The Biochemistry of Archaea (Archaebacteria)

633 Pages·1993·33.84 MB·English

by  M. Kates

THE BIOCHEMISTRY OF ARCHAEA (ARCHAEBACTERIA)
New Comprehensive Biochemistry
Volume 26
General Editors
A. NEUBERGER
London
L.L.M. van DEENEN
Utrecht
ELSEVIER
Amsterdam . London . New York . Tokyo
The Biochemistry of
Archaea (Archaebacteria)
Editors
M. Kates
Department of Biochemistry, University of Ottawa,
Ottawa, Ont. KIN 6N5, Canada
D.J. Kushner
Department of Microbiology, University of Toronto,
Toronto, Ont. M5S IA8, Canada
A.T. Matheson
Department of Biochemistry and Microbiology,
University of Victoria, Victoria, B.C. V5Z 4H4, Canada
1993
ELSEVIER
Amsterdam . London . New York . Tokyo
Elsevier Science Publishers B.V
PO. Box 21 1
1000 AE Amsterdam
The Netherlands
Library of Congress Cataloging-in-Publication Data
The Biochemistry of archaea (archaebacteria) I editors, M. Kates, D.J.
Kushner, A.T. Matheson.
p. cm. -- (New comprehensive biochemistry ; v. 26)
Includes bibliographical references and index.
ISBN 0-444-81713 -1 (acid-free paper)
1. Archaebacteria--Metabolism. 2. Archaebacteria--Molecular
aspects. I. Kates, Morris. 11. Kushner, Donn. 111. Matheson, A.
T. IV. Series
QD415.N48 vol. 26
[QR82.A69]
574.19’2 s--dc20
[589.9]
93-33456
CIP
ISBN 0 444 81713 1
ISBN 0 444 80303 3 (series)
01993 Elsevier Science Publishers B.V All rights reserved.
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V
Preface
In the last ten years, considerable information has accumulated on the biochemistry of
the archaea. Some aspects of this subject, such as bioenergetics, molecular biology and
genetics, membrane lipids, etc., have been dealt with in individual book chapters and
review articles in various treatises, but the subject as a whole has not yet been treated in
a comprehensive manner.
The present volume attempts to bring together recent knowledge concerning general
metabolism, bioenergetics, molecular biology and genetics, membrane lipid and cell-wall
structural chemistry and evolutionary relations, of the three major groups of archaea: the
extreme halophiles, the extreme thermophiles, and the methanogens. We have called upon
a number of experts, all actively involved in research on the above subjects to review
their specialized fields.
In the Introduction, C.R. Woese considers the evolutionary relationship of these
microorganisms to all other living cells. This is followed by a section on special metabolic
features of archaea, covered in Chapters 1 through 4, respectively, by: M.J. Danson on
central metabolism in archaea, including carbohydrate metabolism, the citric-acid cycle,
and amino-acid and lipid metabolism; VP. Skulachev on bioenergetics and transport in
extreme halophiles; L. Daniels on the biochemistry of methanogenesis; and P. Schonheit
dealing with bioenergetics and transport in methanogens and related thermophilic archaea.
A section on protein structural chemistry in archaea includes Chapters 5 through 7,
respectively, by: D. Oesterhelt on the structure and function of photoreceptor proteins in
the Halobacteriaceae; J. Lanyi on the structure and function of ion-transport rhodopsins
in extreme halophiles; and R. Hensel on proteins of extreme thermophiles. In a section
on cell envelopes (Chapters 8-10>, 0. Kandler and H. Konig discuss the structure
and chemistry of archaeal cell walls; M. Kates reviews the chemistry and function
of membrane lipids of archaea; and L.I. Hochstein covers membrane-bound proteins
(enzymes) in archaea.
Chapters 11 through 14 deal with aspects of molecular biology in archaea and include,
respectively, DNA structure and replication by P. Forterre; transcription apparatus by
W. Zillig et al.; translation apparatus by R. Amils et al.; and ribosomal structure and
function by A. Matheson et al.
The final chapters (1 5-1 7) deal with the molecular genetics of archaea: L. Schalkwyk
discusses halophilic genes; J. Reeve and J. Palmer describe genes of methanogens; and
R. Garrett and J.Z. Dalgaard discuss genes of extreme thermophiles.
In an epilogue, W.F. Doolittle presents an overview of all chapters in the larger context
of cellular evolution and our future understanding of this subject.
