Patterns and drivers of dimethylsulfide concentration in the northeast subarctic Pacific across multiple spatial and temporal scales.

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 License. The definitive version was published in Biogeosciences 16(8), (2019):1729-1754, doi:10.5194/bg-16-1729-2019.The northeast subarctic Pacific (NESAP) is a globally important source of the climate-active gas dimethylsulfide (DMS), yet the processes driving DMS variability across this region are poorly understood. Here we examine the spatial distribution of DMS at various spatial scales in contrasting oceanographic regimes of the NESAP. We present new high-spatial-resolution measurements of DMS across hydrographic frontal zones along the British Columbia continental shelf, together with key environmental variables and biological rate measurements. We combine these new data with existing observations to produce a revised summertime DMS climatology for the NESAP, yielding a broader context for our sub-mesoscale process studies. Our results demonstrate sharp DMS concentration gradients across hydrographic frontal zones and suggest the presence of two distinct DMS cycling regimes in the NESAP, corresponding to microphytoplankton-dominated waters along the continental shelf and nanoplankton-dominated waters in the cross-shelf transitional zone. DMS concentrations across the continental shelf transition (range < 1–10 nM, mean 3.9 nM) exhibited positive correlations to salinity (r=0.80), sea surface height anomaly (SSHA; r=0.51), and the relative abundance of prymnesiophyte and dinoflagellates (r=0.89). In contrast, DMS concentrations in nearshore coastal transects (range < 1–24 nM, mean 6.1 nM) showed a negative correlation with salinity (r=−0.69; r=−0.78) and SSHA (r=−0.81; r=−0.75) and a positive correlation to relative diatom abundance (r=0.88; r=0.86). These results highlight the importance of bloom-driven DMS production in continental shelf waters of this region and the role of prymnesiophytes and dinoflagellates in DMS cycling further offshore. In all areas, the rate of DMS consumption appeared to be an important control on observed concentration gradients, with higher DMS consumption rate constants associated with lower DMS concentrations. We compiled a data set of all available summertime DMS observations for the NESAP (including previously unpublished results) to examine the performance of several existing algorithms for predicting regional DMS concentrations. None of these existing algorithms was able to accurately reproduce observed DMS distributions across the NESAP, although performance was improved by the use of regionally tuned coefficients. Based on our compiled observations, we derived an average summertime distribution map for DMS concentrations and sea–air fluxes across the NESAP, estimating a mean regional flux of 0.30 Tg of DMS-derived sulfur to the atmosphere during the summer season.We dedicate this article to the memory of Ronald P. Kiene, a wonderful scientist, mentor and friend. His contributions to DMS and DMSP research have shaped our field over the past 3 decades, and he will be missed by many around the world. We also wish to thank many individuals involved in data collection and logistical aspects of the cruises presented here, including scientists from the Institute of Ocean Sciences, the captain and crew of the R/V Oceanus and the CCGS John P. Tully, and members of the Tortell, Kiene, Levine and Hatton laboratory groups. We also thank Theodore Ahlvin for GIS support and both reviewers for their insightful comments. Support for this work was provided from the US National Science Foundation (grant no. 1436344) and from the Natural Sciences and Engineering Research Council of Canada

A novel pathway producing dimethylsulphide in bacteria is widespread in soil environments

The volatile compound dimethylsulphide (DMS) is important in climate regulation, the sulphur cycle and signalling to higher organisms. Microbial catabolism of the marine osmolyte dimethylsulphoniopropionate (DMSP) is thought to be the major biological process generating DMS. Here we report the discovery and characterisation of the first gene for DMSP-independent DMS production in any bacterium. This gene, mddA, encodes a methyltransferase that methylates methanethiol (MeSH) and generates DMS. MddA functions in many taxonomically diverse bacteria including sediment-dwelling pseudomonads, nitrogen-fixing bradyrhizobia and cyanobacteria, and mycobacteria, including the pathogen Mycobacterium tuberculosis. The mddA gene is present in metagenomes from varied environments, being particularly abundant in soil environments, where it is predicted to occur in up to 76% of bacteria. This novel pathway may significantly contribute to global DMS emissions, especially in terrestrial environments, and could represent a shift from the notion that DMSP is the only significant precursor of DMS

Patterns and drivers of dimethylsulfide concentration in the northeast subarctic Pacific across multiple spatial and temporal scales

