Dimethylsulfoniopropionate Production Research Articles

Effects of micro- and nano-plastics on growth, antioxidant system, DMS, and DMSP production in Emiliania huxleyi

Due to the potential impacts of microplastics (MPs) and nanoplastics (NPs) on algal growth and thereby affect the climate-relevant substances, dimethylsulfoniopropionate (DMSP) and dimethyl sulfide (DMS), we studied the polystyrene (PS) MPs and NPs of 1 μm and 80 nm impacts on the growth, chlorophyll content, reactive oxygen species (ROS), antioxidant enzyme activity, and DMS/DMSP production in Emiliania huxleyi. E. huxleyi is a prominent oceanic alga that plays a key role in DMS and DMSP production. The results revealed that high concentrations of MPs and NPs inhibited the growth, carotenoid (Car), and Chl a concentrations of E. huxleyi. However, short-time exposure to low concentrations of PS MPs and NPs stimulated the growth of E. huxleyi. Furthermore, high concentrations of MPs and NPs resulted in an increase in the superoxide anion radical (O2.–) production rate and a decrease in the malondialdehyde (MDA) content compared with the low concentrations. Exposure to MPs and NPs at 5 mg L−1 induced superoxide dismutase (SOD) activity as a response to scavenging ROS. High concentrations of MPs and NPs significantly inhibited the production of DMSP and DMS. The findings of this study support the potential ecotoxicological impacts of MPs and NPs on algal growth, antioxidant system, and dimethylated sulfur compounds production, which maybe potentially impact the global climate.

The production of dimethylsulfoniopropionate by bacteria with mmtN linked to non-ribosomal peptide synthase gene

ABSTRACT Dimethylsulfoniopropionate (DMSP) is a vital sulfur-containing compound with worldwide significance, serving as the primary precursor for dimethyl sulfide (DMS), a volatile sulfur compound that plays a role in atmospheric chemistry and influences the Earth’s climate on a global scale. The study investigated the ability of four bacterial strains, namely Acidimangrovimonas sediminis MS2-2 (MS2-2), Hartmannibacter diazotrophicus E18T (E18T), Rhizobium lusitanum 22705 (22705), and Nitrospirillum iridis DSM22198 (DSM22198), to produce and degrade DMSP. These strains were assessed for their DMSP synthesis ability with the mmtN linked to non-ribosomal peptide synthase (NRPS) gene. The results showed that MS2-2, and E18T bacteria, which contained the mmtN but not linked to an NRPS gene, increased DMSP production with increasing salinity. The highest production of DMSP was achieved at 25 PSU when either methionine was added or low nitrogen conditions were present, yielding 1656.03 ± 41.04 and 265.59 ± 9.17 nmol/mg protein, respectively, and subsequently under the conditions of methionine addition or low nitrogen, both strains reached their maximum DMSP production at 25 PSU. Furthermore, the strains MS2-2, E18T, and 22705 with the mmtN gene but not linked to an NRPS gene were found to be involved in DMS production. This research contributes to the understanding of the genes involved in DMSP biosynthesis in bacteria that produce DMSP.

Occurrence and emissions of biogenic dimethylated sulfur compounds and their responses to mesoscale eddies and typhoon Yutu in the western tropical Pacific Ocean

