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Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1

Gralnick, Jeffrey A. and Vali, Hojatollah and Lies, Douglas P. and Newman, Dianne K. (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proceedings of the National Academy of Sciences of the United States of America, 103 (12). pp. 4669-4674. ISSN 0027-8424. PMCID PMC1450229. http://resolver.caltech.edu/CaltechAUTHORS:GRApnas06b

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Abstract

Shewanella species are renowned for their respiratory versatility, including their ability to respire poorly soluble substrates by using enzymatic machinery that is localized to the outside of the cell. The ability to engage in "extracellular respiration" to date has focused primarily on respiration of minerals. Here, we identify two gene clusters in Shewanella oneidensis strain MR-1 that each contain homologs of genes required for metal reduction and genes that are predicted to encode dimethyl sulfoxide (DMSO) reductase subunits. Molecular and genetic analyses of these clusters indicate that one (SO1427–SO1432) is required for anaerobic respiration of DMSO. We show that DMSO respiration is an extracellular respiratory process through the analysis of mutants defective in type II secretion, which is required for transporting proteins to the outer membrane in Shewanella. Moreover, immunogold labeling of DMSO reductase subunits reveals that they reside on the outer leaflet of the outer membrane under anaerobic conditions. The extracellular localization of the DMSO reductase in S. oneidensis suggests these organisms may perceive DMSO in the environment as an insoluble compound.


Item Type:Article
Related URLs:
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https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1450229/PubMed CentralArticle
ORCID:
AuthorORCID
Gralnick, Jeffrey A.0000-0001-9250-7770
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2006 by the National Academy of Sciences Edited by Harry B. Gray, California Institute of Technology, Pasadena, CA, and approved January 30, 2006 (received for review July 14, 2005) Published online before print March 14, 2006, 10.1073/pnas.0505959103 We thank the University of Southern California/Agouron Institute 2003 International Geobiology class for technical assistance in isolating type II secretion mutants and Drs. A. Komeili and L. Dietrich for helpful discussions and suggestions. We also thank J. Mui and Dr. S. K. Sears (both of the Facility for Electron Microscopy Research, McGill University) for assistance. This work was supported by grants from the Office of Naval Research, Henry Luce Foundation, Packard Foundation, and the Howard Hughes Medical Institute (to D.K.N.). H.V. acknowledges financial support from the Natural Sciences and Engineering Research Council (NSERC) of Canada. Author contributions: J.A.G., D.P.L., and D.K.N. designed research; J.A.G., H.V., and D.P.L. performed research; H.V. contributed new reagents/analytic tools; J.A.G., H.V., D.P.L., and D.K.N. analyzed data; and J.A.G. H.V., D.P.L., and D.K.N. wrote the paper. Conflict of interest statement: No conflicts declared. This paper was submitted directly (Track II) to the PNAS office.
Funders:
Funding AgencyGrant Number
Office of Naval Research (ONR)UNSPECIFIED
Henry Luce FoundationUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Natural Sciences and Engineering Research Council of Canada (NSERC)UNSPECIFIED
Subject Keywords:DMSO; metabolism; cold temperature adaptation
PubMed Central ID:PMC1450229
Record Number:CaltechAUTHORS:GRApnas06b
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:GRApnas06b
Alternative URL:http://dx.doi.org/10.1073/pnas.0505959103
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:5442
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:17 Oct 2006
Last Modified:24 Oct 2017 15:03

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