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Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1 ^,

Gregory J. Dick,^1, Sheila Podell,¹ Hope A. Johnson,^1, Yadira Rivera-Espinoza,^1,¶ Rizlan Bernier-Latmani,^1,|| James K. McCarthy,¹ Justin W. Torpey,² Brian G. Clement,^1, Terry Gaasterland,¹ and Bradley M. Tebo^1*

Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive, La Jolla, California 92093-0202,¹ Biomolecular Mass Spectrometry Facility, Department of Chemistry and Biochemistry, University of California, San Diego, 9500 Gilman Drive, La Jolla, California 92093-0378²

Received 19 July 2007/ Accepted 2 March 2008

Microbial Mn(II) oxidation has important biogeochemical consequences in marine, freshwater, and terrestrial environments, but many aspects of the physiology and biochemistry of this process remain obscure. Here, we report genomic insights into Mn(II) oxidation by the marine alphaproteobacterium Aurantimonas sp. strain SI85-9A1, isolated from the oxic/anoxic interface of a stratified fjord. The SI85-9A1 genome harbors the genetic potential for metabolic versatility, with genes for organoheterotrophy, methylotrophy, oxidation of sulfur and carbon monoxide, the ability to grow over a wide range of O₂ concentrations (including microaerobic conditions), and the complete Calvin cycle for carbon fixation. Although no growth could be detected under autotrophic conditions with Mn(II) as the sole electron donor, cultures of SI85-9A1 grown on glycerol are dramatically stimulated by addition of Mn(II), suggesting an energetic benefit from Mn(II) oxidation. A putative Mn(II) oxidase is encoded by duplicated multicopper oxidase genes that have a complex evolutionary history including multiple gene duplication, loss, and ancient horizontal transfer events. The Mn(II) oxidase was most abundant in the extracellular fraction, where it cooccurs with a putative hemolysin-type Ca²⁺-binding peroxidase. Regulatory elements governing the cellular response to Fe and Mn concentration were identified, and 39 targets of these regulators were detected. The putative Mn(II) oxidase genes were not among the predicted targets, indicating that regulation of Mn(II) oxidation is controlled by other factors yet to be identified. Overall, our results provide novel insights into the physiology and biochemistry of Mn(II) oxidation and reveal a genome specialized for life at the oxic/anoxic interface.

Published ahead of print on 14 March 2008.

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

Address after 1 September 2008: Department of Geological Sciences, University of Michigan, 1100 N. University Avenue, Ann Arbor, MI 48109-1005.

Present address: The Scripps Research Institute, La Jolla, CA 92037.

^¶ Present address: Departamento de Graduados e Investigación en Alimentos, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Carpio y Plan de Ayala, C.P. 11340, Mexico City, Mexico.

^|| Present address: Environmental Microbiology Laboratory, ISTE, ENAC, Ecole, Polytechnique Federale de Lausanne (EPFL), CH 1015 Lausanne, Switzerland.

Present address: Verenium Corporation, San Diego, CA.