The western tropical Pacific Ocean (WTPO) plays a vital role in the global sulfur biogeochemical cycle. Here, an investigation was conducted to explore the spatial variations in biogenic dimethylated sulfur compounds (BDSCs) and their controlling factors in the WTPO in 2018. Dimethylsulfide (DMS) sea-to-air fluxes and the contribution of DMS emissions to the atmospheric sulfate burden were estimated. The concentrations of BDSCs in the surface seawater were low compared to the marginal seas of the western Pacific Ocean, attributed to a limited supply of nutrients and low primary production. Besides, higher values of the BDSCs were observed in surface and subsurface water. The nanophytoplankton was the main dimethylsulfoniopropionate (DMSP) producer, and the abundance of low DMSP and dimethylsulfoxide (DMSO) producers determined the DMSP/O concentrations in the oligotrophic WTPO. Moreover, mixed layer depth might be the crucial factor affecting DMS values. DMS fluxes were low in the WTPO, but they still contributed substantially to global DMS emissions, given the vast areas of the Pacific Ocean. The contribution of biogenic non-sea-salt sulfate (nss-SO42-) to total SO42- reached 25.87%, which showed the oxidation products of DMS were the crucial sources of SO42- in aerosols. Responses of BDSCs to mesoscale eddies and a typhoon were investigated for the first time. The warm eddy increased the concentrations of chlorophyll a (Chl-a) and BDSCs. Nevertheless, no effect of a mesoscale cold eddy on Chl-a or BDSCs was evident. The values of Chl-a, DMS, DMSP, biogenic nss-SO42-, and the DMS fluxes increased after Typhoon Yutu passed, indicating that typhoons play a prominent role in DMS emissions and the global sulfur cycles.

Fungi increases kelp (Ecklonia radiata) remineralisation and dissolved organic carbon, alkalinity, and dimethylsulfoniopropionate (DMSP) production

Fungi are key players in terrestrial organic matter (OM) degradation, but little is known about their role in marine environments. Here we compared the degradation of kelp (Ecklonia radiata) in mesocosms with and without fungicides over 45 days. The aim was to improve our understanding of the vital role of fungal OM degradation and remineralisation and its relevance to marine biogeochemical cycles (e.g., carbon, nitrogen, sulfur, or volatile sulfur). In the presence of fungi, 68 % of the kelp detritus degraded over 45 days, resulting in the production of 0.6 mol of dissolved organic carbon (DOC), 0.16 mol of dissolved inorganic carbon (DIC), 0.23 mol of total alkalinity (TA), and 0.076 mol of CO2, which was subsequently emitted to the atmosphere. Conversely, when fungi were inhibited, the bacterial community diversity was reduced, and only 25 % of the kelp detritus degraded over 45 days. The application of fungicides resulted in the generation of an excess amount of 1.5 mol of DOC, but we observed only 0.02 mol of DIC, and 0.04 mol of TA per one mole of kelp detritus, accompanied by a CO2 emission of 0.081 mol. In contrast, without fungi, remineralisation of kelp detritus to DIC, TA, dimethyl sulfide (DMS), dimethylsulfoniopropionate (DMSP) and methanethiol (MeSH) was significantly reduced. Fungal kelp remineralisation led to a remarkable 100,000 % increase in DMSP production. The observed substantial changes in sediment chemistry when fungi are inhibited highlight the important biogeochemical role of fungal remineralisation, which likely plays a crucial role in defining coastal biogeochemical cycling, blue carbon sequestration, and thus climate regulation.

Microbial Dimethylsulfoniopropionate Cycling in Deep Sediment of the Mariana Trench.

Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.

Highly active bacterial DMSP metabolism in the surface microlayer of the eastern China marginal seas.

The microbial cycling of dimethylsulfoniopropionate (DMSP) and the resulting gaseous catabolites dimethylsulfide (DMS) or methylmercaptan (MeSH) play key roles in the global sulfur cycle and potentially climate regulation. As the ocean-atmosphere boundary, the sea surface microlayer (SML) is important for the generation and emission of DMS and MeSH. However, understanding of the microbial DMSP metabolism remains limited in the SML. Here, we studied the spatiotemporal differences for DMS/DMSP, bacterial community structure and the key bacterial DMSP metabolic genes between SML and subsurface seawater (SSW) samples in the eastern China marginal seas (the East China Sea and Yellow Sea). In general, DMSPd and DMSPt concentrations, and the abundance of total, free-living and particle-associated bacteria were higher in SML than that in SSW. DMSP synthesis (~7.81-fold for dsyB, ~2.93-fold for mmtN) and degradation genes (~5.38-fold for dmdA, ~6.27-fold for dddP) detected in SML were more abundant compared with SSW samples. Free-living bacteria were the main DMSP producers and consumers in eastern Chinese marginal sea. Regionally, the bacterial community structure was distinct between the East China Sea and the Yellow Sea. The abundance of DMSP metabolic genes (dsyB, dmdA, and dddP) and genera in the East China Sea were higher than those of the Yellow Sea. Seasonally, DMSP/DMS level and DMSP metabolic genes and bacteria were more abundant in SML of the East China Sea in summer than in spring. Different from those in spring, Ruegeria was the dominant DMSP metabolic bacteria. In conclusion, the DMSP synthesis and degradation showed significant spatiotemporal differences in the SML of the eastern China marginal seas, and were consistently more active in the SML than in the SSW.