The editors trust that this volume is sufficiently comprehensive in scope to be of use
to researchers actively engaged or interested in various aspects of the biochemistry of
VI
archaea. They hope that it will also stimulate further studes of the topics covered, and
will open up new areas for investigation.
M. Kates
D.J. Kushner
A.T. Matheson
M. Kates et al. (Eds.), The Biochemiso of Archaea (Archaebacferia) vii
0 1993 Elsevier Science Publishers B.V. All rights reserved
INTRODUCTION
The archaea:
Their history and significance
Carl R. WOESE
Department of Microbiology, University of Illinois, Urbana, IL 61801, USA
1. Introduction
In November of 1977 the president of the National Academy of Sciences of the
United States announced to the world that the human growth hormone gene had been
cloned. This momentous accomplishment ushered in (or at least symbolized) the era of
medicalhndustrial genetic engineering which so strongly impacts society today. However,
the press coverage of this announcement was far less extensive than might have been
expected, for a completely unanticipated reason. Coincidentally, NASA had issued a
press bulletin announcing the discovery of a “third form of life” (which would become
known as the archaebacteria), and it was this that was splashed across the front pages
of the New York Times and other major newspapers, mentioned on the evening TV
news programs, and even drew a quip from Johnny Carson.
For the press and the public the discovery of the archaea was a highly significant event;
it had touched upon that age old basic human concern about where we come from - which
interested the layman more than the promise of a brighter tomorrow through biomedical
technology. The biology community, on the other hand (though not scientists in general),
had a decidedly different reaction. For them the cloning of the somatotropin gene was
an important milestone in the ceaseless efforts of biologists to cure disease. As regards
the discovery of a “third form of life”, however, biologists’ attitudes generally ranged
from skeptical to intensely negative. Some derisively rejected the claim out of hand.
One well-known biologist went so far as to suggest to one of my collaborators that he
publicly dissociate himself from the work. Another counseled one of the three major
US news magazines not to carry the story, and it didn’t. Unfortunately, very little of
this negative reaction was expressed in a scientifically proper way, i.e., in the scientific
literature. It would have been interesting and instructive to quote today.
Why did biologists react so differently than laymen (and other scientists) to the
discovery of the archaea, many even viewing the claim as bogus? Their reaction was
nothing new. It (the rejection, its vehemence, and the associated scorn) is a well-
recognized sociological phenomenon, which Thomas Kuhn discusses extensively in
his now classic work The Structure of ScientiJc Revolutions. What the discovery of
the archaea had done was counter the existing paradigm, cross one of biology’s deep
prejudices:
...
Vlll
All organisms except viruses can be assigned to one of two primary groups lprokaryotes and
eukaryotes] . . . descriptions of them can be found in the better textbooks of general biology,
a sure indication that they have acquired the status of truisms. [I]
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. [2]
To claim that a third primary group existed [3,4] was patently absurd!
As the reader might imagine, those of us involved in the discovery of the archaea had
ourselves experienced the same sense of incredulity when first confronted with the data.
How could there possibly be something that was neither eukaryotic nor prokaryotic?
Yet that seemed the only reasonable interpretation of the data. If so, then what we
all took for granted regarding prokaryotes and eukaryotes must be wrong. Once that
light dawned, the source of the problem was obvious: A prokaryote had originally
been defined as an organism that did not possess certain eukaryotic cellular features,
e.g., a membrane-bounded nucleus and mitochondria. Defined in this purely negative
way “prokaryote” could not be a phylogenetically meaningful grouping. Yet, this is
precisely what it had been taken to be - without any supporting evidence. When,
decades later, it became possible - through electron microscopy and molecular studies -
to redefine “prokaryote” (and “eukaryote”) in comparable, positive terms, and so, to
test the phylogenetic validity of the prokaryote taxon, the biologist, strangely, felt no
need to do so: Prokaryotes were “obviously” all related to one another; therefore, a few
representative cases would suffice. As a consequence, the generalizations that came to be
known as “prokaryotic characteristics” were all based on very few examples; they were,
by and large, merely characteristics of Escherichia coli and a few of its relatives. No
comprehensive characterization of prokaryotes, with the intent of testing their supposed
monophyletic nature, had ever been done!
