Dimethylsulfoniopropionate Lyase Research Articles

An S-methyltransferase that produces the climate-active gas dimethylsulfide is widespread across diverse marine bacteria.

Hydrogen sulfide (H2S), methanethiol (MeSH) and dimethylsulfide (DMS) are abundant sulfur gases with roles in biogeochemical cycling, chemotaxis and/or climate regulation. Catabolism of the marine osmolyte dimethylsulfoniopropionate (DMSP) is a major source of DMS and MeSH, but both also result from S-methylation of H2S via MddA, an H2S and MeSH S-methyltransferase whose gene is abundant in soil but scarce in marine environments. Here we identify the S-adenosine methionine (SAM)-dependent MeSH and H2S S-methyltransferase 'MddH', which is widespread in diverse marine bacteria and some freshwater and soil bacteria. mddH is predicted in up to ~5% and ~15% of seawater and coastal sediment bacteria, respectively, which is considerably higher than mddA. Furthermore, marine mddH transcript levels are similar to those for the most abundant DMSP lyase gene dddP. This study implies that the importance of H2S and MeSH S-methylation pathways in marine environments is significantly underestimated.

Novel insights into dimethylsulfoniopropionate cleavage by deep subseafloor fungi

Dimethylsulfoniopropionate (DMSP), a key organic sulfur compound in marine and subseafloor sediments, is degraded by phytoplankton and bacteria, resulting in the release of the climate-active volatile gas dimethylsulfide (DMS). However, it remains unclear if dominant eukaryotic fungi in subseafloor sediments possess specific abilities and metabolic mechanisms for DMSP degradation and DMS formation. Our study provides the first evidence that fungi from coal-bearing sediments ∼2 km below the seafloor, such as Aspergillus spp., Chaetomium globosum, Cladosporium sphaerospermum, and Penicillium funiculosum, can degrade DMSP and produce DMS. In Aspergillus sydowii 29R-4-F02, which exhibited the highest DMSP-dependent DMS production rate (16.95 pmol/μg protein/min), two DMSP lyase genes, dddP and dddW, were identified. Remarkably, the dddW gene, previously observed only in bacteria, was found to be crucial for fungal DMSP cleavage. These findings not only extend the list of fungi capable of degrading DMSP, but also enhance our understanding of DMSP lyase diversity and the role of fungi in DMSP decomposition in subseafloor sedimentary ecosystems.

Effects of nanoplastics exposure on ingestion, life history traits, and dimethyl sulfide production in rotifer Brachionus plicatilis

Microplastics (MPs) and nanoplastics (NPs) have gained global concern due to their detrimental effects on marine organisms. We investigated the effects of 80 nm polystyrene (PS) NPs on life history traits, ingestion, and dimethyl sulfide (DMS) and dimethylsulfoniopropionate (DMSP) production in the rotifer Brachionus plicatilis. Fluorescently labeled 80 nm PS NPs were ingested by the rotifer B. plicatilis and accumulated in the digestive tract. The lethal rates of B. plicatilis exposed to NPs were dose-dependent. High concentrations of PS NPs exposure had negative effects on developmental duration, leading to prolonged embryonic development and pre-reproductive periods, shortened reproductive period, post-reproductive period, and lifespan in B. plicatilis. High concentrations of PS NPs exposure inhibited life table demographic parameters such as age-specific survivorship and fecundity, generation time, net reproductive rate, and life expectancy. Consequently, the population of B. plicatilis was adversely impacted. Furthermore, exposure to PS NPs resulted in a reduced ingestion rate in B. plicatilis, as well as a decreased in DMS, particulate DMSP (DMSPp) concentration, and DMSP lyase activity (DLA), which exhibited a dose-response relationship. B. plicatilis grazing promoted DLA and therefore increased DMS production. PS NPs exposure caused a decline in the increased DMS induced by rotifer grazing. Our results help to understand the ecotoxicity of NPs on rotifer and their impact on the biogeochemical cycle of dimethylated sulfur compounds.

DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms

Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with roles in oxidative stress protection, global carbon and sulfur cycling and, as shown here, potentially in osmotolerance. Microbial DMSOP cleavage yields dimethyl sulfoxide, a ubiquitous marine metabolite, and acrylate, but the enzymes responsible, and their environmental importance, were unknown. Here we report DMSOP cleavage mechanisms in diverse heterotrophic bacteria, fungi and phototrophic algae not previously known to have this activity, and highlight the unappreciated importance of this process in marine sediment environments. These diverse organisms, including Roseobacter, SAR11 bacteria and Emiliania huxleyi, utilized their dimethylsulfoniopropionate lyase ‘Ddd’ or ‘Alma’ enzymes to cleave DMSOP via similar catalytic mechanisms to those for dimethylsulfoniopropionate. Given the annual teragram predictions for DMSOP production and its prevalence in marine sediments, our results highlight that DMSOP cleavage is likely a globally significant process influencing carbon and sulfur fluxes and ecological interactions.

SAR92 clade bacteria are potentially important DMSP degraders and sources of climate-active gases in marine environments.