Roles of phytoplankton, microzooplankton, and bacteria in DMSP and DMS transformation processes in the East China Continental Sea

The trace gas dimethylsulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) are the most abundant oceanic biogenic organosulfur molecules. Phytoplankton, zooplankton, and bacteria are the most vital biotic factors controlling DMSP and DMS, but their relative effects on the transformation processes still remain uncertain due to their complex biogeochemistry. Here, we provided the relative transformation rates of DMSP and DMS, and their relationships with phytoplankton, microzooplankton, and bacteria in the East China Continental Sea in the summer of 2018. The phytoplankton was the major DMSP producer, contributing 89.8% of DMSP stock with the particulate DMSP production rate at 42.0 nmol L−1 d−1. The DMSP lyase activity was 140.5 nmol DMS L−1h−1, resulting in a short DMSP fate (0.8 d). The microzooplankton grazing resulted in DMSP loss and DMS production at the rates of −49.3 and 8.2 nmol L−1 d−1, equaling 60.0% of total DMSP loss and 71.6% of DMS microbial production. The dissolved DMSP degradation and DMS microbial production rates were at −23.4 and 11.5 nmol L−1 d−1, largely controlled by bacterial abundance. Microbial consumption, photolysis, and ventilation accounted for 41%, 43%, and 16% of surface DMS removal, indicating that most of the DMS was consumed within the surface. Finally, DMS was enriched in the sediment but not significantly enriched in the surface microlayer, with enrichment factors at 3.7 and 1.0, respectively. The budget model in this study could help better estimate the roles of phytoplankton, microzooplankton, and bacteria in DMSP and DMS transformation processes in the continental shelf seas.

Microbially Driven Sulfur Cycling in the River–Wetland–Ocean Continuum

Sulfur (S) is an essential biological element, and S cycling is mainly driven by metabolically versatile microorganisms. The river–wetland–ocean (RWO) continuum here is defined as the dynamically connected region with estuary, wetland, and near-marine ecosystems, and it is considered a hotspot of biogeochemical cycling, especially a major biotope for S cycling. Various forms and oxidation states of S compounds are considered ideal electron donors or acceptors and are widely utilized by microorganisms via inorganic or organic S-cycling processes. The S-cycling pathways are intimately linked to the carbon (C), nitrogen, phosphorus, and metal cycles, playing crucial roles in biogeochemical cycling, C sequestration, and greenhouse gas emissions through various mechanisms in the RWO continuum. This review provides a comprehensive understanding of microbially driven S cycling in the RWO continuum. We first illustrate the importance of S cycling in this continuum, including key microorganisms and functional processes (e.g., dissimilatory sulfate reduction, S oxidation, dimethylsulfoniopropionate production, and catabolism) as well as their corresponding S flux characteristics. In particular, we emphasize recent advances in the coupling mechanisms of the S cycle with other major element cycles. We further propose important perspectives for developing microbiome engineering of S-cycling microbial communities via integration of current knowledge about the multidimensional diversity, cultivation, evolution, and interaction of S-cycling microorganisms and their coupling mechanisms in the RWO continuum, providing a new window on applying microbiome-based biotechnologies to overcome global climate challenges.

