Next Article 
Journal of Bacteriology, June 1999, p. 3613-3617, Vol. 181, No. 12
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
GUEST COMMENTARY
Archaebacteria Then ... Archaes
Now (Are There Really No Archaeal Pathogens?)
John N.
Reeve*
Department of Microbiology, The Ohio State
University, Columbus, Ohio 43210
 |
TEXT |
In 1977, Carl Woese and George Fox
argued that although methanogens looked like bacteria, they had very
different cell wall structures and unique methanogenesis-related
coenzymes and RNase T1 digestion of methanogen 16S rRNAs generated
oligonucleotides so different from those from bacterial 16S rRNAs and
from eukaryotic 18S rRNAs that methanogens should be placed in a third
phylogenetic urkingdom, the Archaebacteria (81).
They conceded that "almost nothing is known regarding their molecular
biology" but concluded that "there is no reason at present to
consider methanogens as any closer to eubacteria than to the
cytoplasmic component of the eukaryote." This started a scientific
debate that has continued with unabated vigor for over 20 years. In
1977, methanogens were the only Archaebacteria, and not many
more were predicted (81), but by 1980 the archaebacterial
urkingdom had already grown to include halophiles and
thermoacidophiles, and the presence of an RNA polymerase with a complex
subunit configuration similar to eukaryotic RNA polymerases had been
added to the list of definitive archaebacterial features
(29). The 16S rRNA sequence data were by then presented in
the now familiar phylogenetic tree format, and the three urkingdoms
were shown arising independently from a common, less complex ancestor
designated the progenote. It was tempting to comment here on the past
and present arguments for and against the urkingdom concept, the number
of urkingdoms, the branching relationships in the 16S rRNA phylogenetic
tree, and the nature of the progenote, the universal and last common
ancestors of all life (6, 9, 30, 32, 39, 49, 50, 54, 78, 81-83). But instead, from my perspective it seemed more
appropriate to review how the revolutionary/heretical archaebacterial
proposal has been investigated experimentally. What has been done, what were the driving forces for the research undertaken, what do we know
now, what have complete archaeal genome sequences contributed, and
what's next?
As the commentary's title highlights, there are language problems. In
1985, a volume of The Bacteria monograph series appeared with the subtitle Archaebacteria (83), and in my
review of this book for ASM News (62), I noted the apparent
contradiction between the title and subtitle and the inherent
difficulty in accepting the premise that Archaebacteria were
not Bacteria when they had bacteria in their name. In 1990, Carl Woese, Otto Kandler, and Mark Wheelis changed the name to
Archaea, eubacteria became Bacteria, eucaryotes
became Eucarya, and urkingdoms became domains
(82). This has helped, but difficulties still remain. We
used the domain terms in the first paper published after their
introduction (67) but were unsure then of the singular forms
and adjectives. Now it is generally accepted that a methanogen is an
archaeon (although occasionally an archaeum), Escherichia
coli remains a bacterium, but yeast has never become a eucaryum.
Eucarya does appear in microbiology journals (with k
sometimes replacing c) but almost never elsewhere, archaeal and
bacterial are often used together with eucaryotic rather than with
eucaryal (9), and archaes is a more easily spoken plural
widely used in oral presentations and conversations. Although not
chronologically accurate, the 1990 terms are used here throughout.
In 1977, I didn't read the 1977 paper (81); I
was working at the Max Planck Institut für Molekular Genetik in
West Berlin on phage infection of minicells. However, in 1979, I moved to The Ohio State University (OSU) and occupied a laboratory next door
to Jim Frea, a cultivator of methanogens, and shortly thereafter Paul
Hamilton, a beginning OSU graduate student, brought the 1979 review of
methanogens by Balch et al. (5) to my attention. Paul argued
that if methanogens were as different as the review claimed then
looking at their genes should reveal interesting novelties. Apparently,
no one had cloned a protein-encoding archaeal gene, and so with
methanogen cell paste provided by Jim Frea, Paul set out to clone
methanogen genes by complementing E. coli auxotrophs. He was
almost immediately successful. Methanogen genomic DNAs shotgun cloned
into E. coli complemented E. coli arginine, proline, histidine, and purine auxotrophs, and the complementation was
independent of the orientation of cloning. This seemed a very surprising result that not only confirmed that methanogens and, by
inference, all Archaea used the standard genetic code but
also that E. coli RNA polymerase recognized archaeal
promoters. Without sequencing the cloned DNA, we submitted this work
for publication, but it was (correctly) rejected as premature. Later,
after almost 3 years of Maxam-Gilbert sequencing, we wrote the
"cloned and sequenced" paper that provided evidence for archaeal
operons, ribosome binding sites, and a methanogen insertion sequence
element (34), and Jordan Konisky's group had also
documented complementation of bacterial auxotrophs by cloned methanogen
genes (18, 84). However, there was still an uncomfortable
suspicion that all methanogen cultures might be contaminated with
anaerobic Bacteria and that the complementing genes were
cloned from bacterial contaminants, but cloning from single-colony
isolates and exchanges of cultures finally eliminated this concern. The
intergenic regions in the cloned methanogen DNAs were very AT rich and
contained sequences that conformed to the consensus sequences for the
AT-rich 
10 and 35 elements of E. coli promoters. We
therefore assumed, but never proved, that these sequences functioned
fortuitously as promoters directing transcription of the cloned
methanogen genes in E. coli and also in Bacillus
subtilis (55).
