Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones

Eutrophication and global climate change lead to expansion of hypoxia in the ocean, often accompanied by the production of hydrogen sulfide, which is toxic to higher organisms. Chemoautotrophic bacteria are thought to buffer against increased sulfide concentrations by oxidizing hydrogen sulfide befo...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 2; pp. 506 - 510
Main Authors: Grote, Jana, Schott, Thomas, Bruckner, Christian G, Glöckner, Frank Oliver, Jost, Günter, Teeling, Hanno, Labrenz, Matthias, Jürgens, Klaus
Format: Journal Article
Language:English
Published: United States National Academy of Sciences 10-01-2012
National Acad Sciences
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Summary:Eutrophication and global climate change lead to expansion of hypoxia in the ocean, often accompanied by the production of hydrogen sulfide, which is toxic to higher organisms. Chemoautotrophic bacteria are thought to buffer against increased sulfide concentrations by oxidizing hydrogen sulfide before its diffusion to oxygenated surface waters. Model organisms from such environments have not been readily available, which has contributed to a poor understanding of these microbes. We present here a detailed study of "Sulfurimonas gotlandica" str. GD1, an Epsilonproteobacterium isolated from the Baltic Sea oxic-anoxic interface, where it plays a key role in nitrogen and sulfur cycling. Whole-genome analysis and laboratory experiments revealed a high metabolic flexibility, suggesting a considerable capacity for adaptation to variable redox conditions. S. gotlandica str. GD1 was shown to grow chemolithoautotrophically by coupling denitrification with oxidation of reduced sulfur compounds and dark CO2 fixation. Metabolic versatility was further suggested by the use of a range of different electron donors and acceptors and organic carbon sources. The number of genes involved in signal transduction and metabolic pathways exceeds those of other EPSILONPROTEOBACTERIA: Oxygen tolerance and environmental-sensing systems combined with chemotactic responses enable this organism to thrive successfully in marine oxygen-depletion zones. We propose that S. gotlandica str. GD1 will serve as a model organism in investigations that will lead to a better understanding how members of the Epsilonproteobacteria are able to cope with water column anoxia and the role these microorganisms play in the detoxification of sulfidic waters.
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Author contributions: J.G., C.G.B., G.J., M.L., and K.J. designed research; J.G., T.S., C.G.B., M.L., and K.J. performed research; F.O.G. and H.T. contributed new reagents/analytic tools; J.G., T.S., C.G.B., G.J., H.T., M.L., and K.J. analyzed data; and J.G., M.L., and K.J. wrote the paper.
Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved December 2, 2011 (received for review July 15, 2011)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1111262109