Production of dimethylsulfoniopropionate, dimethylsulfide and acrylic acid from marine microalgae

Production of dimethylsulfoniopropionate (DMSP), dimethylsulfide (DMS), and acrylic acid (AA) from 22 marine microalgae representing six phyla were examined at different growth stages. The concentrations of DMSP, DMS, and AA per cell in the media showed significant changes during the whole growth period, and the highest concentrations were found at the stationary growth phase or the senescent phase. Different species had different concentration levels of DMSP, DMS, and AA, among which Pyrrhophyta, Bacillariophyte, and Chrysophyta had relatively large release. The highest concentrations of DMSP, DMS, and AA were 56.70, 0.86, and 44.60 fmol cell−1 in Scrippsiella trochoidea, Prymnesiacee, and Karenia mikimotoi, respectively. The ratios of DMS/DMSP and AA/(DMSP+AA) in the 22 marine microalgae differed dramatically over the growth cycle. The DMS/DMSP ratios were <25%, indicating that only a small fraction of DMSP was converted to DMS by enzymatic cleavage. Moreover, there was a higher ratio of enzymatic degradation of DMSP in the senescent growth stage. The AA/(DMSP+AA) ratio, representing the degradation ratio of DMSP, increased significantly at the beginning of growth period and then decreased. Hence, the changes in these ratios could approximately illustrate the degradation mechanism of DMSP among diverse species at different growth phases.

Microbial dimethylsulfoniopropionate (DMSP) cycling in the ultraoligotrophic eastern Indian Ocean

Dimethylsulfoniopropionate (DMSP) is an important source of dissolved organic matter for the marine food web and its cycling is a key step in ocean-atmosphere fluxes involved in the global sulfur cycle. To date, the abundance and biogeography of the genes encoding bacterial DMSP cycling in the eastern Indian Ocean (EIO) is virtually unknown. Moreover, DMSP measurements from the IO are sparse compared to other major oceans. In May–June 2019, we characterized dissolved DMSP (DMSPd) concentrations and the abundance of representative bacterial DMSP cycling genes along the 110 °E transect line as part of a voyage that contributed to Australia's involvement in the second International Indian Ocean Expedition. During the multidisciplinary voyage, surface water samples were collected from 19 stations spanning temperate to tropical waters of the EIO (39.5 °S to 11.5 °S, 110 °E). Somewhat surprisingly, a trend of greater DMSPd was measured in ultraoligotrophic (<0.02 μmol L−1 of nitrate/nitrite), low latitude waters compared to relatively nutrient-rich high latitudes, which contradicts global DMSPd patterns of high concentrations at high latitudes. Additionally, the average DMSPd concentration in EIO samples (17.2 ± 18.64 nM) was an order of magnitude greater than concentrations previously reported at similar latitudes in the Pacific and Atlantic Oceans, which suggests DMSPd is a readily available food source for microbes in a region that is often considered an ocean desert. The abundances of the bacterial DMSP production gene (dsyB), the DMSP lyase gene (dddP) and phylogenetically diverse DMSP demethylation genes (dmdA subclade A/1, D/all and E/2) were reported for the first time in the EIO region, demonstrating significant shifts in all genes with latitude. The SAR11 dmdA (D/all) gene was the dominant DMSP degradation gene across the transect (3.4 ± 0.94% of bacteria) and was notably positively correlated to DMSPd, demonstrating a tight coupling between the variables across the 30° transect. Our results also showed greater DMSPd and relative abundance of genes encoding both DMSP degradation pathways (dddP, dmdA A/1 and D/all) within a Leeuwin Current meander when compared to adjacent stations outside of the meander, providing evidence that mesoscale perturbations from the Leeuwin Current can greatly influence the EIO sulfur cycle. Overall, our data indicates that reduced sulfur in the form of DMSP is an abundant and readily available food source for some microbial metabolisms within the ultraoligotrophic surface waters of the EIO.

