Abstract
Dimethyl sulfoxide (DMSO) is an abundant methylated sulfur compound in deep sea ecosystems. However, the mechanism underlying DMSO-induced reduction in benthic microorganisms is unknown. Shewanella piezotolerans WP3, which was isolated from a west Pacific deep sea sediment, can utilize DMSO as the terminal electron acceptor. In this study, two putative dms gene clusters [type I (dmsEFA1B1G1H1) and type II (dmsA2B2G2H2)] were identified in the WP3 genome. Genetic and physiological analyses demonstrated that both dms gene clusters were functional and the transcription of both gene clusters was affected by changes in pressure and temperature. Notably, the type I system is essential for WP3 to thrive under in situ conditions (4°C/20 MPa), whereas the type II system is more important under high pressure or low temperature conditions (20°C/20 MPa, 4°C/0.1 MPa). Additionally, DMSO-dependent growth conferred by the presence of both dms gene clusters was higher than growth conferred by either of the dms gene clusters alone. These data collectively suggest that the possession of two sets of DMSO respiratory systems is an adaptive strategy for WP3 survival in deep sea environments. We propose, for the first time, that deep sea microorganisms might be involved in global DMSO/DMS cycling.
Highlights
Dimethyl sulfoxide (DMSO) concentrations in deep oceanic water are higher than 1.5 nM at depths up to 1,500 m in the equatorial Pacific Ocean and never drop below 1.3 nM at depths up to 4,000 m in the Arabian Sea (Hatton et al, 1996, 1998, 1999)
We found no significant differences in the cell density and DMSO consumption with a further increase in the DMSO concentration (40 or 60 mM) compared with growth at the 25 mM concentration, suggesting that excess DMSO (40 or 60 mM) had no positive effect on the growth yield
We have shown that two dms operons found in S. piezotolerans WP3 are functional in DMSO respiration
Summary
Dimethyl sulfoxide (DMSO) concentrations in deep oceanic water are higher than 1.5 nM at depths up to 1,500 m in the equatorial Pacific Ocean and never drop below 1.3 nM at depths up to 4,000 m in the Arabian Sea (Hatton et al, 1996, 1998, 1999). It is thought to be an environmentally significant compound due to the potential role it plays in the biogeochemical cycle of the climatically active trace gas dimethyl sulfide (DMS; Hatton et al, 2005). DMSO can be produced either through the transformation of DMS by both photooxidation and bio-oxidation routes or by direct production from marine phytoplankton (Hatton et al, 1996; Simó, 1998; Moran et al, 2012). In addition to its roles in protecting cells against photo-generated oxidants and cryogenic damage, DMSO can be used as an alternative electron acceptor for energy conservation through microbial dissimilatory reduction
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