A mechanism for bacterial transformation of dimethylsulfide to dimethylsulfoxide: a missing link in the marine organic sulfur cycle

Lidbury, Ian; Kröber, Eileen; Zhang, Zhidong; Zhu, Yingying; Murrell, J. Colin; Chen, Yin; Schäfer, Hendrik

doi:10.1111/1462-2920.13354

Cited by 50 publications

(64 citation statements)

References 73 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…trimethylamine in R. pomeroyi, as this is accomplished by a trimethylamine monooxygenase (SPO1551) (24). There is no homologue of this protein in R. lacuscaerulensis.…”

Section: Resultsmentioning

confidence: 99%

Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation inRuegeriaSpecies

Wirth

Wang

Huang

et al. 2020

mBio

View full text Add to dashboard Cite

Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. While both Ruegeria pomeroyi and Ruegeria lacuscaerulensis possessed genes encoding the DMSP demethylation and cleavage pathways, their responses to DMSP differed. A glucose-fed, chemostat culture of R. pomeroyi consumed 99% of the DMSP even when fed a high concentration of 5 mM. At the same time, cultures released 19% and 7.1% of the DMSP as dimethylsulfide (DMS) and methanethiol, respectively. Under the same conditions, R. lacuscaerulensis consumed only 28% of the DMSP and formed one-third of the amount of gases. To examine the pathways of sulfur and methyl C assimilation, glucose-fed chemostats of both species were fed 100 μM mixtures of unlabeled and doubly labeled [dimethyl-13C, 34S]DMSP. Both species derived nearly all of their sulfur from DMSP despite high sulfate availability. In addition, only 33% and 50% of the methionine was biosynthesized from the direct capture of methanethiol in R. pomeroyi and R. lacuscaerulensis, respectively. The remaining methionine was biosynthesized by the random assembly of free sulfide and methyl-tetrahydrofolate derived from DMSP. Thus, although the two species possessed similar genes encoding DMSP metabolism, their growth responses were very different. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is abundant in marine environments and an important source of reduced carbon and sulfur for marine bacteria. DMSP is the precursor for the majority of atmospheric dimethylsulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Although research into the assimilation of DMSP has been conducted for over 20 years, the fate of DMSP in microbial biomass is not well understood. In particular, the biosynthesis of methionine from DMSP has been a focal point, and it has been widely believed that most methionine was synthesized via the direct capture of methanethiol. Using an isotopic labeling strategy, we have demonstrated that the direct capture of methanethiol is not the primary pathway used for methionine biosynthesis in two Ruegeria species, a genus comprised primarily of globally abundant marine bacteria. Furthermore, although the catabolism of DMSP by these species varied greatly, the anabolic pathways were highly conserved.

show abstract

“…trimethylamine in R. pomeroyi, as this is accomplished by a trimethylamine monooxygenase (SPO1551) (24). There is no homologue of this protein in R. lacuscaerulensis.…”

Section: Resultsmentioning

confidence: 99%

Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation inRuegeriaSpecies

Wirth

Wang

Huang

et al. 2020

mBio

View full text Add to dashboard Cite

show abstract

“…Furthermore, MeSH can be formed from DMS via microbial demethylation (Kiene & Hines, ). DMS can also be either a product of the biological reduction of DMSO or produce DMSO through either photochemical oxidation (Bentley & Chasteen, ) or by bacteria containing the DMS hydrogenase gene ( ddhA ; McDevitt et al, ) or the trimethylamine monooxygenase gene ( tmm ; Lidbury et al, ). Sulfate‐reducing bacteria and methanogens are both genetically capable of reducing DMS, with methanogens outcompeting sulfate‐reducing bacteria at high concentrations of DMS (Lomans et al, ).…”