The northeast subarctic Pacific (NESAP) is a globally important source of the climate-active gas dimethylsulfide (DMS), yet the processes driving DMS variability across this region are poorly understood. Here we examine the spatial distribution of DMS at various spatial scales in contrasting oceanographic regimes of the NESAP. We present new high-spatial-resolution measurements of DMS across hydrographic frontal zones along the British Columbia continental shelf, together with key environmental variables and biological rate measurements. We combine these new data with existing observations to produce a revised summertime DMS climatology for the NESAP, yielding a broader context for our sub-mesoscale process studies. Our results demonstrate sharp DMS concentration gradients across hydrographic frontal zones and suggest the presence of two distinct DMS cycling regimes in the NESAP, corresponding to microphytoplankton-dominated waters along the continental shelf and nanoplankton-dominated waters in the cross-shelf transitional zone. DMS concentrations across the continental shelf transition (range&thinsp;&lt;&thinsp;1–10&thinsp;nM, mean 3.9&thinsp;nM) exhibited positive correlations to salinity (r=0.80), sea surface height anomaly (SSHA; r=0.51), and the relative abundance of prymnesiophyte and dinoflagellates (r=0.89). In contrast, DMS concentrations in nearshore coastal transects (range&thinsp;&lt;&thinsp;1–24&thinsp;nM, mean 6.1&thinsp;nM) showed a negative correlation with salinity (r=-0.69; r=-0.78) and SSHA (r=-0.81; r=-0.75) and a positive correlation to relative diatom abundance (r=0.88; r=0.86). These results highlight the importance of bloom-driven DMS production in continental shelf waters of this region and the role of prymnesiophytes and dinoflagellates in DMS cycling further offshore. In all areas, the rate of DMS consumption appeared to be an important control on observed concentration gradients, with higher DMS consumption rate constants associated with lower DMS concentrations. We compiled a data set of all available summertime DMS observations for the NESAP (including previously unpublished results) to examine the performance of several existing algorithms for predicting regional DMS concentrations. None of these existing algorithms was able to accurately reproduce observed DMS distributions across the NESAP, although performance was improved by the use of regionally tuned coefficients. Based on our compiled observations, we derived an average summertime distribution map for DMS concentrations and sea–air fluxes across the NESAP, estimating a mean regional flux of 0.30&thinsp;Tg of DMS-derived sulfur to the atmosphere during the summer season.</p

Methanethiol-dependent dimethylsulfide production in soil environments

Dimethylsulfide (DMS) is an environmentally important trace gas with roles in sulfur cycling, signalling to higher organisms and in atmospheric chemistry. DMS is believed to be predominantly produced in marine environments via microbial degradation of the osmolyte dimethylsulfoniopropionate (DMSP). However, significant amounts of DMS are also generated from terrestrial environments, for example, peat bogs can emit ~6 μmol DMS m−2 per day, likely via the methylation of methanethiol (MeSH). A methyltransferase enzyme termed ‘MddA’, which catalyses the methylation of MeSH, generating DMS, in a wide range of bacteria and some cyanobacteria, may mediate this process, as the mddA gene is abundant in terrestrial metagenomes. This is the first study investigating the functionality of MeSH-dependent DMS production (Mdd) in a wide range of aerobic environments. All soils and marine sediment samples tested produced DMS when incubated with MeSH. Cultivation-dependent and cultivation-independent methods were used to assess microbial community changes in response to MeSH addition in a grassland soil where 35.9% of the bacteria were predicted to contain mddA. Bacteria of the genus Methylotenera were enriched in the presence of MeSH. Furthermore, many novel Mdd+ bacterial strains were isolated. Despite the abundance of mddA in the grassland soil, the Mdd pathway may not be a significant source of DMS in this environment as MeSH addition was required to detect DMS at only very low conversion rates

High concentrations and turnover rates of DMS, DMSP and DMSO in Antarctic sea ice

Author Posting. © American Geophysical Union, 2011. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Geophysical Research Letters 38 (2011): L23609, doi:10.1029/2011GL049712.The vast Antarctic sea-ice zone (SIZ) is a potentially significant source of the climate-active gas dimethylsulfide (DMS), yet few data are available on the concentrations and turnover rates of DMS and the related compounds dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) in sea ice environments. Here we present new measurements characterizing the spatial variability of DMS, DMSP, and DMSO concentrations across the Antarctic SIZ, and results from tracer experiments quantifying the production rates of DMS from various sources. We observed extremely high concentrations (>200 nM) and turnover rates (>100 nM d−1) of DMS in sea-ice brines, indicating intense cycling of DMS/P/O. Our results demonstrate a previously unrecognized role for DMSO reduction as a major pathway of DMS production in Antarctic sea ice.This work was supported in part by Woods Hole Oceanographic Institution’s Ocean Life Institute and by NSF grant ANT-0838872 to KRA.2012-06-1