The first report of a cloned and sequenced archaeal protein-encoding
gene was actually published in 1981 (25). Gobind Khorana and
colleagues cloned the bop gene that encodes bacterio-opsin in Halobacterium halobium as a cDNA following reverse
transcription of purified mRNA. However, to obtain synthesis of
recombinant bacterio-opsin in E. coli, they constructed an
entirely synthetic bop gene (24). bop
transcription in H. halobium was shown to initiate only 2 bp
upstream from the ATG translation-initiating codon (20), the
first example of the now frequent observation of transcription
initiating at or close to the site of translation initiation in
nonmethanogenic Archaea. How translation of the resulting
leaderless mRNAs is initiated remains an open question, and although
most methanogen mRNAs do have 5' leaders with sequences appropriately
positioned to function as ribosome binding sites, this function has not
yet been experimentally documented.
Through the 1980s, archaeal research was reported regularly at
international symposia, and review volumes from these meetings provide
accurate historical perspectives of the then state of the art (42,
43, 63). Cell envelope structures, analogs but not homologs of
bacterial peptidoglycan, and membrane lipids that contained ether
rather than ester linkages were described in detail. Lipids with ether
linkages in Bacteria and Eucarya have also
occasionally been reported, but lipids with branched isoprenoid side
chains attached to the glycerol backbone in the sn-2 and sn-3
configuration remain unique to Archaea (56).
Antibiotic sensitivity and resistance profiles were determined to probe
for the presence of target structures and to identify antibiotic
resistance genes and phenotypes for use in genetics. Consistent with
having different cell envelope structures and hinting at differences in
DNA replication, transcription, and translation, Archaea
were found to be resistant to almost all antibacterial antibiotics, and
sensitivity to aphidicolin and diphtheria toxin argued for the presence
eucarya-like targets. The number of archaeal genes cloned and sequenced
increased, but when Jim Brown surveyed the literature to write a
comprehensive review in 1988, there were still only 46 methanogen, 13 halophile, and 6 Sulfolobus protein-encoding archaeal gene
sequences available to evaluate (10). A larger number of
archaeal tRNA-, rRNA-, and 7S RNA-encoding sequences were known, and
the presence of introns in some of these stable RNA-encoding genes
(41, 46) seemed a persuasive argument for an
archaeal-eucaryal relationship that excluded Bacteria.
However, archaeal mRNAs lacked introns (still the case), did not have a 5' cap structure, and had only very short 3' poly(A) tails
(11). Archaea have since been shown to contain
fibrillarin homologs (3) and small nucleolar RNA-like
molecules (60), and common features in the maturation and
removal of introns from stable RNAs in Archaea and
Eucarya have been established (47, 76), but
archaeal genome sequences provide no hints of an archaeal spliceosome
(12, 44, 48, 70).
With the energy crises, interest in pollutant bioremediation, and
discovery of hyperthermophiles, applied goals were added in the 1980s
to archaeal research. The Department of Energy (DOE), Gas Research
Institute, and Environmental Protection Agency provided support in the
United States to investigate methanogens with an eye to improving
methanogenesis as the terminal step in anaerobic waste biodegradation
and for biogas production, and the Office of Naval Research established
a 5-year program to investigate Archaea and survival
mechanisms in extreme environments. With this financial support,
studies of the ecology, biochemistry, and molecular biology of
methanogens and of extremophiles (as they are now known) progressed
well, adding data to a foundation that now supports regular Gordon and
Keystone conferences on Archaea and the molecular
biology and metabolism of C1 compounds and international symposia on
thermophily and extremophiles. The anticipated practical developments
have however been limited, primarily by the recalcitrance of
Archaea to genetics and genetic engineering. Transformation systems are now established for representative halophiles, methanogens, and hyperthermophiles, but there is still very little real genetics. Such fanciful 1980's ideas as constructing a photosynthetic methanogen with pollutant-biodegrading ability and facile genetic engineering of
temperature and salt tolerance into industrial microorganisms remain
remote and unrealistic.
Although recognized early as an archaeal feature (29), the
complex, eucarya-like subunit composition of archaeal RNA polymerases was not extended into a functional homology until the 1990s. Archaeal promoters were then found to contain a TATA-box element, and Michael Thomm's group established that archaeal transcription initiation required two transcription factors in addition to the RNA polymerase which, subsequently, were shown to be structural and functional homologs of eucaryal TATA-binding protein (TBP) and transcription factor IIB (21, 35, 51, 61, 65, 71, 73). Based on the
eucaryal paradigm, it appears that promoter-specific archaeal transcription factors must interact with regulatory DNA sequences and/or with an archaeal RNA polymerase-containing preinitiation complex
to regulate transcription initiation, although some Archaea contain several TBPs (65, 71) which could function in a
manner analogous to that of alternative sigma factors in
Bacteria. The discovery of histones in Archaea in
1990 added another unambiguously eucaryal feature (67).
Archaeal histones lack the N- and C-terminal regulatory extensions of
their eucaryal homologs but do form the histone fold (72)
and wrap DNA into structures, archaeal nucleosomes (58),
that are very similar to the structure at the center of the eucaryal
nucleosome formed by the histone (H3 + H4)2 tetramer (52, 59). Not all Archaea have histones, and
those that do not have a variety of other "histone-like" DNA
binding proteins. Apparently many unrelated small DNA binding proteins
can solve the genome packaging problem for bacterial (69)
and archaeal (68) procaryotes, but only the
histone-wrapping-DNA-into-nucleosomes solution remained effective when
genome size increased substantially with eucaryal development.
