Ancient Microbes, Extreme Environments, and the Origin of Life

375 Pages·2001·48.78 MB·English

by  Paul Blum (Eds.)

PREFACE
Biologists divide living organisms into prokaryotes, represented by
the bacteria, and eukaryotes such as ourselves. In this scheme, bacteria
are considered to be the most primitive form of life. One popular idea
about how life arose supposes that humans evolved from bacteria. In this
age of genomics, however, DNA sequence comparisons indicate that our
genes are unlike those of bacteria. Where, then, did we come from? An
answer to that question comes from a truly unexpected source, life in
extreme environments.
It was generally thought that boiling acid hot springs or saturating
saline lakes were sterile, however, life is both present and highly suc-
cessful. Many of the resident organisms are still microbes, just not bac-
teria. We call them archaea. Whole-genome DNA sequences of five ar-
chaeal species reveal remarkable gene matches to human genes and
those of other eukaryotes. These matches occur in the most essential
of the subcellular processes carried out by all organisms, the synthe-
sis and repair of DNA, RNA, and protein. This suggests that eukaryotes
evolved from archaea or perhaps that archaea and eukaryotes derive
from a common ancestor.
Gene sequences aside, archaea lay additional claim to the title of an-
cient organism based on geologic and taxonomic considerations. The
early Earth (Archean age) was a time of elevated surface temperatures.
Fossil dating indicates the presence of microbes at the close of this pe-
riod, suggesting that earlier forms of life from which these fossils would
have derived must have been adapted to temperature extremes. Mi-
crobes called hyperthermophiles with just these abilities are still found
on the Earth in geothermal springs and hydrothermal ocean vents. These
extreme locations exhibit geochemistries most like that of early Earth.
To understand how such organisms relate to other forms of life, taxo-
nomic methods based on ribosomal RNA sequences have been used to
create phylogenetic “trees” of life. These hyperthermophilic microbes,
dominated by the archaea, exhibit the deepest phylogenetic branches,
suggesting that they have undergone the longest period of evolution
among extant organisms. Taken together, these ideas suggest that hyper-
thermophilic archaea may represent a form of the earliest type of life.
The intent of this book is to expand the general understanding of the
archaea. As simple organisms with sequenced genomes, they present
unique opportunities to understand better our own origins and, indeed,
ix
X PREFACE
the origin of life. As prokaryotes they provide powerful experimental
systems for genetic and molecular experimentation.
Acknowledgments
I am most grateful for the support and interest of many colleagues, in-
cluding Rolf Bernander, Mike Dyall-Smith, Peter Kennelly, John Leigh,
William Metcalf, Kenneth Noll, Frank Robb, Richard Shand, Dieter
Soll, and William Whitman. The pioneering interests of Thomas Brock,
Richard Morita, Norman Pace, Carl Stetter, Carl Wose, and Wolfram
Zillig helped create my interest in extreme environments and the evo-
lutionary implications of life native to such habitats.
INTRODUCTION
Ribosomal RNA gene sequence comparisons separate life into three
distantly related groups or domains (Fig. 1). Eukaryotes constitute one
domain, encompassing single- and multicelled organisms such as plants
and animals. Despite their morphologic simplicity and apparent simi-
larity, the other two domains are both prokaryotic. These domains are
represented by the bacteria and the archaea. Differences in rRNA se-
quence are but one feature leading to this classification system. Most
scientists are well versed about the evidence which distinguishes bac-
terial from eukaryotic life. This includes a diversity of mechanisms
governing all aspects of basic cell biology, from gene organization to
gene expression, from signal transduction to metabolism. What, then,
beyond differences in rRNA sequence supports the separate classifi-
cation of the archaea from bacterial prokaryotes and eukaryotes? As
predicted by their rRNA sequence divergence and by analogy to the
dissimilarity between bacteria and eukaryotes, archaea are likely to em-
ploy archaeal-specific subcellular mechanisms for conducting essential
processes. While the existence of archaeal-specific subcellular mech-
anisms is supported by the occurrence of a unique group of archaeal
orthologous genes, the functions of these genes remain unknown. The
truly remarkable discovery which is the focus of this book concerns the
finding that archaea use eukaryotic-like mechanisms and not bacterial
mechanisms for much of their information processing functions.
The literature on bacterial prokaryotes is both extensive and diverse,
however, such is not yet the case for archaea. As a recognized group,
archaea are relative newcomers to the prokaryotic world. Despite their
recent entry into the research arena, studies on archaea are blossom-
ing, largely in response to the availability of whole-genome DNA se-
quences. Three distinctive biotypes of archaea are best known: the
methanogens, the halophiles, and the hyperthermophiles. Due to the
radical nature of their respective niches, these organisms have been
dubbed extremophiles. Studies on life in extreme environments portend
many exciting areas in biology research including studies on the origins
of life and the possibility of extraplanetary organisms. Archaea have
contributed, and will continue to contribute, greatly to these areas. How-
ever, phylogenetic studies of marine, dirt, and other environmental sam-
ples indicate that some archaea are not extremophilic but mesophilic
members of microbial communities. More importantly, these types of
xi
xii INTRODUCTION
‘Plants
FIG. 1. Archaeal, bacterial, and eukaryotic sequences were aligned with ClustalW. The
programs DNADIST, NEIGHBOR, CONSENSE, and FITCH, of the Phylip package, were
used to build the tree. The alignment was bootstrapped 100 times with SEQBOOT.
archaea appear to constitute a significant proportion of the total plane-
tary microbial biomass.
