Biodata of Derek R. Lovley author of “Potential Role of Dissimilatory Iron Reduction
in The Early Evolution of Microbial Respiration”
Dr. Derek R. Lovley is a Professor at the Department of Microbiology, University of
Massachusetts-Amherst, Amherst MA. He was honored as a Distinguished University
Professor at his Department. Dr. Lovley obtained his Ph.D. (1982) at the Michigan State
University in Microbiology. Among his awards are: the Division K Lecturer for the
American Society for Microbiology, Fellow, American Academy of Microbiology,
Grant Winner, Popular Science, U.S. Geological Survey Mendenhall Lecturer (highest
scientific honor of USGS).
E-mail: [email protected]
299
J. Seckbach (ed.), Origins, 299–313.
© 2004 Kluwer Academic Publishers. Printed in the Netherlands.
POTENTIAL ROLE OF DISSIMILATORY IRON REDUCTION IN THE
EARLY EVOLUTION OF MICROBIAL RESPIRATION
DEREK R. LOVLEY
Department of Microbiology, University of Massachusetts-Amherst,
Amherst MA 01003 USA
1. Introduction
In the absence of time travel, it may be impossible to ever definitively determine the
mechanisms by which early life evolved on Earth. Proposals for early forms of
microbial respiration should be consistent with mechanisms of energy conservation that
would be possible under geochemical conditions likely to have been present at the time
that life emerged. Furthermore, it might be expected that this early form of respiration
would be highly conserved in those microorganisms most closely related to the last
common ancestor(s) of modern life. As detailed below, of all the known forms of
microbial respiration, electron transfer to Fe(III) best fits these geological and
microbiological criteria.
Until recently, speculation about the earliest forms of microbial respiration has
focused on virtually every known form of microbial respiration other than Fe(III)
reduction. One reason for Fe(III) being ignored in the past is that Fe(III) reduction has
only recently been recognized as a form of energy conservation (Lovley 1991).
Although it has been known for many years that Fe(III) could be reduced during
anaerobic growth of some microorganisms, these Fe(III)-reducing microorganisms had
a primarily fermentative metabolism and only reduced Fe(III) as a side reaction in their
metabolism (Lovley 1987). There was no evidence that this Fe(III) reduction yielded
energy to support cell growth and it was often considered that Fe(III) was reduced by
non-enzymatic reactions in the cultures. The ability of microorganisms to conserve
energy to support growth with Fe(III) serving as the electron acceptor was first reported
in the 1980s (Balashova and Zavarzin 1980; Lovley et al. 1987). Unlike other more
well-studied forms of anaerobic respiration, the biochemical mechanisms for
dissimilatory Fe(III) reduction are still largely unknown.
Microbial Fe(III) reduction is generally considered to be an environmentally
significant process on modern Earth. Fe(III) is typically the most abundant potential
electron acceptor for organic matter oxidation in most soils and sediments (Lovley
1991, 2000). Therefore, with the development of anoxic conditions, microbial Fe(III)
reduction can become important in organic matter oxidation in environments such as
flooded soils, aquatic sediments, or subsurface environments (Lovley 1991, 2000). In
addition to contributing to the degradation of naturally occurring organic matter,
microbial Fe(III) reduction can play an important role in the removal of organic
contaminants from subsurface environments (Lovley 1995; Anderson and Lovley
301
302
1997). This is apparent, for example, in petroleum-contaminated aquifers in which
Fe(III)-reducing microorganisms effectively remove aromatic hydrocarbons from
groundwater (Lovley et al. 1989; Lovley and Lonergan 1990; Lovley et al. 1994;
Anderson et al. 1998; Rooney-Varga et al. 1999; Snoeyenbos-West et al. 2000). Some
Fe(III)-reducing microorganisms, such as Geobacter species, can substitute toxic
metals, such as U(VI), for Fe(III) in their respiration and in the process aid in the
bioremediation of metal-contaminated groundwaters (Lovley et al. 1991; Finneran et al.