Investigations of heat shock and stress responses have identified
archaeal homologs of bacterial and eucaryal chaperonins
(75), and archaeal hsp60s with sequences related to the
eucaryal cytosolic TCP1 chaperonins form proteasomes (designated thermosomes) with subunits similarly assembled into hexadecameric rings. However, as is the case for archaeal transcription
initiation complexes and nucleosomes, archaeal proteasomes appear
to be reduced, simplified versions of their eucaryal homologs. They
contain only 
and 
subunits, whereas eucaryal TCP1 proteasomes
contain at least eight different subunits (53, 85).
In 1994, the DOE again boosted archaeal research by promoting and
supporting archaeal genome sequencing, and now four archaeal genome
sequences have been published (12, 44, 47, 70) and several
more are nearing completion. What was learnt immediately? That
methanogens, absolute autotrophs that conserve energy and synthesize
themselves in toto from just three gases (CO2,
H2, and N2) and salts have genomes less than
40% the size of the E. coli genome. Based on the
differences in the two methanogen genome sequences (12, 70),
as little as 1.2 Mbp may be sufficient to encode a fully independent,
autotrophic cell. Genome neighborhoods and operon organizations are not
well conserved, and although most components of the central dogma
machinery (DNA, RNA, and protein synthesis and modification activities)
do have sequences more closely related to their eucaryal than bacterial
counterparts, most archaeal metabolic enzymes have sequences more
similar to bacterial than eucaryal enzymes (66, 70). There
is evidence for interspecies gene transfer having occurred on a large
scale (4) and support for the progenote concept
(81) in which the universal ancestor was not an individual
but rather a genetically intermingling community. The small-subunit
rRNA tree is no longer viewed as reflecting the early evolution of
whole organisms but rather "in its deep branches,...is merely a
gene tree" (80).
Where next in archaeal research? An entirely new family of DNA
polymerases has been discovered (14) which will be studied in detail, together with novel topoisomerases, including a relative of
enzymes involved in eucaryal meiotic recombination (7, 28). Reassembling an active archaeal RNA polymerase from individual subunits
(19, 27) and establishing an in vitro transcription system
that exhibits regulation are now urgent projects. Based on in vivo
results, archaeal transcription factors will be identified and
characterized that participate in the hydrogen and metal regulation of
methane gene expression (36, 64), ammonia regulation of nif and glnA expression (17),
substrate induction of catabolic enzymes (1, 23),
biosynthetic pathway expression, gas vacuole synthesis, prophage
induction (71), and the heat shock response (16, 40,
74). Progress has already been made in determining how some UGA
codons direct selenocysteine incorporation in Archaea (79), but now it appears that UAG can also function as a
sense codon in Methanosarcina species, promising another
intriguing archaeal novelty (13). Determining how
macromolecules, cofactors, and metabolites maintain their structure and
functional integrity under extremophile growth conditions remains a
major research challenge, and the obvious potential of extremophiles
for biotechnological applications ensures their continued intense
investigation. Ribulose bisphosphate carboxylase/oxygenase
(RubisCo) was recently documented in hyperthermophilic, anaerobic
Archaea (77), and enzymes and cofactors
previously considered unique to methanogenesis were found in
methylotrophic Bacteria (15). Research to
determine what these surprisingly "misplaced" enzymes do is
undoubtedly already well underway. The apparent lack of lysyl-tRNA
synthetase genes in some archaeal genome sequences provoked experiments
that have dramatically advanced amino acyl-tRNA synthetase biochemistry and phylogenetics (37, 38), and pursuing the still-missing cysteinyl-tRNA synthetase genes should similarly soon provide new
insights (45). Archaeal cell cycle studies have only
recently begun (8), but the presence of a combination of
bacterial ftsZ and minD homologs (31)
(back to minicell research?) and eucaryal cdc homologs
(12, 44, 48, 70) promises an interesting mixture of
features. Identifying an archaeal origin of DNA replication would be a
valuable first step (26).
Finally to the commentary title's parenthetical question. Support from
the more mission-oriented U.S. funding agencies has played a vital role
in developing archaeal research in the United States, and a European
community initiative has similarly supported a consortium of
~40 research groups to investigate extremophile biology,
predominantly archaeal projects, explicitly aimed at biotechnology
development (2). Recently, following the Martian meteorite
excitement, the National Science Foundation established a Life in
Extreme Environments (LExEN) initiative and the National Aeronautics
and Space Administration founded the astrobiology program. Funding for
environmental and ecological studies of Archaea should
therefore now increase, and hopefully this will expedite the isolation
and characterization of the many globally important (paradoxically)
nonextremophile Archaea that currently defy laboratory cultivation (22, 57). But what about an archaeal animal,
plant, or insect pathogen that might encourage more interest and
support from the National Institutes of Health? Methanogens live as
intracellular symbionts (33) and inhabit the rumen and lower
digestive tracts of animals and insects, so they know how to interact
with a host, but do they never cause problems? As Archaea
are innately resistant to almost all clinically and agriculturally used
antibiotics, surely there should be an occasional opportunistic
archaeal infection, but where are the reports? Could Archaea
be such clever pathogens that we don't recognize them as the true
causative agents of disease?
| |
ACKNOWLEDGMENTS |
Archaeal research in my laboratory at The Ohio State
University has been supported by grants from the Department of Energy, Environmental Protection Agency, Gas Research Institute, Office of
Naval Research, National Science Foundation, National Institutes of
Health, and North Atlantic Treaty Organization.