The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol

Marine phytoplankton produce ~109 tons of dimethylsulfoniopropionate (DMSP) per year1,2, an estimated 10% of which is catabolized by bacteria through the DMSP cleavage pathway to the climatically active gas dimethyl sulfide (DMS)3,4. SAR11 Alphaproteobacteria (order Pelagibacterales), the most abundant chemoorganotrophic bacteria in the oceans, have been shown to assimilate DMSP into biomass, thereby supplying this cell’s unusual requirement for reduced sulfur5,6. Here we report that Pelagibacter HTCC1062 produces the gas methanethiol (MeSH) and that simultaneously a second DMSP catabolic pathway, mediated by a cupin-like DMSP lyase, DddK, shunts as much as 59% of DMSP uptake to DMS production. We propose a model in which the allocation of DMSP between these pathways is kinetically controlled to release increasing amounts of DMS as the supply of DMSP exceeds cellular sulfur demands for biosynthesis

Bacteria are important dimethylsulfoniopropionate producers in marine aphotic and high-pressure environments

Dimethylsulfoniopropionate (DMSP) is an important marine osmolyte. Aphotic environments are only recently being considered as potential contributors to global DMSP production. Here, our Mariana Trench study reveals a typical seawater DMSP/dimethylsulfide (DMS) profile, with highest concentrations in the euphotic zone and decreased but consistent levels below. The genetic potential for bacterial DMSP synthesis via the dsyB gene and its transcription is greater in the deep ocean, and is highest in the sediment.s DMSP catabolic potential is present throughout the trench waters, but is less prominent below 8000 m, perhaps indicating a preference to store DMSP in the deep for stress protection. Deep ocean bacterial isolates show enhanced DMSP production under increased hydrostatic pressure. Furthermore, bacterial dsyB mutants are less tolerant of deep ocean pressures than wild-type strains. Thus, we propose a physiological function for DMSP in hydrostatic pressure protection, and that bacteria are key DMSP producers in deep seawater and sediment

Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere

Oxidation of methanethiol (MT) is a significant step in the sulfur cycle. MT is an intermediate of metabolism of globally significant organosulfur compounds including dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS), which have key roles in marine carbon and sulfur cycling. In aerobic bacteria, MT is degraded by a MT oxidase (MTO). The enzymatic and genetic basis of MT oxidation have remained poorly characterized. Here, we identify for the first time the MTO enzyme and its encoding gene (mtoX) in the DMS-degrading bacterium Hyphomicrobium sp. VS. We show that MTO is a homotetrameric metalloenzyme that requires Cu for enzyme activity. MTO is predicted to be a soluble periplasmic enzyme and a member of a distinct clade of the Selenium-binding protein (SBP56) family for which no function has been reported. Genes orthologous to mtoX exist in many bacteria able to degrade DMS, other one-carbon compounds or DMSP, notably in the marine model organism Ruegeria pomeroyi DSS-3, a member of the Rhodobacteraceae family that is abundant in marine environments. Marker exchange mutagenesis of mtoX disrupted the ability of R. pomeroyi to metabolize MT confirming its function in this DMSP-degrading bacterium. In R. pomeroyi, transcription of mtoX was enhanced by DMSP, methylmercaptopropionate and MT. Rates of MT degradation increased after pre-incubation of the wild-type strain with MT. The detection of mtoX orthologs in diverse bacteria, environmental samples and its abundance in a range of metagenomic data sets point to this enzyme being widely distributed in the environment and having a key role in global sulfur cycling.The ISME Journal advance online publication, 24 October 2017; doi:10.1038/ismej.2017.148

Unusual Regulation of a Leaderless Operon Involved in the Catabolism of Dimethylsulfoniopropionate in Rhodobacter sphaeroides

Rhodobacter sphaeroides strain 2.4.1 is a widely studied bacterium that has recently been shown to cleave the abundant marine anti-stress molecule dimethylsulfoniopropionate (DMSP) into acrylate plus gaseous dimethyl sulfide. It does so by using a lyase encoded by dddL, the promoter-distal gene of a three-gene operon, acuR-acuI-dddL. Transcription of the operon was enhanced when cells were pre-grown with the substrate DMSP, but this induction is indirect, and requires the conversion of DMSP to the product acrylate, the bona fide co-inducer. This regulation is mediated by the product of the promoter-proximal gene acuR, a transcriptional regulator in the TetR family. AcuR represses the operon in the absence of acrylate, but this is relieved by the presence of the co-inducer. Another unusual regulatory feature is that the acuR-acuI-dddL mRNA transcript is leaderless, such that acuR lacks a Shine-Dalgarno ribosomal binding site and 5′-UTR, and is translated at a lower level compared to the downstream genes. This regulatory unit may be quite widespread in bacteria, since several other taxonomically diverse lineages have adjacent acuR-like and acuI-like genes; these operons also have no 5′ leader sequences or ribosomal binding sites and their predicted cis-acting regulatory sequences resemble those of R. sphaeroides acuR-acuI-dddL