2002; Holmes et al. 2002). Another practical use of Fe(III)-reducing microorganisms is
their ability to transfer electrons onto electrodes, making it possible to harvest
electricity from anoxic aquatic sediments and other sources of waste organic matter
(Bond et al. 2002; Bond and Lovley 2003).
Speculation about the potential role of Fe(III)-reducing microorganisms on early
Earth began with the discovery that microbial reduction of Fe(III) oxides could produce
copious quantities of the magnetic mineral magnetite (Lovley et al. 1987; Lovley 1990).
This provided a potential explanation for the magnetite accumulations in Precambrian
Banded Iron Formations, which geological evidence suggested was formed as the result
of the oxidation of organic matter to carbon dioxide, coupled to the reduction of Fe(III)
oxide to magnetite (Baur et al. 1985; Walker 1987). The discovery of magnetite,
presumably the result of microbial activity, deep in the Earth’s surface led to the
proposal of a deep, hot biosphere below the surface of Earth, and possibly other planets
(Gold 1992). Magnetite with a morphology similar to that produced by Fe(III)-reducing
microorganisms in a Martian meteorite was suggested to provide evidence for previous
life on Mars (McKay et al. 1996). These discoveries led to the further investigation of
whether Fe(III) reduction might be an important process in extreme environments, such
as those found on early Earth.
2. Hyperthermophilic Fe(III)-Reducing Microorganisms
2.1. Fe(III) REDUCTION IS A HIGHLY CONSERVED CHARACTERISTIC OF
HYPERTHERMOPHILES
It is often speculated that life emerged on a hot, early Earth (Baross and Hoffman 1985;
Pace 1991; Holm 1992; Bock and Goode 1996). A common justification for this is that,
based on 16S rDNA sequences, all of the extant microorganisms that are most closely
related to the last common ancestor(s) of modern life are hyperthermophilic Archaea
and Bacteria. An alternative explanation is that hyperthermophiles were the only life
forms that survived some catastrophic, high temperature event that took place well after
life had evolved. However, if it is accepted that the physiological characteristics of the
most deeply branching extant organisms represent those found in the last common
ancestor(s), then current microbiological evidence suggests that the earliest
microorganisms were hyperthermophiles.
Using this same logic, speculations can also be made about the forms of respiration
found in the last common ancestor(s). All of the commonly considered types of
microbial respiration including oxygen reduction, nitrate reduction, sulfate reduction,
and methanogenesis are found in representative deeply branching hyperthermophilic
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microorganisms (Stetter 1996) and thus each has been regarded as a potential early form
of respiration by one or more investigators. Until 1998 (Vargas et al. 1998), it was not
recognized that hyperthermophiles could use Fe(III) as an electron acceptor as previous
investigations into the potential for hyperthermophiles to reduce Fe(III) had yielded
negative results (Stetter 1996).
However, when a diversity of hypethermophiles that had been isolated on electron
acceptors other than Fe(III) were tested for their ability to reduce Fe(III) with hydrogen
as an electron donor, all of the organisms were capable of Fe(III) reduction (Vargas et
al. 1998). Many of these organisms could also reduce extracellular quinones, such as
humic acids (Lovley et al. 2000), which is a common feature of mesophilic Fe(III)
reducers (Lovley et al. 1996; Lovley et al. 1998).
Furthermore, those
hyperthermophiles that were investigated in more detail for their ability to grow with
Fe(III) serving as the sole electron acceptor, conserved energy to support growth from
Fe(III) reduction. Most remarkable in this regard was the hyperthermophilic bacterium
Thermotoga maritima. This organism was previously regarded to have a fermentative
metabolism and even though it could transfer electrons to S°, S° reduction did not
appear to be an energy-conserving form of respiration in T. maritima. In contrast, with
Fe(III) as the electron acceptor, T. maritima grew with hydrogen as the sole electron
donor and Fe(III) as the electron acceptor (Vargas et al. 1998). Hyperthermophiles such
as Archaeoglobus fulgidus that do not reduce S° do reduce Fe(III) (Vargas et al. 1998),
and as detailed below, providing Fe(III) as an electron acceptor also expands the
metabolic capabilities of some other hyperthermophilic Archaea. These results suggest
that Fe(III) reduction is more closely associated with central metabolism in some
hyperthermophiles than reduction of S° or other electron acceptors.
