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Applied and Environmental Microbiology, July 2008, p. 4277-4284, Vol. 74, No. 14
0099-2240/08/$08.00+0     doi:10.1128/AEM.02901-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Genome-Wide Gene Expression Patterns and Growth Requirements Suggest that Pelobacter carbinolicus Reduces Fe(III) Indirectly via Sulfide Production ^,

Shelley A. Haveman,^1* Raymond J. DiDonato Jr.,^1, Laura Villanueva,^1, Evgenya S. Shelobolina,^1,¶ Bradley L. Postier,^1,|| Bo Xu,² Anna Liu,³ and Derek R. Lovley¹

Department of Microbiology,¹ Department of Public Health,² Department of Mathematics and Statistics, University of Massachusetts, Amherst, Massachusetts 01003³

Received 21 December 2007/ Accepted 21 May 2008

Although Pelobacter species are closely related to Geobacter species, recent studies suggested that Pelobacter carbinolicus may reduce Fe(III) via a different mechanism because it lacks the outer-surface c-type cytochromes that are required for Fe(III) reduction by Geobacter sulfurreducens. Investigation into the mechanisms for Fe(III) reduction demonstrated that P. carbinolicus had growth yields on both soluble and insoluble Fe(III) consistent with those of other Fe(III)-reducing bacteria. Comparison of whole-genome transcript levels during growth on Fe(III) versus fermentative growth demonstrated that the greatest apparent change in gene expression was an increase in transcript levels for four contiguous genes. These genes encode two putative periplasmic thioredoxins; a putative outer-membrane transport protein; and a putative NAD(FAD)-dependent dehydrogenase with homology to disulfide oxidoreductases in the N terminus, rhodanese (sulfurtransferase) in the center, and uncharacterized conserved proteins in the C terminus. Unlike G. sulfurreducens, transcript levels for cytochrome genes did not increase in P. carbinolicus during growth on Fe(III). P. carbinolicus could use sulfate as the sole source of sulfur during fermentative growth, but required elemental sulfur or sulfide for growth on Fe(III). The increased expression of genes potentially involved in sulfur reduction, coupled with the requirement for sulfur or sulfide during growth on Fe(III), suggests that P. carbinolicus reduces Fe(III) via an indirect mechanism in which (i) elemental sulfur is reduced to sulfide and (ii) the sulfide reduces Fe(III) with the regeneration of elemental sulfur. This contrasts with the direct reduction of Fe(III) that has been proposed for Geobacter species.

Published ahead of print on 30 May 2008.

Supplemental material for this article may be found at http://aem.asm.org/.

Present address: BIOBASE Corporation, Beverly, MA 01915.

Present address: Harvard FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138.

^¶ Present address: Department of Geology and Geophysics, University of Wisconsin, Madison, WI 53706.

^|| Present address: Department of Biology, Washington University, St. Louis, MO 63130.