I thank the students and postdoctoral scientists who have contributed
to the work and ideas discussed and G. Dilworth, E. Eisenstadt, P. Harriman, R. Rabson, and A. Venosa for their long-term interest, help,
and support.
| |
FOOTNOTES |
*
Mailing address: Department of Microbiology, The Ohio
State University, Columbus, OH 43210. Phone: (614) 292-2301. Fax: (614) 292-8120. E-mail: reeve.2{at}osu.edu.
The views expressed in this Commentary do not necessarily
reflect the views of the journal or of ASM.
| |
REFERENCES |
| 1.
|
Adams, M. W. W., and A. Kletzin.
1996.
Oxidoreductase-type enzymes and redox proteins involved in fermentative metabolisms of hyperthermophilic archaea.
Adv. Protein Chem.
48:101-180[Medline].
|
| 2.
|
Aguilar, A.
1996.
Extremophile research in the European Union: from fundamental aspects to industrial expectations.
FEMS Microbiol. Lett.
18:89-92.
|
| 3.
|
Amiri, K. A.
1994.
Fibrillarin-like proteins occur in the domain Archaea.
J. Bacteriol.
176:2124-2127[Abstract/Free Full Text].
|
| 4.
|
Aravind, L.,
R. L. Tatusov,
Y. I. Wolf,
R. D. Walker, and E. V. Koonin.
1998.
Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles.
Trends Genet.
14:442-444[Medline].
|
| 5.
|
Balch, W. E.,
G. E. Fox,
L. J. Magrum,
C. R. Woese, and R. S. Wolfe.
1979.
Methanogens: reevaluation of a unique biological group.
Microbiol. Rev.
43:260-296[Free Full Text].
|
| 6.
|
Baldauf, S. L.,
J. D. Palmer, and W. F. Doolittle.
1996.
The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny.
Proc. Natl. Acad. Sci. USA
93:7749-7754[Abstract/Free Full Text].
|
| 7.
|
Bergerat, A.,
B. de Massy,
D. Gadelle,
P.-C. Varoutas,
A. Nicholas, and P. Forterre.
1997.
An atypical topoisomerase II from archaea with implications for meiotic recombination.
Nature
386:414-417[Medline].
|
| 8.
|
Bernander, R., and A. Poplawski.
1997.
Cell cycle characteristics of thermophilic Archaea.
J. Bacteriol.
179:4963-4969[Abstract/Free Full Text].
|
| 9.
|
Brown, J. R., and W. F. Doolittle.
1997.
Archaea and the prokaryote-to-eukaryote transition.
Microbiol. Mol. Biol. Rev.
61:456-502[Abstract].
|
| 10.
|
Brown, J. W.,
C. J. Daniels, and J. N. Reeve.
1989.
Gene structure, organization, and expression in Archaebacteria.
Crit. Rev. Microbiol.
16:287-338[Medline].
|
| 11.
|
Brown, J. W., and J. N. Reeve.
1985.
Polyadenylated, noncapped RNA from the archaebacterium Methanococcus vannielii.
J. Bacteriol.
162:909-917[Abstract/Free Full Text].
|
| 12.
|
Bult, C. J.,
O. White,
G. J. Olsen,
L. Zhou,
R. D. Fleischmann,
G. G. Sutton,
J. A. Blake,
L. M. FitzGerald,
R. A. Clayton,
J. D. Gocayne,
A. R. Kerlavage,
B. A. Dougherty,
J.-F. Tomb,
M. D. Adams,
C. I. Reich,
R. Overbeek,
E. F. Kirkness,
K. G. Weinstock,
J. M. Merrick,
A. Glodek,
J. L. Scott,
N. S. M. Geoghagen,
J. F. Weidman,
J. L. Fuhrmann,
D. Nguyen,
T. R. Utterback,
J. M. Kelley,
J. D. Peterson,
P. W. Sadow,
M. C. Hanna,
M. D. Cotton,
K. M. Roberts,
M. A. Hurst,
B. P. Kaine,
M. Borodovsky,
H.-P. Klenk,
C. M. Fraser,
H. O. Smith,
C. R. Woese, and J. C. Venter.
1996.
Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii.
Science
273:1058-1073[Abstract].
|
| 13.
|
Burke, S. A.,
S. L. Lo, and J. A. Krzycki.
1998.
Clustered genes encoding the methytransferases of methanogenesis from monomethylamine.
J. Bacteriol.
180:3432-3440[Abstract/Free Full Text].
|
| 14.
|
Cann, I.,
K. Komori,
H. Toh,
S. Kanai, and Y. Ishino.
1998.
A heterodimeric DNA polymerase: evidence that members of euryarchaeota possess a distinct DNA polymerase.
Proc. Natl. Acad. Sci. USA
95:14250-14255[Abstract/Free Full Text].
|
| 15.
|
Chistoserdova, L.,
J. A. Vorholt,
R. K. Thauer, and M. E. Lidstrom.
1998.
C1-transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic archaea.
Science
281:99-102[Abstract/Free Full Text].
|
| 16.
|
Clarens, M.,
A. J. L. Macario, and E. Conway de Macario.
1995.