Succession of protistan functional traits is influenced by bloom timing

Surface ocean eukaryotic phytoplankton biogeography can be determined as chlorophyll-a using remote sensing techniques yet evaluating its community composition remains limited. Given our ability to track site-specific chlorophyll-a concentration, we tested which factors influenced protistan functional trait distribution, and whether the distributions can be inferred from bloom succession. Here we surveyed the Labrador Sea during spring over three consecutive years, sequenced 18S data over 15 stations and collected satellite-derived chlorophyll-a concentration from March to July for each year. We evaluated changes in distribution of taxonomic composition as well as the functional traits of protistan size, trophic strategy (defined as phototrophy, phagotrophy, and mixotrophy as capable of both), motility and dimethylsulfoxide or dimethylsulfoniopropionate production by building a functional trait database after an extensive literature review. More variability in the biogeography of protistan functional traits was explained across water masses, and among years than taxonomic composition and patterns in trait variability were more apparent when site-specific timing of peak chlorophyll-a was considered. We found that reconstructing bloom phenology using days before peak (DBP) chlorophyll explained a significant amount of variability in functional trait community structure that was previously attributed to water masses or years, suggesting that spatial and interannual variations can be explained by the sampling moment during succession. Approximately 30 days prior to peak, mixotrophy as a trophic strategy was replaced by phototrophic protists of typically larger size classes. Our work suggests DBP influences protistan community trait succession that could inform biogeochemical models, and likely acts a proxy for the onset of stratification.

The Microbiological Drivers of Temporally Dynamic Dimethylsulfoniopropionate Cycling Processes in Australian Coastal Shelf Waters.

The organic sulfur compounds dimethylsulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) play major roles in the marine microbial food web and have substantial climatic importance as sources and sinks of dimethyl sulfide (DMS). Seasonal shifts in the abundance and diversity of the phytoplankton and bacteria that cycle DMSP are likely to impact marine DMS (O) (P) concentrations, but the dynamic nature of these microbial interactions is still poorly resolved. Here, we examined the relationships between microbial community dynamics with DMS (O) (P) concentrations during a 2-year oceanographic time series conducted on the east Australian coast. Heterogenous temporal patterns were apparent in chlorophyll a (chl a) and DMSP concentrations, but the relationship between these parameters varied over time, suggesting the phytoplankton and bacterial community composition were affecting the net DMSP concentrations through differential DMSP production and degradation. Significant increases in DMSP were regularly measured in spring blooms dominated by predicted high DMSP-producing lineages of phytoplankton (Heterocapsa, Prorocentrum, Alexandrium, and Micromonas), while spring blooms that were dominated by predicted low DMSP-producing phytoplankton (Thalassiosira) demonstrated negligible increases in DMSP concentrations. During elevated DMSP concentrations, a significant increase in the relative abundance of the key copiotrophic bacterial lineage Rhodobacterales was accompanied by a three-fold increase in the gene, encoding the first step of DMSP demethylation (dmdA). Significant temporal shifts in DMS concentrations were measured and were significantly correlated with both fractions (0.2–2 μm and >2 μm) of microbial DMSP lyase activity. Seasonal increases of the bacterial DMSP biosynthesis gene (dsyB) and the bacterial DMS oxidation gene (tmm) occurred during the spring-summer and coincided with peaks in DMSP and DMSO concentration, respectively. These findings, along with significant positive relationships between dsyB gene abundance and DMSP, and tmm gene abundance with DMSO, reinforce the significant role planktonic bacteria play in producing DMSP and DMSO in ocean surface waters. Our results highlight the highly dynamic nature and myriad of microbial interactions that govern sulfur cycling in coastal shelf waters and further underpin the importance of microbial ecology in mediating important marine biogeochemical processes.

Mechanistic insights into the key marine dimethylsulfoniopropionate synthesis enzyme DsyB/DSYB.