Every
hyperthermophile that has been tested to date can reduce Fe(III), representing a wide
phylogenetic diversity within the hyperthermophiles (Fig. 1). Thus, other than the
ability to grow at high temperature, the capacity for Fe(III) reduction may be amongst
the most highly conserved metabolic characteristics of hyperthermophiles.
2.2. NOVEL FORMS OF HYPERTHERMOPHILIC METABOLISM LINKED TO
Fe(III) REDUCTION
Another example in which provision of Fe(III) as an electron acceptor was found to
increase the metabolic capability of a hyperthermophile is the expanded range of carbon
metabolism in Ferroglobus placidus in the presence of Fe(III). In the initial
characterization of F. placidus it was concluded that it did not use organic electron
donors to support growth with its known electron acceptors, nitrate and thiosulfate
(Hafenbradl et al. 1996). However, when Fe(III) oxide was provided as an electron
acceptor F. placidus could grow with acetate as the electron donor and Fe(III) as the
electron acceptor (Tor et al. 2001). Acetate was oxidized to carbon dioxide with the
following stoichiometry:
acetate-+ 8 Fe(III) + 4 H2O _____> 2 HCO3- + 8 Fe(II) + 9 H+ (1)
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Geothermobacterium ferrireducens
100
Thermotoga maritima
Strain 121
100
Pyrodictium abyssi
94
Methanopyrus kandleri
100
Pyrobaculum aerophilum
100
Pyrobaculum islandicum
Geoglobus ahangari
100
86
100
65
100
Archaeoglobus fulgidus
Ferroglobus placidus
Pyrococcus furiosus
Methanothermococcus thermolithotrophicus
0.05 nucleotide substitutions/site
Figure 1. Phylogenetic tree constructed by maximum likelihood analysis showing the phylogenetic
relationship of known Fe(III)-reducing hyperthermophiles. Bootstrap analysis was performed with 100
replicates. Thermotoga maritima served as an outgroup.
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A novel isolate from the Guaymas Basin in the Gulf of California, Geoglobus
ahangari, oxidized acetate in a similar manner (Tor et al. 2001; Kashefi et al. 2002b).
These represent the only documented cases of anaerobic acetate oxidation in
hyperthermophilic microorganisms. Although there have been instances in which it has
been suggested that hyperthermophiles might anaerobically oxidize acetate with sulfate
or sulfite as the electron acceptor (Volkl et al. 1993; Huber et al. 1997), quantitative
data on acetate oxidation were not presented and subsequent attempts to grow these
other organisms on acetate have been unsuccessful (Afshar et al. 1998; Tor et al. 2001).
In fact, prior to the report of hyperthermophiles that could oxidize acetate with the
reduction of Fe(III), it was considered that acetate produced in hot (i.e. > 80°C)
microbial ecosystems would need to diffuse into cooler environments before
microorganisms could metabolize it (Slobodkin et al. 1999b). Acetate is expected to be
a key intermediate in the anaerobic degradation of organic matter in hot, microbial
ecosystems (Tor et al. 2003), just as it is in cooler environments (Lovley and Chapelle
1995). The finding that there are hyperthermophiles that can oxidize acetate with
Fe(III) suggests that acetate produced within hot microbial ecosystems can serve as an
important energy source within these ecosystems, rather than being exported as an
energy source for surrounding cooler environments. It seems likely that as the diversity
of hyperthermophiles is further explored, hyperthermophiles capable of anaerobically
oxidizing acetate with electron acceptors other than Fe(III) will also be found.
