DOI: 10.1073/pnas.0505959103. Extracellular respiration of dimethyl sulfoxide by <i>Shewanella oneidensis</i> strain MR-1

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

10.1073/pnas.0505959103

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

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.

Bibliography

Gralnick, J. A., Vali, H., Lies, D. P., & Newman, D. K. (2006). Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proceedings of the National Academy of Sciences, 103(12), 4669â4674.

Authors 4

Jeffrey A. Gralnick (first)
Hojatollah Vali (additional)
Douglas P. Lies (additional)
Dianne K. Newman (additional)

References 51 Referenced 182

M. Begon, J. L. Harper, C. R. Townsend Ecology (Blackwell Scientific, Oxford, 1996). / Ecology by Begon M. (1996)
10.1099/00207713-49-2-705
K. H. Nealson, J. Scott The Prokaryotes, ed M. Dworkin (Springer, New York) Vol. 2004 (2003). / The Prokaryotes by Nealson K. H. (2003)
10.1046/j.1529-8817.1999.3510008.x
10.1016/0304-4203(86)90055-1
10.4319/lo.1980.25.6.1054
10.3354/meps167291
10.1099/13500872-140-8-1953
10.3354/meps203001
A. D. Hatton Deep-Sea Res 49, 3053–3065 (2002). / Deep-Sea Res by Hatton A. D. (2002)
10.4319/lo.1988.33.3.0364
10.4319/lo.1985.30.1.0059
10.1016/S0304-4203(09)90030-5
10.1038/nature00851
10.1038/326655a0
10.1146/annurev.pa.12.040172.002033
10.1046/j.1365-2958.2002.02797.x
10.1016/0005-2728(85)90248-8
10.1146/annurev.genet.38.072902.091138
10.1128/AEM.68.11.5585-5594.2002
10.1128/jb.170.4.1505-1510.1988
10.1111/j.1574-6976.1998.tb00383.x
10.1016/j.resmic.2004.06.013
10.1021/bi034456f
10.1111/j.1472-765X.2004.01611.x
10.1111/j.1365-2958.2005.04628.x
10.1046/j.1365-2958.2001.02403.x
10.1128/JB.184.1.142-151.2002
10.1042/bj3020587
10.1126/science.240.4857.1319
E. L. Mills, K. T. Holeck Clearwaters 31, 22–25 (2001). / Clearwaters by Mills E. L. (2001)
10.1128/AEM.71.2.811-816.2005
10.1099/00207713-47-4-1040
10.3354/ame038081
10.1099/00207713-40-4-331
10.1046/j.1462-2920.2003.00407.x
10.1038/2201315a0
10.1016/S0041-1345(97)00198-X
10.1093/humrep/14.9.2338
10.4319/lo.2001.46.7.1624
10.1073/pnas.0502088102
10.1128/JB.184.6.1806-1810.2002
10.1073/pnas.1834303100
10.1111/j.1365-2672.1994.tb01624.x
10.1016/0378-1119(95)00584-1
10.1073/pnas.0400391101
10.1007/BF01011956
K. Zierold Scan. Electron Microsc 2, 713–724 (1986). / Scan. Electron Microsc by Zierold K. (1986)
10.1083/jcb.95.3.781
10.1016/S0076-6879(83)96041-X
10.1126/science.1093857

Dates

Type	When
Created	19 years, 5 months ago (March 14, 2006, 9:43 p.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 2:07 p.m.)
Indexed	6 days, 7 hours ago (Aug. 31, 2025, 6:31 a.m.)
Issued	19 years, 5 months ago (March 14, 2006)
Published	19 years, 5 months ago (March 14, 2006)
Published Online	19 years, 5 months ago (March 14, 2006)
Published Print	19 years, 5 months ago (March 21, 2006)

Funders 0

None

BibTeX

@article{Gralnick_2006, title={Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1}, volume={103}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0505959103}, DOI={10.1073/pnas.0505959103}, number={12}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Gralnick, Jeffrey A. and Vali, Hojatollah and Lies, Douglas P. and Newman, Dianne K.}, year={2006}, month=mar, pages={4669–4674} }

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