This book provides an overview of key aspects of the archaea includ-
ing chapters on their genomics and phylogeny, micropaleontology, cell
biology, and molecular genetics. This information should be useful to
microbiology students at both the graduate and the undergraduate lev-
els. More importantly, this text should focus the attention of researchers
on the importance of archaea as model systems to address fundamental
biological questions. As prokaryotes, archaea can and should be used
to wield the power of haploid genetics providing cost-efficient systems
for scientific investigations into life.
Paleobiology of the Archean
SHERRY L. CADY
Department of Geology
Portland State University
PO. Box 751
Portland, Oregon 97207-0751
I. Introduction
II. Historical Review
A. Main Phases of Archean Paleobiological Studies
B. Reviews of Archean Paleobiology
III. Evidence for Life-Microbial Biosignatures
A. Bona Fide Microfossils
B. Microbialities and Biogenic Stromatolites
C. Chemofossils-Biomarkers and Isotopes
IV. Criteria for Assessing Biogenicity
V. Biogeochemical Interactions and Biosignature Formation
VI. Extreme Ecosystems
VII. Geological and Paleobiological History of the Archean (4000-2500 Ma)
A. Oldest Dated Terrestrial Rocks and Minerals
B. Oldest Types of Crustal Terrane
C. Chemofossils, West Greenland
D. Oldest Microfossils
E. Microfossils in Hydrothermal Deposits
F. Oldest Stromatolites
G. Oldest Isotopic Evidence of a Specific Metabolic Pathway
in Archean Evaporite Deposits
H. Evidence of Hydrothermal Oil Generation during the Archean
I. Oldest Compelling Chemofossil Evidence of Methanogenic Archaea
J. Oxygenic Phototrophy
VIII. Conclusion
References
I. Introduction
Four billion years ago our planet began accumulating a rock record, a
geological event that heralded the beginning of the Archean Eon (Fig. 1).
Though the Earth itself is approximately 4550 million years old, the
oldest known rocks are the 4030 million-year-old Acasta gneisses of
northwestern Canada (Bowring and Williams, 1999). These rocks, and
others of comparable age, indicate that the ancient Earth harbored a
number of environments that could have supported life. The presence
of even older minerals, 4400 million-year-old detrital zircons from the
Yilgarn Craton, Western Australia (Wilde et al., ZOOl), provides evidence
3
ADVANCES IN APPLIED MICROBIOLOGY, VOLUME 50
Copyright 0 2001 by Academic Press
All rights of reproduction in any form reserved.
0065.2164/01535.00
4 SHERRY L. CADY
LOGIC TIME SC
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FIG. 1. Geological time scale. Geologic time is represented here by numerically desig-
nated bins of geologic time, each 100 million years long. The intervals, called geons (from
GEOlogical EON), are counted from the present. The geon scale allows for Earth history
(and that of other planets) to be viewed in a succession of large, simply named, equal time
units, in the same way that centuries and millennia are used for familiar smaller intervals.
PALEOBIOLOGY OF THE ARCHEAN 5
that the Earth was tectonically active shortly after it formed. Without
plate tectonic activity commencing early and persisting throughout our
planet’s history, it is unlikely that life would exist today. It is yet a
mystery when life began; its origin is not revealed in the paleobiological
record. Chemical fossil evidence in rocks from West Greenland indicate,
however, that microbial life had evolved by 3700 Ma (mega-annum;
meaning million years) (Rosing, 1999). The possibility exists that life
emerged within a few hundred million years after crustal rocks began
accumulating and began to leave traces in the paleobiological record.
The Archean Eon, by definition, ends at precisely 2500 Ma.
Fossil evidence indicates that once life emerged it evolved rapidly
and occupied new ecological niches as soon as they became available
(e.g., hydrothermal systems, shallow coastlines, continental seas). The
Archean paleobiological record is preserved in geological units that
consist primarily of chemical precipitates and volcanogenic sediments.
Such deposits accumulated on the edges of accreting continental cra-
tons and along the rims of protocontinents. Although only meager bits of
evidence have been discovered to date, new and significant discoveries
regarding Archean paleobiology and paleoecology continue to be made.