The archaeal dnaK-dnaJ gene cluster: organization and expression in the methanogen Methanosarcina mazei.
J. Mol. Biol.
250:191-201[Medline].
|
| 17.
|
Cohen-Kupiec, R.,
C. J. Marx, and J. A. Leigh.
1999.
Function and regulation of glnA in the methanogenic archaeon Methanococcus maripaludis.
J. Bacteriol.
181:256-261[Abstract/Free Full Text].
|
| 18.
|
Cue, D.,
G. S. Beckler,
J. N. Reeve, and J. Konisky.
1985.
Structure and sequence divergence of two archaebacterial genes.
Proc. Natl. Acad. Sci. USA
82:4207-4211[Abstract/Free Full Text].
|
| 19.
| Darcy, T. J., W. Hausner, D. E. Awery, A. M. Edwards, M. Thomm, and J. N. Reeve. Methanobacterium
thermoautotrophicum RNA polymerase and transcription in vitro. J. Bacteriol., in press.
|
| 20.
|
DasSarma, S.,
U. L. RajBhandary, and H. G. Khorana.
1984.
Bacterio-opsin mRNA in wild-type and bacterio-opsin deficient Halobacterium halobium strains.
Proc. Natl. Acad. Sci. USA
81:125-130[Abstract/Free Full Text].
|
| 21.
|
DeDecker, B. S.,
R. O'Brien,
P. J. Fleming,
J. H. Geiger,
S. P. Jackson, and P. B. Sigler.
1996.
The crystal structure of a hyperthermophilic archaeal TATA-box binding protein.
J. Mol. Biol.
264:1072-1084[Medline].
|
| 22.
|
DeLong, E. F.,
K. Y. Wu,
B. B. Prézelin, and R. V. M. Jovine.
1994.
High abundance of Archaea in Antarctic marine picoplankton.
Nature
371:695-697[Medline].
|
| 23.
|
de Vos, W. M.,
S. W. M. Kengen,
W. G. B. Voorhorst, and J. van der Oost.
1998.
Sugar utilization and its control in hyperthermophiles.
Extremophiles
2:201-205.
[Medline] |
| 24.
|
Dunn, R. J.,
N. R. Hackett,
B. H. Chao,
K. Kimura, and H. G. Khorana.
1987.
Structure-function studies on bacteriorhodopsin. I. Expression of the bacteriorhodopsin gene in Escherichia coli.
J. Biol. Chem.
262:9246-9254[Abstract/Free Full Text].
|
| 25.
|
Dunn, R. J.,
J. McCoy,
M. Simsek,
A. Majumdar,
S. H. Chang,
U. L. RajBhandary, and H. G. Khorana.
1981.
The bacteriorhodopsin gene.
Proc. Natl. Acad. Sci. USA
78:6744-6749[Abstract/Free Full Text].
|
| 26.
|
Edgell, D. P., and W. F. Doolittle.
1997.
Archaea and the origin(s) of DNA replication.
Cell
89:995-998[Medline].
|
| 27.
|
Eloranta, J. J.,
A. Kato,
M. S. Teng, and R. O. J. Weinzierl.
1998.
In vitro assembly of an archaeal D-L-N RNA polymerase subunit complex reveals a eukaryote-like structural arrangement.
Nucleic Acids Res.
26:5562-5567[Abstract/Free Full Text].
|
| 28.
|
Forterre, P.,
A. Bergerat, and P. Lopez-Garcia.
1996.
The unique DNA topology and DNA topoisomerases of hyperthermophilic archaea.
FEMS Microbiol. Rev.
18:237-248[Medline].
|
| 29.
|
Fox, G. E.,
E. Stackebrandt,
R. B. Hespell,
J. Gibson,
J. Maniloff,
T. A. Dyer,
R. S. Wolfe,
W. E. Balch,
R. S. Tanner,
L. J. Magrum,
L. B. Zablen,
R. Blakemore,
R. Gupta,
L. Bonen,
B. J. Lewis,
D. A. Stahl,
K. R. Luehrsen,
K. N. Chen, and C. R. Woese.
1980.
The phylogeny of prokaryotes.
Science
209:457-463[Free Full Text].
|
| 30.
|
Galtier, N.,
N. Tourasse, and M. Gouy.
1999.
A non-hyperthermophilic common ancestor to extant life forms.
Science
283:220-221[Abstract/Free Full Text].
|
| 31.
|
Gerard, E.,
B. Labedan, and P. Forterre.
1998.
Isolation of a minD-like gene in the hyperthermophilic archaeon Pyrococcus AL585, and phylogenetic characterization of related proteins in the three domains of life.
Gene
222:99-106[Medline].
|
| 32.
|
Gupta, R. S.
1998.
What are archaebacteria: life's third domain or monoderm prokaryotes related to Gram-positive bacteria? A new proposal for the classification of prokaryotic organisms.
Mol. Microbiol.
29:695-707[Medline].
|
| 33.
|
Guzen, H. J.,
C. A. M. Broers,
M. Barughare, and C. K. Stumm.
1991.
Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalus in the cockroach hindgut.
Appl. Environ. Microbiol.
57:1630-1634[Abstract/Free Full Text].
|
| 34.
|
Hamilton, P. T., and J. N. Reeve.
1985.
Structure of genes and an insertion element in the methane producing archaebacterium Methanobrevibacter smithii.