Further investigation of the metabolism of F. placidus and G. ahangari
demonstrated that the capacity of these hyperthermophiles to oxidize organic
compounds not previously known to be microbially degraded in hot microbial
ecosystems extended beyond acetate. For example, F. placidus grew with a variety of
aromatic compounds as the electron donor and Fe(III) oxide as the sole electron
acceptor (Tor and Lovley 2001). To date, F. placidus is still the only hyperthermophile
known to have this capability. The stoichiometry of benzoate and phenol uptake and
Fe(III) reduction demonstrated that F. placidus completely oxidized these aromatic
compounds to carbon dioxide with Fe(III) serving as the sole electron acceptor. Other
aromatic compounds supporting growth included 4-hydroxybenzoate, benzaldehyde, phydroxybenzaldehyde, and t-cinnamic acid (3-phenyl-2-propenoic acid). F. placidus
only oxidized aromatic compounds with Fe(III). Nitrate, which serves as an electron
acceptor for growth on hydrogen or Fe(II), did not support growth on aromatic
compounds.
Long-chain fatty acids are a significant component of organic matter in many
environments. G. ahangari oxidized palmitate and stearate with Fe(III) as the electron
acceptor (Kashefi et al. 2002b). The stoichiometry of Fe(III) reduction suggested that
the long-chain fatty acids were completely oxidized to carbon dioxide. G. ahangari is
the only hyperthermophile known to oxidize long-chain fatty acids.
The ability of Fe(III) reducers such as F. placidus and G. ahangari to oxidize
organic acids and aromatic compounds, suggests for the first time that the complete
oxidation of complex organic matter back to carbon dioxide may be possible in hot
microbial ecosystems. Consortia of fermentative microorganisms and Fe(III) reducers
should be able to oxidize the major components of organic matter. Since Fe(III) is
likely to be available as an electron acceptor in many hot microbial ecosystems,
including the deep hot subsurface (Gold 1992), petroleum reservoirs (Greene et al.
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1997; Slobodkin et al. 1999a), terrestrial hot springs (Brock et al. 1976), and
hydrothermal marine sediments (Jannasch 1995; Karl 1995), this may be a fairly
common phenomenon. As discussed below, early Earth represents another environment
in which such metabolism may have been common.
2.3. CULTURING “UNCULTURABLE” HYPERTHERMOPHILES WITH FE(III)
Many of the microorganisms that live in hot microbial ecosystems and have been
detected via analysis of 16S rDNA sequences have yet to be cultured. Given the finding
that the capacity for Fe(III) reduction is so highly conserved among hyperthermophiles,
a likely strategy for recovering many of these “as-yet-uncultured” organisms is to use
Fe(III) as the electron acceptor for isolation. This was evident in a study of
microorganisms living in Calcite Springs in Yellowstone National Park. A novel
bacterium, Geothermobacterium ferrireducens, was isolated with a novel procedure in
which Fe(III) oxide was incorporated into solidified medium (Kashefi et al. 2002a).
The 16S rDNA sequence of G. ferrireducens was closely related to 16S rDNA
sequences that were abundant in Calcite Spring (Hugenholtz et al. 1998). The likely
physiology of these previously uncultured microorganisms was in doubt because of a
lack of close relatives in culture. G. ferrireducens grows exclusively with hydrogen as
the electron donor and Fe(III) oxide as the electron acceptor (Kashefi et al. 2002a).
Thus, one likely reason organisms in this phylogenetic clade had not been previously
cultured is that few studies have employed Fe(III) as an electron acceptor. In a similar
manner, G. ahangari, described above, only uses Fe(III) as an electron acceptor
(Kashefi et al. 2002b). Another Fe(III) reducer, strain 121, which was isolated from a
marine hydrothermal vent and has the highest upper temperature limit for growth of any
known organism (Kashefi and Lovley 2003) also exclusively uses Fe(III). These results
suggest that much of the vast diversity of hyperthermophilic microorganisms that have
not yet been cultured may be microorganisms that use Fe(III), but not other electron
acceptors such as sulfur forms, nitrate, oxygen, or carbon dioxide that have been used in
the vast majority of previous isolation attempts.