In general, paleobiological information comes from a potentially wide
range of fossil data known collectively as biosignatures. Evidence for the
existence of the Archean biosphere is preserved in the fossil remains
of microorganisms (i.e., microfossils), in the sedimentary structures mi-
croorganisms helped construct (i.e., stromatolites), and in the biomarker
compounds, isotopic signatures, and biominerals life leaves behind
(i.e., chemofossils). Bona fide microfossils, carbonaceous microorgan-
isms preserved in three dimensions, contain structural and chemical
rem- nants of cellular and extracellular components (e.g., cell walls,
sheathes, exopolysaccharides), which together can provide direct evi-
dence for life. Also, microbially influenced fabrics and structures that
form in ecosystems where authigenic minerals precipitate and rock de-
tritus accumulate provide indirect evidence of microscopic life forms.
Microbially influenced accretionary growth structures and fabrics in-
clude nonlaminated microbialites and laminated biogenic stromatolites.
Although both types of biogenic structures are found throughout the
Archean, they usually lack microfossils. Chemical fossils (“chemofos-
sils”), such as biomarkers and isotopic signatures, also provide indirect
The geon scale complements the traditional, history-based scale with complex names and
unequal geologic periods, much like dynasties in history overlap centuries. The Archean
Eon is defined as that interval of time that began with the formation of the oldest geological
record and that ends at 2500 Ma (mega annum; meaning million years), which is the
beginning of the Proterozoic Eon. [Reproduced with permission from Hofmann (1990,
1992, 2000).]
6 SHERRYL.CADY
evidence for life. Biomarker compounds consist of organic molecules
highly diagnostic for their parent organisms. Elements that can be iso-
topically fractionated by biological or biochemical processes include
carbon, sulfur, and nitrogen.
Not only have a number of types of fossil biosignatures shown that
life emerged and spread globally during the early Archean, but evidence
for life has been reported from all of the major Archean cratons. The pa-
leobiological record has shown that life occupied several niches during
the Archean and, within a few hundred million years, diversified and
became metabolically sophisticated. Although fossil evidence cannot
provide precise data as to when a metabolic innovation evolved, it can
reveal that a particular metabolic capability existed. Chemofossil evi-
dence demonstrates that many major metabolic pathways evolved dur-
ing the Archean. Though the data for these evolutionary innovations
are scattered throughout the ancient rock record, the continuous and
relatively robust paleontological record of the Proterozoic Eon (2500 to
543 Ma) has confirmed that prior to the end of the Archean, analogues
of modern microbial ecosystems, including those considered extreme,
were established.
Several lines of evidence suggest that the earliest microbial inhabi-
tants occupied sediments and colonized newly formed minerals that
precipitated around hydrothermal vents, environments characterized
by high temperatures and an abundance of dissolved metal ions
(Nisbet, 1995). As shown in Fig. 2 molecular phylogenetic analysis
of the small-subunit ribosomal RNA of extant life indicates that hy-
perthermophiles in the bacterial and archaeal domains are the closest
living relatives of the hypothetical last common ancestor (Pace, 1997).
Whether life originated at high temperatures (Shock and Schulte, 1998)
is not known, and evidence for a hyperthermophilic ancestry has been
challenged (Doolittle, 2000; Galtier et al., 1999). The possibility exists
that hyperthermophiles emerged during that brief but finite period of
time after the collision that presumably formed the Earth-Moon sys-
tem; after the collision (-4450 to 4500 Ma), when the Earth began to
cool, surface temperatures could have hovered around 100°C for 100
to 200 million years (Sleep et al., 2001). The catastrophic conditions
created by large impactor events during the latter part of the heavy
bombardment period (-3900 to 3800 Ma) would also have created
and sustained high-temperature habitats that could have supported hy-
perthermophilic communities; large impactors ( >GIOOk m in diameter)
could have vaporized the ocean, while smaller impactors (>200 km in
diameter) might have been able to heat the ocean above 100°C (Sleep
and Zahnle, 1998). Alternatively, if life originated at lower temper-
atures, and then radiated and adapted to high-temperature environ-
ments, hyperthermophiles living in the subsurface portions of deep-sea
PALEOBIOLOGY OF THE ARCHEAN
3ACTERIA 3 f
FIG. 2. Universal phylogenetic tree based on SSU rRNA sequences. The largest formal
unit of the tree consists of domains that include the Archaea, Bacteria, and Eukarya. The
tree can be considered a rough map of the evolutionary distance between the organisms
shown. Although the nature of the hypothetical last common ancestor is not known,
hyperthermophilic and thermophilic microbial lineages are clustered around the root of
the microbial domains. Constructed by comparison of 16s small-subunit ribosomal RNA
sequences, the tree includes 64 rRNA sequences representative of all known phylogenetic
domains. [Reproduced with permission from Pace (lggi’).]
hydrothermal systems may have been the only microbial communities
that could have survived the impact-induced ocean sterilizing events
(Maher and Stevenson, 1988).
The Earth has always been a volcanically active planet, and hydrother-
mal activity prevailed after liquid water became stable at the Earth’s