Mol. Gen. Genet.
200:47-59[Medline].
|
| 35.
|
Hausner, W.,
J. Wettach,
C. Hethke, and M. Thomm.
1996.
Two transcription factors related with the eucaryal transcription factors TATA-binding protein and transcription factor IIB direct promoter recognition by an archaeal RNA polymerase.
J. Biol. Chem.
271:30144-30148[Abstract/Free Full Text].
|
| 36.
|
Hochheimer, A.,
R. Hedderich, and R. K. Thauer.
1999.
The DNA binding protein Tfx from Methanobacterium thermoautotrophicum: structure, DNA binding properties and transcriptional regulation.
Mol. Microbiol.
31:641-650[Medline].
|
| 37.
|
Ibba, M.,
H. C. Losey,
Y. Kawarabayasi,
H. Kikuchi,
S. Bunjun, and D. Söll.
1999.
Substrate recognition by class I lysyl-tRNA synthetases: a molecular basis for gene displacement.
Proc. Natl. Acad. Sci. USA
96:418-423[Abstract/Free Full Text].
|
| 38.
|
Ibba, M.,
S. Morgan,
A. W. Curnow,
D. R. Pridmore,
U. C. Vothknecht,
W. Gardner,
W. Lin,
C. R. Woese, and D. Söll.
1997.
A euryarchaeal lysyl-tRNA synthetase: resemblance to class I synthetases.
Science
278:1119-1122[Abstract/Free Full Text].
|
| 39.
|
Iwabe, N.,
K.-I. Kuma,
M. Hasegawa,
S. Osawa, and T. Miyata.
1989.
Evolutionary relationships of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes.
Proc. Natl. Acad. Sci. USA
86:9355-9359[Abstract/Free Full Text].
|
| 40.
|
Kagawa, H. K.,
J. Osipiuk,
N. Maltsev,
R. Overbeek,
E. Quaite-Randall,
A. Joackimiak, and J. D. Trent.
1995.
The 60 kDa heat shock proteins in the hyperthermophilic archaeon Sulfolobus shibatae.
J. Mol. Biol.
253:712-725[Medline].
|
| 41.
|
Kaine, B. P.,
R. Gupta, and C. R. Woese.
1983.
Putative introns in tRNA genes of prokaryotes.
Proc. Natl. Acad. Sci. USA
80:3309-3312[Abstract/Free Full Text].
|
| 42.
|
Kandler, O.
1982.
Proceedings of the First International Workshop on Archaebacteria.
Gustav Fischer Verlag, Stuttgart, Federal Republic of Germany.
|
| 43.
|
Kandler, O., and W. Zillig.
1986.
Archaebacteria `85.
Gustav Fischer Verlag, Stuttgart, Federal Republic of Germany.
|
| 44.
|
Kawarabayasi, Y.,
M. Sawada,
H. Horikawa,
Y. Haikawa,
Y. Hino,
S. Yamamoto,
M. Sekine,
S. Baba,
H. Kosugi,
A. Hosoyama,
Y. Nagai,
M. Sakai,
K. Ogura,
R. Otsuka,
H. Nakazawa,
M. Takamiya,
Y. Ohfuku,
T. Funahashi,
T. Tanaka,
Y. Kudoh,
J. Yamazaki,
N. Kushida,
A. Oguchi,
K. Aoki,
T. Yoshizawa,
Y. Nakamura,
F. T. Robb,
K. Horikoshi,
Y. Masuchi,
H. Shizuya, and H. Kikuchi.
1998.
Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3.
DNA Res.
5:55-76[Abstract].
|
| 45.
|
Kim, H.-S.,
U. C. Vothknecht,
R. Hedderich,
I. Celic, and D. Söll.
1998.
Sequence divergence of seryl-tRNA synthetases in Archaea.
J. Bacteriol.
180:6446-6449[Abstract/Free Full Text].
|
| 46.
|
Kjems, J., and R. A. Garrett.
1985.
An intron in the 23S ribosomal RNA gene of the archaebacterium Desulfurococcus mobilis.
Nature
318:675-677.
|
| 47.
|
Kleman-Leyer, K.,
D. W. Armbruster, and C. J. Daniels.
1997.
Properties of H. volcanii tRNA intron endonuclease reveal a relationship between the archaeal and eucaryal tRNA intron processing systems.
Cell
89:839-847[Medline].
|
| 48.
|
Klenk, H.-P.,
R. A. Clayton,
J.-F. Tomb,
O. White,
K. E. Nelson,
K. A. Ketchum,
R. J. Dodson,
M. Gwinn,
E. K. Hickey,
J. D. Peterson,
D. L. Richardson,
A. R. Kerlavage,
D. E. Graham,
N. C. Kyrpides,
R. D. Fleischmann,
J. Quackenbush,
N. H. Lee,
G. G. Sutton,
S. Gill,
E. F. Kirkness,
B. A. Dougherty,
K. McKenney,
M. D. Adams,
B. Loftus,
S. Peterson,
C. I. Reich,
L. K. McNeil,
J. H. Badger,
A. Glodek,
L. Zhou,
R. Overbeek,
J. D. Gocayne,
J. F. Weidman,
L. McDonald,
T. Utterback,
M. D. Cotton,
T. Spriggs,
P. Artiach,
B. P. Kaine,
S. M. Sykes,
P. W. Sadow,
K. P. D'Andrea,
C. Bowman,
C. Fujii,
S. A. Garland,
T. M. Mason,
G. J. Olsen,
C. M. Fraser,
H. O. Smith,
C. R. Woese, and J. C. Venter.
1997.