2.4. GEOLOGICAL SIGNATURES FROM MICROBIAL METAL REDUCTION
Hyperthermophiles can reduce poorly crystalline Fe(III) oxide to ultra-fine grained
crystals of the magnetic mineral magnetite (Kashefi and Lovley 2000). This is similar
to the production of magnetite during microbial Fe(III) reduction at cooler temperatures
(Lovley et al. 1987; Lovley 1990). Although accumulations of ultra-fine grained
magnetite have been considered evidence for the activity of Fe(III)-reducing
microorganisms in extreme environments (Gold 1992; McKay et al. 1996), at the
present time there is no reliable way to distinguish the ultra-fine grained magnetite
produced as the result of microbial Fe(III) reduction from magnetite produced by
abiotic oxidation of Fe(II). The possibility that Fe(III) reducers might isotopically
fractionate iron during Fe(III) reduction (Beard et al. 1999) might ultimately provide a
method for distinguishing between these different mechanisms of magnetite formation.
If so, then magnetite in ancient rocks might serve as a geological signature of the
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activity of hyperthermophiles on early Earth. However, strategies for accounting for
abiological mechanisms for fractionation (Anbar et al. 2000) must first be developed.
In addition to Fe(III), hyperthermophiles can reduce a variety of other metals. The
ability of a diversity of hyperthermophiles to reductively precipitate gold via reduction
of soluble Au(III) to Au(0) might be responsible for the formation of some gold
deposits (Kashefi et al. 2001). The reduction of alternative metals in hypethermophiles
has been studied most intensively in Pyrobaculum islandicum which, in addition to
Fe(III), can reduce U(VI), Tc(VII), Cr(VI), Co(III), Mn(IV), and Au(III) with hydrogen
as the electron donor. The reduced products of some of these metals, most notably
uranium, might provide a geological signature for the activity of hyperthermophilic
Fe(III) reducers. For example, the precipitation of uranium as the result of the reduction
of soluble U(VI) to insoluble U(IV) at temperatures of ca. 100°C is considered to have
led to the formation of typical sandstone-type uranium deposits (Hostetler and Garrels
1962). Given that the lignite organic matter often associated with U(IV) deposits does
not abiotically reduce U(VI) at temperatures below 120°C (Nakashima et al. 1984), the
accumulation of the U(IV) minerals in environments that are considered to have been at
80-120° C at the time of U(VI) reduction could reasonably be assumed to be a
geological signature of hyperthermophilic microorganisms. For example, it is tempting
to speculate that the large U(IV) accumulations that formed the naturally generated
Oklo nuclear reactor in the Precambrian period (Brookins 1990) was the result of the
activity of hyperthermophiles reducing U(VI).
3. Hydrogen Oxidation Coupled to Fe(III) Reduction as the First Form as
Microbial Respiration
Prebiotic Earth has been described as a “giant photoelectrochemical cell” (Russell and
Hall 2002). Numerous studies (see Cairns-Smith et al. 1992; Russell and Hall 2002
for reviews) have suggested that high levels of ultraviolet radiation impinging upon the
Archaean sea, which contained high levels of dissolved Fe(II), resulted in the formation
of Fe(III) and hydrogen gas as follows:
hv
2 Fe(II) + 2 H+ ______> 2 Fe(III) + H2 (2)
The H2 formed in this manner was probably primarily lost to the atmosphere, whereas
the Fe(III) would have precipitated as insoluble Fe(III) oxides, forming a “positive
electrode” (Russell and Hall 2002). Geologically produced hydrogen emanating from
the subsurface represented a “negative electrode”. Other potential electron acceptors
for hydrogen oxidation, such as oxygen, nitrate, or sulfate were probably not abundant
(Cameron 1982; Walker and Brimblecombe 1985; Eastoe et al. 1990). If this geological
scenario is correct, then conditions were highly favorable for the development of a
biological entity that could take advantage of the energy available from hydrogen
oxidation coupled to Fe(III) reduction.