Catabolism of dimethylsulfoniopropionate (DMSP) by marine bacteria has important impacts on the global sulfur cycle and climate. However, whether and how members of most oligotrophic bacterial groups participate in DMSP metabolism in marine environments remains largely unknown. In this study, by characterizing culturable strains, we have revealed that bacteria of the SAR92 clade, an abundant oligotrophic group of Gammaproteobacteria in coastal seawater, can catabolize DMSP through the DMSP lyase DddD-mediated cleavage pathway and/or the DMSP demethylase DmdA-mediated demethylation pathway to produce climate-active gases dimethylsulfide and methanethiol. Additionally, we found that SAR92 clade bacteria capable of catabolizing DMSP are widely distributed in global oceans. These results indicate that SAR92 clade bacteria are potentially important DMSP degraders and sources of climate-active gases in marine environments that have been overlooked, contributing to a better understanding of the roles and mechanisms of the oligotrophic bacteria in oceanic DMSP degradation.

Genomic potential for inorganic carbon sequestration and xenobiotic degradation in marine bacterium Youngimonas vesicularis CC-AMW-ET affiliated to family Paracoccaceae.

Ecological studies on marine microbial communities largely focus on fundamental biogeochemical processes or the most abundant constituents, while minor biological fractions are frequently neglected. Youngimonas vesicularis CC-AMW-ET, isolated from coastal surface seawater in Taiwan, is an under-represented marine Paracoccaceae (earlier Rhodobacteraceae) member. The CC-AMW-ET genome was sequenced to gain deeper insights into its role in marine carbon and sulfur cycles. The draft genome (3.7Mb) contained 63.6% GC, 3773 coding sequences and 51 RNAs, and displayed maximum relatedness (79.06%) to Thalassobius litoralis KU5D5T, a Roseobacteraceae member. While phototrophic genes were absent, genes encoding two distinct subunits of carbon monoxide dehydrogenases (CoxL, BMS/Form II and a novel form III; CoxM and CoxS), and proteins involved in HCO3- uptake and interconversion, and anaplerotic HCO3- fixation were found. In addition, a gene coding for ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO, form II), which fixes atmospheric CO2 was found in CC-AMW-ET. Genes for complete assimilatory sulfate reduction, sulfide oxidation (sulfide:quinone oxidoreductase, SqrA type) and dimethylsulfoniopropionate (DMSP) cleavage (DMSP lyase, DddL) were also identified. Furthermore, genes that degrade aromatic hydrocarbons such as quinate, salicylate, salicylate ester, p-hydroxybenzoate, catechol, gentisate, homogentisate, protocatechuate, 4-hydroxyphenylacetic acid, N-heterocyclic aromatic compounds and aromatic amines were present. Thus, Youngimonas vesicularis CC-AMW-ET is a potential chemolithoautotroph equipped with genetic machinery for the metabolism of aromatics, and predicted to play crucial roles in the biogeochemical cycling of marine carbon and sulfur.

Acrylic acid and DMSP lyases in the green algae Ulva

Green macroalgae of the genus Ulva contain dimethylsulfoniopropionate (DMSP) produced from methionine through a transamination pathway. DMSP is converted by DMSP lyase enzymes (DLs) into acrylic acid (AA), a high-value compound with a vast market as its esters have applications in the production of plastic additives, textiles, sealants, adhesives and surface coatings. The levels of AA produced by Ulva species, and the processes to extract it from this biomass, are currently poorly understood. In this study an analytical method was implemented for the simultaneous measurement of AA, DMSP and the pathway intermediates (4-methylthio-2-oxobutyrate, 4-methylthio-2-hydroxybutyrate, and 4-dimethylsulfonio-2-hydroxybutyrate) in Ulva biomass. The amounts of these compounds – with a focus on AA – were then quantified after processing the macroalgae with different chemical, thermal, and enzymatic treatments. AA was extracted in the range of 0.22–0.45 % of the algal dry weight. Sequential enzyme treatments showed no higher yields compared to individual enzymatic treatments or chemico-physical extractions, an encouraging result for the application of the treatments in industry. Codon-optimised synthetic genes for two candidate DLs from Ulva mutabilis were expressed and purified in E. coli with solubility tags, and the biochemical characteristics of these recombinant lyases were investigated. Both enzymes UM021_MBP and UM030_Halo7 had lower activity than their microalgal counterpart Alma1, with whom they share 33.9 % and 39.7 % similarity at amino acid level respectively. UM030_Halo7 appeared more active than UM021_MBP, with Km and Vm of 7.10 mM and 5.99 mM/min/mg protein respectively. UM030_Halo7 showed a preferred pH of 6.0, an optimal of temperature of 20 °C, was inhibited by NaCl concentration equal or higher than 0.5 M but not by H2O2 up to 50 μM. These results advance our understanding of AA biosynthesis in Ulva at the molecular level, and could be useful to implement processes for extracting AA from Ulva species within a biorefinery framework.