This was a mistake of major proportions, for, among other things, it almost certainly
delayed the discovery of the archaea by at least a decade (see below). Such a logical
transgression might be excused among botanists and zoologists on the grounds that
they knew and cared little about prokaryotes. But, for the keepers of the prokaryote,
the microbiologists, never to have questioned their monophyletic nature would have
been unpardonable. As it turns out, this was not actually what happened; but what
did happen, nevertheless, had the same effect. Microbiologists of an earlier era were
very much concerned with the phylogenetic relationships among bacteria, and were,
therefore, skeptical of the idea that “prokaryote” represented a monophyletic grouping.
Yet, a few decades later, and for reasons that are hard even in retrospect to understand, this
critical scientific attitude was unaccountably replaced by a naive, unscientific acceptance
of “prokaryote” as a phylogenetically valid taxon. We will examine this unfortunate
transformation, so central to the history of the archaea, in some detail below.
My reason for saying that the prokaryote-eukaryote prejudice delayed the discovery of
the archaea by at least a decade is that (anecdotal) evidence for their existence had been
in the literature some time before 1977. These bits and pieces in retrospect constituted
a prima facie case that something might be wrong with the idea that prokaryote is a
monophyletic taxon, and the situation cried for deeper, more comprehensive investigation.
Yet, at the time no one came to this conclusion.
ix
The cards were definitely stacked against the discovery of the archaea, for in addition
to the hegemony of the prokaryote concept, other factors and prejudices worked to
prevent their emergence. The early evidence for the existence of the archaea came in
the main from an odd collection of organisms that lived in “extreme” environments.
At that time conventional wisdom held that organisms living in extreme environments
represent evolutionary adaptations to their environments, and such adaptations required
an organism to undergo unusual phenotypic changes. Thus, not only were all bacteria
by definition “prokaryotic”; but anything that was atypical and lived in an “extreme”
environment was atypical by reason of that circumstance. The case for the archaea was
not helped either by the fact that the key organisms in question were very unlike one
another in their overall phenotypes, making it particularly difficult for even the best
microbiologists to sense their relationship. To make matters worse, idiosyncrasy could
also be found scattered among (what turned out to be) the (eu)bacteria as well. And, of
course, since the natural relationships among bacteria were not understood, there was no
basis for sorting any of this out.
One early piece in the archaeal puzzle was methanogenesis, an unusual biochemistry
that involved a variety of new coenzymes [5,6]. Except for this common biochemistry,
however, methanogens seemed to have little in common (morphologically, that is)
with one another. What did this mean? To those who took morphology as a primary
indicator of relationship it meant only that patches of methanogenic metabolism existed
scattered across the phylogenetic landscape, a view reflected in the seventh edition of
Bergey’s Manual [7]. To those who took physiology as a primary indicator of relationship,
methanogens constituted a phylogenetically coherent, separate, taxon, the view that
prevailed in the Manual’s eighth edition [8]. Despite their highly unusual biochemistry,
however, methanogens were never perceived as anything but typical “prokaryotes” in the
phylogenetic sense.
Another early piece of the puzzle was the unusual isoprenoid ether linked type of
lipid found by Morris Kates and his colleagues in the extreme halophiles (refs. [9,10];
see Chapter 9 of this volume]. This sort of lipid was also to be discovered in
Thermoplasma [ 11 1 and in Sulfolobus [ 12,131 before 1977, but was not discovered in
the methanogens [13a] until after the archaea were recognized as a group. Yet, no
phylogenetic connection among the organisms that possessed them was considered.
Conventional wisdom held firm; adaptation to extreme environments had somehow
caused those “unrelated” lineages all to independently arrive at the same unusual lipid
structure [ 121.
The fact that Sulfolobus and Thennoplasma have similar lipids is of interest, but almost certainly
this can be explained by convergent evolution. This hypothesis is strengthened by the fact that
Hulobacterium, another quite different organism, also has lipids similar to those of the two
acidophilic thermophiles.[ 141
These same organisms shared another peculiar characteristic: cell walls that did not
contain peptidoglycan; and this was known to be true even for a methanogen [ 15-17]. Still,
no phylogenetic interpretation followed; but in fairness it should be noted that the walls
of certain (eu)bacteria, such as the planctomyces, also contain no peptidoglycan [ 181.
The extreme halophiles in addition possessed peculiar ribosomes, which contained
acidic, rather than basic, proteins [ 191. While this fact alone carried no obvious