In fact, it has been proposed that the development of the first membrane system
capable of electron transport and energy conservation through a chemiosmotic
308
mechanism started by catalyzing the oxidation of hydrogen with the reduction of Fe(III)
(Russell et al. 1998; Russell and Hall 2002). Initially, such membranes were probably
inorganic, possibly comprised of iron sulfide minerals, but eventually evolved into lipid
membranes as life became more similar to known forms of extant life (Russell et al.
1998; Russell and Hall 2002). If so, then it seems likely that this earliest of organic life
forms would also have been a hydrogen-oxidizing Fe(III)-reducing entity. This
concept, originated by geologists, and based upon the best current information on the
geochemical conditions on early Earth, matches well with the extrapolation from the
physiology of hyperthermophilic Bacteria and Archaea that the last common
ancestor(s) were hydrogen-oxidizing Fe(III) reducers. Although the last common
ancestor(s) was likely to have been a metabolically sophisticated respiratory organism
(Pace 1991; de Duve 1995; Woese 1998), it is probable that the more primitive
microorganisms that preceded the last common ancestor would also have had the
capacity to transfer electrons to extracellular Fe(III).
The next major advance in the development of microbial communities based on
Fe(III) reduction is likely to have coincided with the evolution of photosynthesis. The
earliest photosynthesis may have relied on Fe(II) as an electron donor (Hartman 1984;
Widdel et al. 1993; Ehrenreich and Widdel 1994) or could have been oxygenic
photosynthesis. The emergence of photosynthesis would have greatly increased the
availability of organic matter while also generating large quantities of Fe(III), either
from the direct oxidation of Fe(II) in photosynthesis or from oxygen abiotically
oxidizing Fe(II). Thus, it is expected that as photosynthesis became important
hydrogen-based Fe(III)-reducing communities were increasingly supplanted by Fe(III)reducing microorganisms fueled primarily by organic matter oxidation. Such
heterotrophic Fe(III)-reducing communities appear to have been prevalent by the early
Precambrian period as evidenced by the accumulation of massive amounts of magnetite
in the Precambrian Banded Iron Formations that can be attributed to the activity of
Fe(III)-reducing microorganisms (Lovley 1991, 2000). The geological record indicates
that this oxidation of organic matter coupled to Fe(III) reduction was globally
significant before other mechanisms for anaerobic or aerobic oxidation of organic
matter to carbon dioxide (Walker 1987).
3.1. WHY Fe(III) REDUCTION RATHER THAN CARBON DIOXIDE REDUCTION
AS THE FIRST FORM OF RESPIRATION
Although many commonly considered electron acceptors such as oxygen, nitrate, and
sulfate are not likely to have been prevalent when life evolved, carbon dioxide was.
Thus, it is important to consider whether electron transfer to carbon dioxide, rather than
Fe(III) reduction, could have been the first form of microbial respiration. Modern
forms of energy conservation with hydrogen as the electron donor and carbon dioxide
as the electron acceptor are methane production and acetogenesis. Both of these
processes are biochemically complex in part due to the fact that there is little energy
available from these reactions as well as kinetic constraints on carbon dioxide
reduction. In contrast, Fe(III) is readily reduced by a wide variety of redox-active
molecules. For example, it is much more likely that the iron-sulfide membranes
proposed to have led to the evolution of life could have transferred electrons to Fe(III)
309
than onto carbon dioxide. Even highly evolved, extant methanogens may preferentially
transfer electrons to Fe(III) rather than produce methane (Bond and Lovley 2002).
When Fe(III) is available, methanogens can maintain hydrogen concentrations at levels
so low that methane production from hydrogen is not thermodynamically favorable
(Bond and Lovley 2002). Thus, it seems unlikely methanogenesis could have prevailed
over Fe(III) reduction in less highly regulated primitive life forms.
A less compelling, but notable argument against methanogenesis or acetogenesis
being one of the earliest forms of respiration is that none of the deeply branching
hyperthermophiles are acetogens and few have the capacity for methane production.
There are no methanogens among the Bacteria. In contrast, as discussed above, the
ability to oxidize hydrogen with the reduction of Fe(III) is highly conserved among
deeply branching hyperthermophilic Bacteria as well as Archaea.
