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Published online on April 18, 2007, 10.1073/pnas.0610456104

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Microbiology
The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth

( anaerobic food chains | syntrophic metabolism | fatty acid and benzoate utilization )

Michael J. McInerney *, Lars Rohlin {dagger}, Housna Mouttaki *, UnMi Kim {dagger}, Rebecca S. Krupp {dagger}, Luis Rios-Hernandez *, Jessica Sieber *, Christopher G. Struchtemeyer *, Anamitra Bhattacharyya {ddagger}, John W. Campbell {ddagger}, and Robert P. Gunsalus {dagger}{sect}

*Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73019; {ddagger}Integrated Genomics, 2201 West Campbell Park Drive, Chicago, IL 60612; and {dagger}Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, CA 90095

Edited by Ralph S. Wolfe, University of Illinois at Urbana-Champaign, Urbana, IL, and approved March 12, 2007 (received for review November 27, 2006)

Biochemically, the syntrophic bacteria constitute the missing link in our understanding of anaerobic flow of carbon in the biosphere. The completed genome sequence of Syntrophus aciditrophicus SB, a model fatty acid- and aromatic acid-degrading syntrophic bacterium, provides a glimpse of the composition and architecture of the electron transfer and energy-transducing systems needed to exist on marginal energy economies of a syntrophic lifestyle. The genome contains 3,179,300 base pairs and 3,169 genes where 1,618 genes were assigned putative functions. Metabolic reconstruction of the gene inventory revealed that most biosynthetic pathways of a typical Gram-negative microbe were present. A distinctive feature of syntrophic metabolism is the need for reverse electron transport; the presence of a unique Rnf-type ion-translocating electron transfer complex, menaquinone, and membrane-bound Fe-S proteins with associated heterodisulfide reductase domains suggests mechanisms to accomplish this task. Previously undescribed approaches to degrade fatty and aromatic acids, including multiple AMP-forming CoA ligases and acyl-CoA synthetases seem to be present as ways to form and dissipate ion gradients by using a sodium-based energy strategy. Thus, S. aciditrophicus, although nutritionally self-sufficient, seems to be a syntrophic specialist with limited fermentative and respiratory metabolism. Genomic analysis confirms the S. aciditrophicus metabolic and regulatory commitment to a nonconventional mode of life compared with our prevailing understanding of microbiology.

Author contributions: M.J.M., A.B., J.W.C., and R.P.G. designed research; M.J.M., L.R., H.M., A.B., J.W.C., and R.P.G. performed research; M.J.M., L.R., L.R.-H., C.G.S., A.B., and J.W.C. contributed new reagents/analytic tools; M.J.M., L.R., H.M., U.K., R.S.K., L.R.-H., J.S., C.G.S., A.B., J.W.C., and R.P.G. analyzed data; and M.J.M., L.R., J.W.C., and R.P.G. wrote the paper.

Conflict of interest statement: J.W.C. and A.B. were employed by Integrated Genomics, Inc., which performed DNA sequencing and gene-calling analysis under contract to the University of California at Los Angeles. They may be viewed as having commercial interests in the product as a representation of their company's performance.

{sect}To whom correspondence should be addressed.

Robert P. Gunsalus, E-mail: robg{at}microbio.ucla.edu

www.pnas.org/cgi/doi/10.1073/pnas.0610456104
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