). By contrast, mycoplasmas
genotypically i.e., by rRNA sequence measure) are quite ordinary bacteria. The mycoplasma group
stems from the bacillus-lactobacillus-streptococcus lineage, which is one of a number of lineages within
the Gram-positive phylum; in other words, the mycoplasmas represent a relatively superficial branching
within the bacterial tree (Woese et al., 1980; Woese, 1987). What is unusual about the mycoplasmas by
this genotypic measure is that their individual lineages tend to be relatively long; they appear to be
evolving more rapidly than normal bacteria (Woese et al., 1980; Woese, 1987). Another unusual
characteristic of their rRNAs, which also appears to reflect their rapid evolution, is that the compositions
of the “highly conserved” positions in the molecule tend to be less conserved in this group (Woese et
al., 1980, 1985). Indeed all bacterial lineages that appear to be rapidly evolving show this same tendency
to alter the composition of the more conserved positions (Woese, 1987).

While this relationship between rapid rate and unusual phenotype is most clearly demonstrated by the
mycoplasmas, it can be seen in more typical bacteria as well—where its converse can also be
recognized; i.e., slow rates, as judged by shorter lineages and a higher than average tendency to
conserve composition of the “highly conserved” sequence positions, correlate with phenotypes that
would be described as typical or ancestral in a group. A number of examples of both types can be seen
among the Gram-positive bacteria and the purple bacteria (groups for which extensive sequence
collections now exist). Among the Gram-positive bacteria, examples of rapid evolution are Leuconostoc
oenos, Fusobacterium , Haloanaerobium, and the general group of “high GC” Gram-positive bacteria.
(The members of this last group have evolved an impressive variety of unusual and complex
morphological traits, as their taxonomic treatment by early bacteriologists amply demonstrates [Kluyver
and van Niel, 1936; Stanier and van Niel, 1941]). Typical or presumed ancestral Gram-positive
phenotypes would include organisms such as Clostridium, (e.g., C. pasteurianum), Lactobacillus (e.g., L.
casei), Bacillus, and Heliobacterium (its photosynthesis being taken as ancestral), all of which are
characterized on the genotypic level by relatively short lineages and relative high retention of
composition for the highly conserved sequence positions in 16S rRNA (Woese, 1987 ). Among the purple
bacteria, one sees Chromatium, whose phenotype can be judged ancestral and whose evolutionary
tempo gives evidence of being slow; as opposed, for example, to Haemophilus, an atypical “enteric”
bacterium that shows a decidedly rapid evolutionary tempo.

If it is true that drastic evolutionary change among prokaryotes invariably accompanies rapid
evolutionary rate, the question then becomes what brings about such rate increases. This discussion is
too long and too tenuous for the present context. Let me simply leave the reader with a few brief
comments: Increased evolutionary tempo among prokaryotes seems to reflect an increase in the
(optimum) mutation rate of a lineage. (Mycoplasmas are a special case because they have very small
genomes and so do not require mutation rates as low as those found among normal bacteria [ Woese,
1987].) This increase may be brought about by environmental factors, such as by being in unsuitable
niches, in which merely survival, rather than survival-of-the -fittest, is the criterion, and in which the
selection constraints in a sense are “internal,” rather than external

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(Woese, 1987). Under these conditions, an increased optimum mutation rate may not only be acceptable,
but even advantageous. Such evolutionary situations then produce evolutionary saltations, those major
changes that bring into existence new high-level taxa. Many, if not most, such evolutionary situations
will probably involve global environmental shifts—major changes in the physical state of the planet that
result in prolonged periods of relative instability. (This would explain the occurrence of major
evolutionary radiations.) Thus, it is conceivable that biologists in the future will find a close connection
between major evolutionary changes among prokaryotes and major changes in the state of the planet:
the history of prokaryotes that is written in their genes may also include a history of the planet itself.

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