3.2. EVIDENCE THAT HYDROGEN-BASED MICROBIAL ECOSYSTEMS CAN
EXIST
A microbial community fueled primarily by hydrogen and using Fe(III) as the sole
electron acceptor, as proposed for the earliest life, is unlikely to be found on modern
Earth because 1) most environments even in the subsurface contain organic matter
capable of supporting microbial growth and 2) environments devoid of organic matter
and containing hydrogen are now restricted to deep subsurface environments in which
there is no mechanism for generating significant quantities of Fe(III). However, the
concept that hydrogen could have served as the primary energy source for hydrogenbased microbial ecosystems on Early Earth has been supported by the discovery of a
hydrogen-based community in deeply buried igneous subsurface rock in Idaho
(Chapelle et al. 2002). Molecular analyses indicated that over 90% of the
microorganisms in this environment were hydrogen-oxidizing, methane-producing
microorganisms. Geochemical data demonstrated that hydrogen was present at levels
capable of supporting methanogenesis, but that significant quantities of organic matter
were not available. Although there have been other claims for hydrogen-based
microbial communities, subsequent geochemical and microbiological analyses have
suggested that organic matter was the primary energy source in those other
environments (Anderson et al. 1998). However, there is now at least one site in which a
hydrogen-based microbial exists.
4. Future Directions and Conclusions
There is so little geological and biological data available from early Earth that is
relevant to the evolution of the first forms of microbial respiration that the topic of
which form of respiration evolved first is certain to be debated for some time.
However, a strong case can be made for hydrogen oxidation coupled to Fe(III)
reduction being the first form of microbial respiration because: 1) it is likely that Fe(III)
was abundant at the time life evolved, whereas other commonly considered electron
acceptors such as oxygen, nitrate, or sulfate were not; 2) it is also likely that hydrogen
was present in sufficient quantities to serve as an electron donor for Fe(III) reduction; 3)
310
Fe(III) reduction can be catalyzed by simpler biochemical mechanisms than those
required for reduction of carbon dioxide, the only other abundant electron acceptor
available; and 4) the capacity for hydrogen oxidation coupled to Fe(III) reduction is a
much more highly conserved metabolic capability than the reduction of other known
electron acceptors among the hyperthermophilic Bacteria and Archaea that are most
closely related to the last common ancestor(s).
The finding that deeply branching hyperthermophiles have the capacity for Fe(III)
reduction leads to the question of whether the same mechanisms for Fe(III) reduction
are conserved in Fe(III)-reducing mesophilic microorganisms in the Bacteria, which are
considered to have evolved later. At present, there have only been preliminary
investigations into the mechanisms of Fe(III) reduction in hyperthermophiles (Childers
and Lovley 2001). Although there has been considerably more study of Fe(III)
reduction in mesophilic Bacteria, the mechanisms for electron transport to Fe(III) have
yet to be elucidated (Lovley 2000).
The finding that the capacity for Fe(III) reduction is so highly conserved in
hyperthermophiles suggests that Fe(III) reduction is still an important process in
modern, hot microbial ecosystems. Many hot environments, which are cool enough to
support life, are at anoxic/oxic boundaries in which hot, anoxic, Fe(II)-rich
hydrothermal fluids contact cooler, oxic environments. The oxidation of Fe(II) at the
anoxic/oxic boundary can produce significant quantities of Fe(III) which precipitates
onto the surrounding hot sediments where it can potentially serve as an electron
acceptor (Jannasch 1995; Karl 1995). Thus, although, Fe(III) reduction in hot,
microbial ecosystems has received little attention, a better understanding of this process
is likely to provide significant insight into microbial activity in hot environments such
as those that may have led to the evolution of early life.
5. Acknowledgements
I thank Dawn Holmes for preparing the phylogenetic tree and Kazem Kashefi and Jason
Tor for sharing unpublished data. This research was supported by the National Science
Foundation LExEn Program grant MCB-0085365.
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