Geotimes
Highlights
Geomicrobiology
Jan P. Amend


In 1983, Stanley Awramik at the University of California, Santa Barbara, and colleagues discovered fossils of microorganisms in 3.556 billion-year-old rocks of the Warrawoona Group in Western Australia. A decade later, based on exquisitely preserved filamentous microbes from the Apex chert, also in the Warrawoona Group, Bill Schopf at the University of California, Los Angeles, apparently found evidence of oxygen-producing, photosynthetic life at 3.465 billion years. In 1996, Steve Mojzsis, then at Scripps Institute of Oceanography, and others used apparent chemical evidence of biological activity, so-called chemofossils, to push the date for life's origin back beyond 3.8 billion years — analyzing isotopically light carbon within apatite grains from sedimentary sequences in West Greenland.

For the past 20 years, geologists and biologists have confidently cited these studies as proof that metabolically and morphologically advanced microorganisms have inhabited Earth for at least 3.5 billion years and perhaps significantly longer. However, several papers published last year challenge some of the biological and chemical fossil evidence. Advances in geomicrobiology in 2002 were also made in deciphering microbial metabolic strategies that are completely independent from sunlight and from the seemingly omnipresent products of photosynthesis — biomass and oxygen. These studies combined culturing-independent microbiology (where the organisms are not cultured and only their DNA or RNA is analyzed), chemical analyses of deep crustal water and hydrothermal fluids, and calculations of reaction energetics.

The oldest biofossils

The geologic source of the 3.556 billion-year-old samples proved questionable, but Schopf and others reexamined the 3.465 billion-year-old filaments for their authenticity with Laser-Raman spectroscopy, focusing in particular on the compositional aspects of the fossilized materials (Nature, v. 416, 2002, p. 73-76). The new data reasserted the biogenicity, or biological origin, of the Apex chert filaments. Other investigators, however, do not agree with these conclusions. They contend that Schopf's fossils are likely artifacts, based on reinterpretations of the Warrawoona structures — after new geologic mapping, more extensive optical and electron microscopy, stable isotopic analyses, and Raman spectroscopy of other carbonaceous materials.

Martin Brasier at the University of Oxford and others suggest that the locality of the Apex chert microfossils is not, as previously suggested, a bedded conglomerate, but rather a metalliferous hydrothermal vein that formed at temperatures of 250 to 350 C — more than 100 C hotter than even the most optimistic view of the upper limit for life (Nature, v. 416, 2002, p. 76-81). They further argue that abiotic synthesis may be responsible for the reduced carbon compounds analyzed in the chert and their light isotopic signatures. Jill Pasteris and Brigitte Wopenka of Washington University take further issue with the Raman analysis of the Apex fossils (Nature, v. 420, 2002, p. 476-477). They note that this technique can in no way unambiguously identify biogenic carbon, citing numerous examples of clearly non-biogenic carbon compounds that yield spectra indistinguishable from Schopf's spectra. In their reply, Schopf and colleagues state that Raman spectra can hint at biogenicity, but add that these data should always be interpreted in connection with other lines of evidence — evidence, which, however, is also being reevaluated (Nature, v. 420, 2002, p. 477).

The oldest chemofossils

In May of last year, Chris Fedo and Martin Whitehouse reported evidence that directly contradicts the origin of the Greenland rocks that harbor the oldest chemofossils (Science, v. 296, 2002, p. 1448-1452). What Mojzsis and colleagues described as a metamorphosed sedimentary banded iron formation, Fedo and Whitehouse interpreted as an ultramafic igneous rock. This reinterpretation is largely based on trace element comparisons between this and various igneous rocks and on a different reading of the regional geologic history. The new view, if accurate, precludes that the isotopically light, graphitic carbon analyzed by Mojzsis' group represents a biological signature. Whether or not the rocks in question are sedimentary in origin remains unresolved, and, consequently, so does the validity of the chemofossils at about 3.8 billion years (Palin, Science, v. 298, 2002, p. 961).

Sunlight-independent microbial metabolism

Solar radiation provides energy to photosynthetic life, driving the progression of otherwise thermodynamically unfavorable reactions. A few studies notwithstanding, there is a consensus, however, that the earliest organisms on Earth were chemotrophs and not phototrophs. In addition, approximately the first billion years of life predated oxygenic photosynthesis. Hence, finding extant communities that live completely independent from photosynthesis is of great interest. Such communities and their environments would provide significant clues not only for understanding life's origin on Earth, but also for elucidating extraterrestrial ecosystems {emdash} most directly, subsurface abodes for microbes on Mars and Europa.

In January 2002, Francis Chapelle and others described a hydrogen-based microbial community 200 meters down in the subsurface hydrothermal groundwater of Lidy Hot Springs in Idaho (Nature, v. 415, 2002, p. 312-315). Based on three different culturing-independent molecular techniques, they determined that more than 95 percent of the microbial population belonged to the domain Archaea (which together with the domain Bacteria defines the prokaryotes); no eukaryotes and only 1 to 5 percent Bacteria were present. Further, phylogenetic analyses revealed that more than 90 percent of the archaeal sequences were most closely related to methanogens — strict anaerobes that use carbon dioxide to oxidize hydrogen, forming methane and water. Geochemical analyses showed that neither organic carbon nor oxygen, which are common products of photosynthesis, figured in the microbial metabolism at this site. Chapelle and colleagues argue that hot water-rock interactions produced the hydrogen, which serves as the primary energy for these subsurface communities.

Hydrogen is also a critical source of energy and reducing power in other continental and marine hydrothermal ecosystems. A recent review on this topic by Anna-Louise Reysenbach and Everett Shock (Science, v. 296, 2002, p. 1077-1082) reminds us that methanogenesis and sulfur-reduction — two hydrogen-consuming processes — are common metabolic strategies of primary producers deep in the global phylogenetic tree of life. Many high temperature Archaea and Bacteria, most of which thrive in the dark subsurface, are fueled by thermodynamically favorable, but kinetically inhibited redox reactions. Reysenbach and Shock also note that both genomes and rocks are "records of evolutionary changes;" once encoded and annotated, they may reveal how Earth became habitable first to chemosynthetic, most likely thermophilic, single-celled life — later to photosynthesizers, eukaryotes, and ultimately the explosion of multicellular organisms.

Expanding the field

Although the timing and process of life's origin remain obscured and the extent to which life inhabits Earth's subsurface and extraterrestrial planets remains unbounded, the sandbox in which a geomicrobiologist plays is rapidly expanding. Rovers will scour the martian surface next year looking for clues to life. Ocean and continental drilling programs are aggressively incorporating — in fact rallying around — geomicrobiology. This year, the National Science Foundation will fund its first research proposals through the Biogeosciences Program. New journals are targeting the biology-geology interface; Geobiology will publish its inaugural volume later this year. In short, the field of geomicrobiology is more dynamic than ever, and the questions being pursued hit at the core of life on Earth … and elsewhere.

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Amend is an assistant professor of microbial geochemistry at Washington University in St. Louis, MO. E-mail: amend@levee.wustl.edu.

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