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BIOLOGICAL SCIENCES / MICROBIOLOGY
An unconventional pathway for reduction of CO₂ to methane in CO-grown Methanosarcina acetivorans revealed by proteomics

Daniel J. Lessner^*, Lingyun Li, Qingbo Li^*,, Tomas Rejtar, Victor P. Andreev, Matthew Reichlen^*, Kevin Hill^*, James J. Moran, Barry L. Karger^,¶, and James G. Ferry^*,¶

*Department of Biochemistry and Molecular Biology and Center for Microbial Structural Biology, Pennsylvania State University, 205 South Frear Laboratory, University Park, PA 16802; Barnett Institute and Department of Chemistry, Northeastern University, Boston, MA 02115; and Department of Geosciences and Penn State Astrobiology Research Center, Pennsylvania State University, 220 Deike Building, University Park, PA 16802

Communicated by Lonnie O. Ingram, University of Florida, Gainesville, FL, October 5, 2006 (received for review June 27, 2006)

16929–16934

Methanosarcina acetivorans produces acetate, formate, and methane when cultured with CO as the growth substrate [Rother M, Metcalf WW (2004) Proc Natl Acad Sci USA 101:], which suggests novel features of CO metabolism. Here we present a genome-wide proteomic approach to identify and quantify proteins differentially abundant in response to growth on CO versus methanol or acetate. The results indicate that oxidation of CO to CO₂ supplies electrons for reduction of CO₂ to a methyl group by steps and enzymes of the pathway for CO₂ reduction determined for other methane-producing species. However, proteomic and quantitative RT-PCR results suggest that reduction of the methyl group to methane involves novel methyltransferases and a coenzyme F₄₂₀H₂:heterodisulfide oxidoreductase system that generates a proton gradient for ATP synthesis not previously described for pathways reducing CO₂ to methane. Biochemical assays support a role for the oxidoreductase, and transcriptional mapping identified an unusual operon structure encoding the oxidoreductase. The proteomic results further indicate that acetate is synthesized from the methyl group and CO by a reversal of initial steps in the pathway for conversion of acetate to methane that yields ATP by substrate level phosphorylation. The results indicate that M. acetivorans utilizes a pathway distinct from all known CO₂ reduction pathways for methane formation that reflects an adaptation to the marine environment. Finally, the pathway supports the basis for a recently proposed primitive CO-dependent energy-conservation cycle that drove and directed the early evolution of life on Earth.

anaerobic | Archaea | carbon monoxide

Present address: Center for Pharmaceutical Biotechnology and Department of Microbiology and Immunology, University of Illinois, Chicago, IL 60607-7173.

The authors declare no conflict of interest.

^¶To whom correspondence may be addressed. E-mail: jgf3{at}psu.edu or b.karger{at}neu.edu

© 2006 by The National Academy of Sciences of the USA

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