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Journal of Bacteriology, October 2005, p. 7126-7137, Vol. 187, No. 20
0021-9193/05/$08.00+0     doi:10.1128/JB.187.20.7126-7137.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Clustered Genes Related to Sulfate Respiration in Uncultured Prokaryotes Support the Theory of Their Concomitant Horizontal Transfer{dagger}

Marc Mussmann,1* Michael Richter,1 Thierry Lombardot,1 Anke Meyerdierks,1 Jan Kuever,2 Michael Kube,3 Frank Oliver Glöckner,1 and Rudolf Amann1

Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany,1 Bremen Institute for Materials Testing, Paul-Feller-Str. 1, D-28199 Bremen, Germany,2 Max Planck Institute for Molecular Genetics, Ihnestr. 63-73, D-14195 Berlin, Germany3

Received 26 April 2005/ Accepted 26 July 2005

The dissimilatory reduction of sulfate is an ancient metabolic process central to today's biogeochemical cycling of sulfur and carbon in marine sediments. Until now its polyphyletic distribution was most parsimoniously explained by multiple horizontal transfers of single genes rather than by a not-yet-identified "metabolic island." Here we provide evidence that the horizontal transfer of a gene cluster may indeed be responsible for the patchy distribution of sulfate-reducing prokaryotes (SRP) in the phylogenetic tree. We isolated three DNA fragments (32 to 41 kb) from uncultured, closely related SRP from DNA directly extracted from two distinct marine sediments. Fosmid ws39f7, and partially also fosmids ws7f8 and hr42c9, harbored a core set of essential genes for the dissimilatory reduction of sulfate, including enzymes for the reduction of sulfur intermediates and synthesis of the prosthetic group of the dissimilatory sulfite reductase. Genome comparisons suggest that encoded membrane proteins universally present among SRP are critical for electron transfer to cytoplasmic enzymes. In addition, novel, conserved hypothetical proteins that are likely involved in dissimilatory sulfate reduction were identified. Based on comparative genomics and previously published experimental evidence, a more comprehensive model of dissimilatory sulfate reduction is presented. The observed clustering of genes involved in dissimilatory sulfate reduction has not been previously found. These findings strongly support the hypothesis that genes responsible for dissimilatory sulfate reduction were concomitantly transferred in a single event among prokaryotes. The acquisition of an optimized gene set would enormously facilitate a successful implementation of a novel pathway.

* Corresponding author. Mailing address: Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany. Phone: 49-(0)421-2028940. Fax: 49-(0)421-2028690. E-mail: mmussman{at}mpi-bremen.de.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, October 2005, p. 7126-7137, Vol. 187, No. 20
0021-9193/05/$08.00+0     doi:10.1128/JB.187.20.7126-7137.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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