Section: Introductionmentioning

confidence: 99%

The Production and Fate of Volatile Organosulfur Compounds in Sulfidic and Ferruginous Sediment

et al. 2019

View full text Add to dashboard Cite

Volatile organic sulfur compounds (VOSCs) link the atmospheric, marine, and terrestrial sulfur cycles in marine and marginal marine environments. Despite the important role VOSCs play in global biogeochemical sulfur cycling, less is known about how the local geochemical conditions influence production and consumption of VOSCs. We present a study of dimethyl sulfide (DMS), methanethiol (MeSH), and dimethylsulfoniopropionate (DMSP) in sulfide-rich (sulfidic) and iron-rich (ferruginous) salt marsh sediment from north Norfolk, UK. Initial results illustrate the importance of minimizing time between sampling in remote field locations and laboratory analysis, due to rapid degradation of VOSCs. With rapid analysis of sediment from different depths, we observe high concentrations of DMS, MeSH, and DMSP, with concentrations in surface sediment an order of magnitude higher than those in previous studies of surface water. We measure systematic differences in the concentration and depth distribution of MeSH and DMS between sediment environments; DMS concentrations are higher in ferruginous sediment, and MeSH concentrations are higher in sulfidic sediment. With repeated measurements over a short time period, we show that the degradation patterns for DMS and MeSH are different in the ferruginous versus sulfidic sediment. We discuss potential biogeochemical interactions that could be driving the observed differences in VOSC dynamics in ferruginous and sulfidic sediment. Plain Language SummaryOceans and coastal wetlands are dynamic environments where the carbon, sulfur, and iron biogeochemical cycles are tightly coupled. One important process that occurs in these environments is the formation of organic sulfur gases, which are involved in cloud formation and acid rain. Organic sulfur gases can be formed through a number of biological and chemical pathways, but little is known about how environmental conditions influence the chemical and microbial reactions that form these gases. In this study, we investigate how different chemical environments in salt marsh sediment influence the formation and destruction of organic sulfur gases. Different organic sulfur gases are produced in iron-rich environments compared to those produced in sulfide-rich environments. Further, the two geochemical environments also showed different patterns in the breakdown of these gases. These results indicate that the geochemical conditions influence how organic sulfur gases form and how they are released to the atmosphere. These findings have the potential to help explain observed differences in the release of organic sulfur gases among modern-day environments, as well as how the release of organic sulfur gases may have changed throughout Earth history as environmental conditions evolved.

show abstract

“…DMS production is balanced by losses that include reactions with reactive oxygen species (ROS), which may be a major source of cellular DMSO (Spiese et al, 2016). The enzymatic oxidation of DMS to DMSO can also provide an important energy source for marine bacteria (Lidbury et al, 2016). However, among marine bacteria only highly specialized methylotrophs have been shown to grow on DMS as a carbon source (Vila-Costa et al, 2006;del Valle et al, 2007, del Valle et al, 2009Hatton et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Modelling dimethylsulfide diffusion in the algal external boundary layer: implications for mutualistic and signalling roles

Lavoie

Galí

Sévigny

et al. 2018

Environmental Microbiology

View full text Add to dashboard Cite

Summary Dimethylsulfide (DMS), a dominant organic sulfur species in the surface ocean, may act as a signalling molecule and contribute to mutualistic interactions between bacteria and marine algae. These proposed functions depend on the DMS concentration in the vicinity of microorganisms. Here, we modelled the DMS enrichment at the surface of DMS‐releasing marine algal cells as a function of DMS production rate, algal cell radius and turbulence. Our results show that the DMS concentration at the surface of unstressed phytoplankton with low DMS production rates can be enriched by <1 nM, whereas for mechanically stressed algae with high activities of the enzyme DMSP‐lyase (a coccolithophore and a dinoflagellate) DMS cell surface enrichments can reach ~10 nM, and could potentially reach μM levels in large cells. These DMS enrichments are much higher than the median DMS concentration in the surface ocean (1.9 nM), and thus may attract and support the growth of bacteria living in the phycosphere. The bacteria in turn may provide photoactive iron chelators (siderophores) that enhance algal iron uptake and provide algal growth factors such as auxins and vitamins. The present study highlights new insights on the extent and impact of microscale DMS enrichments at algal surfaces, thereby contributing to our understanding of the potential chemoattractant and mutualistic roles of DMS in marine microorganisms.

show abstract

A mechanism for bacterial transformation of dimethylsulfide to dimethylsulfoxide: a missing link in the marine organic sulfur cycle

Cited by 50 publications

References 73 publications

Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation inRuegeriaSpecies

Dimethylsulfoniopropionate Sulfur and Methyl Carbon Assimilation inRuegeriaSpecies

The Production and Fate of Volatile Organosulfur Compounds in Sulfidic and Ferruginous Sediment

Modelling dimethylsulfide diffusion in the algal external boundary layer: implications for mutualistic and signalling roles

Contact Info

Product

Resources

About