Marine algae and bacteria produce approximately eight billion tonnes of the organosulfur molecule dimethylsulfoniopropionate (DMSP) in Earth's surface oceans annually. DMSP is an antistress compound and, once released into the environment, a major nutrient, signaling molecule, and source of climate-active gases. The methionine transamination pathway for DMSP synthesis is used by most known DMSP-producing algae and bacteria. The S-directed S-adenosylmethionine (SAM)-dependent 4-methylthio-2-hydroxybutyrate (MTHB) S-methyltransferase, encoded by the dsyB/DSYB gene, is the key enzyme of this pathway, generating S-adenosylhomocysteine (SAH) and 4-dimethylsulfonio-2-hydroxybutyrate (DMSHB). DsyB/DSYB, present in most haptophyte and dinoflagellate algae with the highest known intracellular DMSP concentrations, is shown to be far more abundant and transcribed in marine environments than any other known S-methyltransferase gene in DMSP synthesis pathways. Furthermore, we demonstrate in vitro activity of the bacterial DsyB enzyme from Nisaea denitrificans and provide its crystal structure in complex with SAM and SAH-MTHB, which together provide the first important mechanistic insights into a DMSP synthesis enzyme. Structural and mutational analyses imply that DsyB adopts a proximity and desolvation mechanism for the methyl transfer reaction. Sequence analysis suggests that this mechanism may be common to all bacterial DsyB enzymes and also, importantly, eukaryotic DSYB enzymes from e.g., algae that are the major DMSP producers in Earth's surface oceans.

Insights into methionine S-methylation in diverse organisms

Dimethylsulfoniopropionate (DMSP) is an important marine anti-stress compound, with key roles in global nutrient cycling, chemotaxis and, potentially, climate regulation. Recently, diverse marine Actinobacteria, α- and γ-proteobacteria were shown to initiate DMSP synthesis via the methionine (Met) S-methyltransferase enzyme (MmtN), generating S-methyl-Met (SMM). Here we characterize a roseobacterial MmtN, providing structural and mechanistic insights into this DMSP synthesis enzyme. We propose that MmtN uses the proximity and desolvation mechanism for Met S-methylation with two adjacent MmtN monomers comprising the Met binding site. We also identify diverse functional MmtN enzymes in potentially symbiotic archaeal Candidatus Woesearchaeota and Candidate Phyla Radiation (CPR) bacteria, and the animalcule Adineta steineri, not anticipated to produce SMM and/or DMSP. These diverse MmtN enzymes, alongside the larger plant MMT enzyme with an N-terminus homologous to MmtN, likely utilize the same proximity and desolvation mechanism. This study provides important insights into the catalytic mechanism of SMM and/or DMSP production, and proposes roles for these compounds in secondary metabolite production, and SMM cycling in diverse organisms and environments.

DMSP Production by Coral-Associated Bacteria

Dimethylsulfoniopropionate (DMSP) is an important molecule in the marine sulfur cycle, produced in large amounts by corals and their dinoflagellate endosymbionts, Symbiodiniaceae. Although corals are known to harbour bacteria that can catabolise DMSP, the recent discovery of bacteria capable of producing DMSP in coastal and deep-sea environments raises the possibility of a bacterial contribution to the DMSP output of corals. Here, 157 bacteria associated with four common coral species were isolated and screened for their ability to produce DMSP by targeting dsyB, a key gene involved in DMSP biosynthesis. Approximately 9% (14 out of 157) of the bacterial isolates harboured dsyB, all being members of the Alphaproteobacteria. The ability of these isolates to produce DMSP was confirmed by liquid chromatography-mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR) measurements. A dsyB-harbouring strain, Shimia aestuarii AMM-P-2, was selected for genome sequencing. This strain harbours the complete genetic machinery to (i) assimilate sulfate and synthesise the DMSP precursors, cysteine and methionine; (ii) demethylate DMSP and generate methanethiol; (iii) cleave DMSP, generating dimethyl sulfide (DMS) and acrylate; and (iv) utilise or detoxify acrylate. The impacts of varied environmental factors (temperature, salinity, light and UV radiation) on S. aestuarii AMM-P-2 DMSP biosynthesis were characterised. DMSP levels in S. aestuarii AMM-P-2 increased almost two-fold under both hypersaline conditions (40 PSU) and high UV exposure. DMSP catabolism through the cleavage pathway also increased under these conditions, producing the antioxidants DMS and acrylate, a potential response to the oxidative stress generated. Overall, our results reveal that coral-associated bacteria can synthesize DMSP and may therefore contribute to DMSP production by the coral holobiont.

Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton

Ecological interactions between marine bacteria and phytoplankton play a pivotal role in governing the ocean’s major biogeochemical cycles. Among these, members of the marine Roseobacter Group (MRG) can establish mutualistic relationships with phytoplankton that are, in part, maintained by exchanges of the organosulfur compound, dimethylsulfoniopropionate (DMSP). Yet most of what is known about these interactions has been derived from culture-based laboratory studies. To investigate temporal and spatial co-occurrence patterns between members of the MRG and DMSP-producing phytoplankton we analysed 16S and 18S rRNA gene amplicon sequence variants (ASVs) derived from 5 years of monthly samples from seven environmentally distinct Australian oceanographic time-series. The MRG and DMSP-producer communities often displayed contemporaneous seasonality, which was greater in subtropical and temperate environments compared to tropical environments. The relative abundance of both groups varied latitudinally, displaying a poleward increase, peaking (MRG at 33% of total bacteria, DMSP producers at 42% of eukaryotic phototrophs) during recurrent spring-summer phytoplankton blooms in the most temperate site (Maria Island, Tasmania). Network analysis identified 20,140 significant positive correlations between MRG ASVs and DMSP producers and revealed that MRGs exhibit significantly stronger correlations to high DMSP producers relative to other DMSP-degrading bacteria (Pelagibacter, SAR86 and Actinobacteria). By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound.

Responses of Biogenic Sulfur Compound Concentrations to Dust Aerosol Enrichment and Ocean Acidification in the Western Pacific Ocean

AbstractDeck incubation experiments were conducted to investigate how the addition of atmospheric dust aerosols and ocean acidification (OA) affects phytoplankton growth and the production of dimethylsulfide (DMS), its precursor dimethylsulfoniopropionate (DMSP), and dimethylsulfoxide (DMSO) in the oligotrophic western Pacific Ocean. The incubation experiment showed that the deposition of simulated dust aerosols greatly influenced phytoplankton growth and the release of biogenic sulfur compounds (BSCs). Furthermore, it altered the N:P ratios in seawater and phytoplankton community composition, elevating the proportions of strong DMSP and DMSO producers (mainly haptophytes). The average Chl‐a and DMS/P/O concentrations in the acidified treatment (pH 7.9) were 86.76%, 82.53%, 84.17%, and 231.06% higher than in the control. The results indicated that lower pH promoted the growth of diatoms and to a certain extent, the release of the three BSCs.

Growth, DMS and DMSP production in Emiliania huxleyi under elevated CO2 and UV radiation

The effects of ocean acidification and solar radiation on marine organisms have received increasing attention. Coccolithophores are a major producer of dimethylsulfoniopropionate (DMSP), which is a precursor of dimethylsulfide (DMS), a volatile biogenic active gas related to climate. Here, we investigated the individual and combined effects of elevated CO2 and ultraviolet radiation (UVR) on growth, DMS, and DMSP production of Emiliania huxleyi. Elevated CO2 (1000 μatm, HC) decreased the cell concentration, DMS, and particulate DMSP (DMSPp) concentrations by 17%, 20%, and 13%, respectively, compared with ambient CO2 (400 μatm, LC) in the semi-continuous culture. The addition of UVA to photosynthetically active radiation (PAR) increased cell concentration of E. huxleyi by 16% on day 4, which may be due to the photorepair effects induced by UVA, and the effect was time-dependent. PAR + UVA and PAR + UVA + UVB exposure decreased cellular DMS by 25%–56%, and increased cellular DMSPp by 60%–130% compared with PAR on days 3–4. Cellular DMSPp followed the order: PAR + UVA > PAR + UVA + UVB > PAR, and HC had no significant effects on cellular DMSPp compared with LC in the combined experiment. These results aid our understanding of the effects of ocean acidification and UV radiation on the production of methyl sulfur compounds in the ocean.

