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Geomicrobiology and Genomes
Jan P. Amend

Many have proclaimed that genomics will revolutionize geomicrobiology. This revolution seems to have arrived now. At the turn of the millennium, approximately 20 microbial genomes had been sequenced. Most were from thermophilic archaea and bacteria with small genomes (1.5 to 2 megabase pairs) or from pathogens, parasites and other model organisms. In the last four years, researchers fully sequenced and at least partially annotated more than 100 additional genomes, several key players in geomicrobiology among them.

To understand better how microbes drive geologic processes, we are beginning to study the blueprints of cellular function: genes and the proteins they encode. Genomic data, when interpreted in the context of geochemistry and microbial ecology, will on the one hand help elucidate the co-evolution of Earth and its biota through geologic time, and on the other, help identify the capabilities of modern organisms to alter their geochemical environments and serve as agents for bioremediation. Since November 2002, researchers published genome sequences for several of the most important microorganisms found in natural and contaminated geologic environments.

John Heidelberg and colleagues description of the genome of Shewanella oneidensis (Nature Biotechnology, v. 20, p. 1118) confirms and further reveals this bacterium's ability to function both aerobically and anaerobically; its full suite of respiratory metabolisms is staggering. The researchers identified dozens of new genes, including 32 novel cytochromes, that relate to Shewanella's electron transport system. Deciphering such data will cement the link between microbial metabolic activities and redox processes in Earth's geochemical cycles. In addition, a phage identified in the genome may permit molecular engineering to improve Shewanella's role in the bioremediation of pollutant organic compounds and radioactive or otherwise toxic metals. And genome analysis can clarify how Shewanella attaches to and then exploits solid phases, in particular metal (oxy)hydroxides.

The metabolic diversity of Geobacter is also explained by its genome (Methé et al., Science, v. 302, p. 1967). This proteobacterium — which is abundant in diverse soils, the deep continental subsurface and marine sediments — is capable of oxidizing organic matter with various metal oxides, making it another prime target for use in bioremediation. Genetic evidence also points to unsuspected aerobic metabolism, diverse carbon metabolisms, motility and chemotactic behavior. In addition, Daniel Bond and Derek Lovley explored the biotechnological potential of Geobacter — specifically its ability during organic waste oxidation to produce electricity, which can be captured by platinum electrodes (Applied and Environmental Microbiology, v. 69, p. 1548). Furthermore, Kazem Kashefi and colleagues (Applied and Environmental Microbiology, v. 69, p. 2985) expanded the impressive list of physiologic characteristics by showing that a close relative of Geobacter, called Geothermobacter, thrives at temperatures as high as 65 degrees Celsius in deep-sea hydrothermal vent environments.

Phytoplankton floating in the ocean may not catalyze much mineral precipitation or dissolution, but they nevertheless play vital roles in biogeochemical processes and account for half of the global oxygen production annually. The genomes of two Prochlorococcus strains reveal what may be the minimum genetic requirements for an oxygenic photoautotroph (Rocap et al., Nature, v. 424, p. 1042 and Dufresne et al., Proceedings of the National Academy of Sciences, v. 100, p. 10,020). Combined with genome analyses of Synechococcus (Palenik et al., Nature, v. 424, p. 1037) and another Prochlorococcus strain, evolutionary events, including gene transfer, in oxygen producing photosynthetic microbes are beginning to emerge. In addition, we are starting to understand how the open ocean cycles and conserves nutrients, such as nitrogen and iron, and how planktonic organisms respond to changing light intensity and other environmental variables.

The genomes of Shewanella, Geobacter and the cyanobacteria will help to unravel the evolution of microbial metal cycling on Earth and nutrient cycling in the upper oceans. Other geologic targets are waiting. This year, highlights will include the sequencing of Marinobacter, a key organism in iron-cycling in the oceans, and whole genome shotgun sequencing of microbial populations, not merely individual species; Craig Venter and colleagues (Science, in press) used this approach on North Atlantic surface seawater to identify 1.2 million new genes from at least 1,800 species.

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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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