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus.
Nature
390:364-370[Medline].
|
| 49.
|
Lake, J. A.
1994.
Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances.
Proc. Natl. Acad. Sci. USA
91:1455-1459[Abstract/Free Full Text].
|
| 50.
|
Lake, J. A.,
M. W. Clark,
E. Henderson,
S. P. Fay,
M. Oakes,
A. Scheinman,
J. P. Thornber, and R. A. Mah.
1985.
Eubacteria, halobacteria, and the origin of photosynthesis: the photocytes.
Proc. Natl. Acad. Sci. USA
82:3716-3720[Abstract/Free Full Text].
|
| 51.
|
Langer, D.,
J. Hain,
P. Thuriaux, and W. Zillig.
1995.
Transcription in Archaea: similarity to that in Eucarya.
Proc. Natl. Acad. Sci. USA
92:5768-5772[Abstract/Free Full Text].
|
| 52.
|
Luger, K.,
A. W. Mäder,
R. K. Richmond,
D. F. Sargent, and T. J. Richmond.
1997.
Crystal structure of the nucleosome core particle at 2.8Å resolution.
Nature
389:251-260[Medline].
|
| 53.
|
Maupin-Furlow, J. A., and J. G. Ferry.
1995.
A proteasome from the methanogenic Archaeon Methanosarcina thermophila.
J. Biol. Chem.
270:28617-28622[Abstract/Free Full Text].
|
| 54.
|
Mayr, E.
1998.
Two empires or three?
Proc. Natl. Acad. Sci. USA
95:9720-9723[Free Full Text].
|
| 55.
|
Morris, C. J., and J. N. Reeve.
1985.
Functional expression of methanogen genes in Escherichia coli and Bacillus subtilis, p. 175-186.
In
Proceedings of the First International Symposium on Biotechnological Advances in Processing Municipal Wastes for Fuels and Chemicals. Argonne National Laboratory Press, Argonne, Ill.
|
| 56.
|
Nishihara, M.,
T. Kyuragi,
N. Sone, and Y. Koga.
1998.
sn-Glycerol-1-phosphate dehydrogenase: a key enzyme in the biosynthesis of ether phospholipids in Archaea, p. 281-285.
In
J. Wiegel, and M. W. W. Adams (ed.), Thermophiles. The keys to molecular evolution and the origin of life. Taylor and Francis Ltd., London, United Kingdom.
|
| 57.
|
Pace, N. R.
1997.
A molecular view of microbial diversity and the biosphere.
Science
276:743-740.
|
| 58.
|
Pereira, S.,
R. A. Grayling,
R. Lurz, and J. N. Reeve.
1997.
Archaeal nucleosomes.
Proc. Natl. Acad. Sci. USA
94:12633-12637[Abstract/Free Full Text].
|
| 59.
|
Pereira, S. L., and J. N. Reeve.
1998.
Histones and nucleosomes in Archaea and Eukarya: a comparative analysis.
Extremophiles
2:141-148.
[Medline] |
| 60.
|
Potter, S.,
P. Durovic, and P. P. Dennis.
1995.
Ribosomal RNA precursor processing by a eukaryotic U3 small nucleolar RNA-like molecule in an archaeon.
Science
268:1056-1060[Abstract/Free Full Text].
|
| 61.
|
Qureshi, S. A.,
S. D. Bell, and S. P. Jackson.
1997.
Factor requirements for transcription in the archaeon Sulfolobus shibatae.
EMBO J.
16:2927-2936[Medline].
|
| 62.
|
Reeve, J. N.
1986.
The bacteria. A treatise on structure and function.
ASM News
52:172.
|
| 63.
|
Reeve, J. N.
1986.
Microbiology.
American Society for Microbiology, Washington, D.C.
|
| 64.
|
Reeve, J. N.,
J. Nölling,
R. M. Morgan, and D. R. Smith.
1997.
Methanogenesis: genes, genomes and who's on first.
J. Bacteriol.
179:5975-5986[Free Full Text].
|
| 65.
|
Reeve, J. N.,
K. Sandman, and C. J. Daniels.
1997.
Archaeal histones, nucleosomes, and transcription initiation.
Cell
89:999-1002[Medline].
|
| 66.
|
Rivera, M. C.,
R. Jain,
J. E. Moore, and J. A. Lake.
1998.
Genomic evidence for two functionally distinct gene classes.
Proc. Natl. Acad. Sci. USA
95:6239-6244[Abstract/Free Full Text].
|
| 67.
|
Sandman, K.,
J. A. Krzycki,
B. Dobrinski,
R. Lurz, and J. N. Reeve.
1990.
DNA binding protein HMf, isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones.
Proc. Natl. Acad. Sci. USA
87:5788-5791[Abstract/Free Full Text].
|
| 68.
|
Sandman, K.,
S. L. Pereira, and J. N. Reeve.
1998.
Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome.
Cell. Mol. Life Sci.
54:1350-1364[Medline].
|
| 69.
|
Schmid, M.
1990.
More than just "histone-like" proteins.