Spatiotemporal distribution of bacterial dimethylsulfoniopropionate producing and catabolic genes in the Changjiang Estuary.

The osmolyte dimethylsulfoniopropionate (DMSP) is produced in petagram amounts by marine microorganisms. Estuaries provide natural gradients in salinity and nutrients, factors known to regulate DMSP production; yet there have been no molecular studies of DMSP production and cycling across these gradients. Here, we study the abundance, distribution and transcription of key DMSP synthesis (e.g. dsyB and mmtN) and catabolic (e.g. dddP and dmdA) genes along the salinity gradient of the Changjiang Estuary. DMSP levels did not correlate with Chl a across the salinity gradient. In contrast, DMSP concentration, abundance of bacterial DMSP producers and their dsyB and mmtN transcripts were lowest in the freshwater samples and increased abruptly with salinity in the transitional and seawater samples. Metagenomics analysis suggests bacterial DMSP-producers were more abundant than their algal equivalents and were more prominent in summer than winter samples. Bacterial DMSP catabolic genes and their transcripts followed the same trend of being greatly enhanced in transitional and seawater samples with higher DMSP levels than freshwater samples. DMSP cleavage was likely the dominant catabolic pathway, with DMSP lyase genes being ~4.3-fold more abundant than the demethylase gene dmdA. This is an exemplar study for future research on microbial DMSP cycling in estuary environments.

Dimethylsulfoniopropionate Biosynthetic Bacteria in the Subseafloor Sediments of the South China Sea.

Dimethylsulfoniopropionate (DMSP) is one of Earth’s most abundant organosulfur molecules, and bacteria in marine sediments have been considered significant producers. However, the vertical profiles of DMSP content and DMSP-producing bacteria in subseafloor sediment have not been described. Here, we used culture-dependent and -independent methods to investigate microbial DMSP production and cycling potential in South China Sea (SCS) sediment. The DMSP content of SCS sediment decreased from 11.25 to 20.90 nmol g–1 in the surface to 0.56–2.08 nmol g–1 in the bottom layers of 8-m-deep subseafloor sediment cores (n = 10). Very few eukaryotic plastid sequences were detected in the sediment, supporting bacteria and not algae as important sediment DMSP producers. Known bacterial DMSP biosynthesis genes (dsyB and mmtN) were only predicted to be in 0.0007–0.0195% of sediment bacteria, but novel DMSP-producing isolates with potentially unknown DMSP synthesis genes and/or pathways were identified in these sediments, including Marinobacter (Gammaproteobacteria) and Erythrobacter (Alphaproteobacteria) sp. The abundance of bacteria with the potential to produce DMSP decreased with sediment depth and was extremely low at 690 cm. Furthermore, distinct DMSP-producing bacterial groups existed in surface and subseafloor sediment samples, and their abundance increased when samples were incubated under conditions known to enrich for DMSP-producing bacteria. Bacterial DMSP catabolic genes were also most abundant in the surface oxic sediments with high DMSP concentrations. This study extends the current knowledge of bacterial DMSP biosynthesis in marine sediments and implies that DMSP biosynthesis is not only confined to the surface oxic sediment zones. It highlights the importance of future work to uncover the DMSP biosynthesis genes/pathways in novel DMSP-producing bacteria.