Cell
63:451-453[Medline].
|
| 70.
|
Smith, D. R.,
L. A. Doucette-Stamm,
C. DeLoughery,
H. Lee,
J. Dubois,
T. Aldredge,
R. Bashirzadeh,
D. Blakely,
R. Cook,
K. Gilbert,
D. Harrison,
L. Hoang,
P. Keagle,
W. Lumm,
B. Pothier,
D. Qiu,
R. Spadafora,
R. Vicaire,
Y. Wang,
J. Wierzbowski,
R. Gibson,
N. Jiwani,
A. Caruso,
D. Bush,
H. Safer,
D. Patwell,
S. Prabhakar,
S. McDougall,
G. Shimer,
A. Goyal,
S. Pietrokovski,
G. Church,
C. J. Daniels,
J. Mao,
P. Rice,
J. Nölling, and J. N. Reeve.
1997.
The complete genome sequence of Methanobacterium thermoautotrophicum strain  H: functional analysis and comparative genomics.
J. Bacteriol.
179:7135-7155[Abstract/Free Full Text].
|
| 71.
|
Soppa, J.
1999.
Transcription initiation in Archaea: facts, factors and future aspects.
Mol. Microbiol.
31:1295-1305[Medline].
|
| 72.
|
Starich, M. R.,
K. Sandman,
J. N. Reeve, and M. F. Summers.
1996.
NMR structure of HMfB from the hyperthermophile, Methanothermus fervidus, confirms that this archaeal protein is a histone.
J. Mol. Biol.
255:187-203[Medline].
|
| 73.
|
Thomm, M.
1996.
Archaeal transcription factors and their role in transcription initiation.
FEMS Microbiol. Lett.
18:159-171.
|
| 74.
|
Thompson, D. K., and C. J. Daniels.
1998.
Heat shock inducibility of an archaeal TATA-like promoter is controlled by adjacent sequence elements.
Mol. Microbiol.
27:541-551[Medline].
|
| 75.
|
Trent, J. D.
1996.
A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea.
FEMS Microbiol. Lett.
18:249-258.
|
| 76.
|
Trotta, C. R.,
F. Miao,
E. A. Arn,
S. W. Stevens,
C. K. Ho,
R. Rauhut, and J. N. Abelson.
1997.
Cloning and analysis of the subunits of the Saccharomyces cerevisiae tRNA splicing endonuclease: identification of a family of tRNA endonucleases in eukaryotes and Archaea.
Cell
89:849-858[Medline].
|
| 77.
|
Watson, G. M. F.,
J.-P. Yu, and F. R. Tabita.
1999.
Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic Archaea.
J. Bacteriol.
181:1569-1575[Abstract/Free Full Text].
|
| 78.
|
Wiegel, J., and M. W. W. Adams.
1998.
Thermophiles:the keys to molecular evolution and the origin of life?
Taylor and Francis Ltd., London, United Kingdom.
|
| 79.
|
Wilting, R.,
S. Schorling,
B. C. Persson, and A. Böck.
1997.
Selenoprotein synthesis in Archaea: identification of an mRNA element of Methanococcus jannaschii probably directing selenocysteine insertion.
J. Mol. Biol.
266:637-641[Medline].
|
| 80.
|
Woese, C.
1998.
The universal ancestor.
Proc. Natl. Acad. Sci. USA
95:6854-6859[Abstract/Free Full Text].
|
| 81.
|
Woese, C. R., and G. E. Fox.
1977.
Phylogenetic structure of the prokaryotic domain: the primary kingdoms.
Proc. Natl. Acad. Sci. USA
74:5088-5090[Abstract/Free Full Text].
|
| 82.
|
Woese, C. R.,
O. Kandler, and M. L. Wheelis.
1990.
Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
Proc. Natl. Acad. Sci. USA
87:4576-4579[Abstract/Free Full Text].
|
| 83.
|
Woese, C. R., and R. S. Wolfe.
1985.
The bacteria, vol. 8. Archaebacteria.
Academic Press, Orlando, Fla.
|
| 84.
|
Wood, A. G.,
H. Redborg,
D. R. Cue,
W. B. Whitman, and J. Konisky.
1983.
Complementation of argG and hisA mutations of Escherichia coli by DNA cloned from the archaebacterium Methanococcus voltae.
J. Bacteriol.
156:19-29[Abstract/Free Full Text].
|
| 85.
|
Zwickl, P.,
A. Grziwa,
G. Pühler,
B. Dahlmann,
F. Lottspeich, and W. Baumeister.
1992.
Primary structure of the Thermoplasma proteasome and its implications for the structure, function, and evolution of the multicatalytic proteinase.
Biochemistry
31:964-972[Medline].
|
Journal of Bacteriology, June 1999, p. 3613-3617, Vol. 181, No. 12
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Eckburg, P. B., Lepp, P. W., Relman, D. A.
(2003). Archaea and Their Potential Role in Human Disease. Infect. Immun.
71: 591-596
[Full Text]
-
Hanzelka, B. L., Darcy, T. J., Reeve, J. N.
(2001). TFE, an Archaeal Transcription Factor in Methanobacterium thermoautotrophicum Related to Eucaryal Transcription Factor TFIIE{alpha}. J. Bacteriol.
183: 1813-1818
[Abstract]
[Full Text]
-
Stathopoulos, C., Li, T., Longman, R., Vothknecht, U. C., Becker, H. D., Ibba, M., Söll, D.
(2000). One Polypeptide with Two Aminoacyl-tRNA Synthetase Activities. Science
287: 479-482
[Abstract]
[Full Text]
Top
Text
References