The Effect of Zooplankton on the Distributions of Dimethyl Sulfide and Dimethylsulfoniopropionate in the Bohai and Yellow Seas

AbstractDimethyl sulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) are ubiquitous sulfur compounds in the ocean. DMS is emitted into the atmosphere and has potential climatic effects. The distributions of DMS and DMSP are affected by various biological factors (i.e., bacterial catabolism and phytoplankton and zooplankton community composition). The horizontal and vertical distributions of DMSP, DMSP lyase activity (DLA), DMS, and the abundances of bacteria, DMSP‐consuming bacteria, dimethyl sulfoxide‐consuming bacteria, and picophytoplankton were investigated in the Bohai Sea (BS) and Yellow Sea (YS) during autumn 2020. DLA was significantly correlated with chlorophyll a, DMS, and dissolved DMSP concentrations. Our data show that bacteria Clade_I SAR11 was a significant contributor to DLA. A dilution experiment indicated that the highest microzooplankton grazing rate coincided with the highest DMS concentration and DMS production rate. A proportion of 16%–62% of the DMSPt was converted to DMS in the dilution experiment. Copepods dominated the mesozooplankton community. Calanus sinicus was the predominant copepod in the BS and YS. C. sinicus grazing stimulated DMS production. DMS concentration increased 299% after C. sinicus grazing on physically broken algal cells for 48 hr. These results will help with a better understanding of the control of DMS and DMSP concentrations by zooplankton and the DMS release mechanisms that occur through zooplankton grazing.

Observational evidence linking ocean sulfur compounds to atmospheric dimethyl sulfide during Icelandic Sea phytoplankton blooms

In two Icelandic Sea spring blooms (May 2018 and 2019) in the North Atlantic Ocean (62.9–68.0°N, 9.0–28.0°W), chlorophyll-a and dimethylsulfoniopropionate (DMSP) concentrations and DMSP lyase activity (the DMSP-to-dimethyl sulfide (DMS) conversion efficiency) were measured at 67 stations, and the hourly atmospheric DMS mixing ratios were concurrently measured only in May 2019 at Storhofdi on Heimaey Island, located south of Iceland (63.4°N, 20.3°W). The ocean parameters for biology (i.e., chlorophyll-a, DMSP, and DMSP lyase activity) were broadly associated in distribution; however, the statistical significance of the association differed among four ocean domains and also between 2018 and 2019. Specifically, the widespread dominance of Phaeocystis, coccolithophores, and dinoflagellates (all rich in DMSP and high in DMSP lyase activity) across the study area is a compelling indication that variations in DMSP-rich phytoplankton were likely a main cause of the variations in statistical significance. For all the ocean domains defined here, we found that the DMS production capacity (calculated using the exposures of air masses to ocean biology prior to their arrivals at Heimaey and the atmospheric DMS mixing ratios of those air masses at Heimaey) was surprisingly consistent with in situ ocean S data (i.e., DMSP and DMSP lyase activity). Our study shows that the proposed computational approach enabled the detection of changes in DMS production and emission in association with changes in ocean primary producers.

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.

A new dimethylsulfoniopropionate lyase of the cupin superfamily in marine bacteria.

Dimethylsulfoniopropionate (DMSP) is a marine organosulfur compound with important roles in stress protection, marine biogeochemical cycling, chemical signalling and atmospheric chemistry. Diverse marine microorganisms catabolize DMSP via DMSP lyases to generate the climate-cooling gas and info-chemical dimethyl sulphide. Abundant marine heterotrophs of the Roseobacter group (MRG) are well known for their ability to catabolize DMSP via diverse DMSP lyases. Here, a new DMSP lyase DddU within the MRG strain Amylibacter cionae H-12 and other related bacteria was identified. DddU is a cupin superfamily DMSP lyase like DddL, DddQ, DddW, DddK and DddY, but shares <15% amino acid sequence identity with these enzymes. Moreover, DddU proteins forms a distinct clade from these other cupin-containing DMSP lyases. Structural prediction and mutational analyses suggested that a conserved tyrosine residue is the key catalytic amino acid residue in DddU. Bioinformatic analysis indicated that the dddU gene, mainly from Alphaproteobacteria, is widely distributed in the Atlantic, Pacific, Indian and polar oceans. For reference, dddU is less abundant than dddP, dddQ and dddK, but much more frequent than dddW, dddY and dddL in marine environments. This study broadens our knowledge on the diversity of DMSP lyases, and enhances our understanding of marine DMSP biotransformation.

Discovery of dimethylsulfoxonium propionate lyases - a missing enzyme relevant to the global sulfur cycle.

Six dimethylsulfoniopropionate (DMSP) lyases have been shown to cleave the marine sulfur metabolite dimethylsulfoxonium propionate (DMSOP) into DMSO and acrylate. This discovery characterises a missing enzyme relevant to the global sulfur cycle.

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.

Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater

BackgroundUbiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently difficult to discern which microbes actively catabolise DMSP in the environment, why they do so and the pathways used.ResultsHere, a novel DNA-stable isotope probing (SIP) approach, where only the propionate and not the DMS moiety of DMSP was 13C-labelled, was strategically applied to identify key microorganisms actively using DMSP and also likely DMS as a carbon source, and their catabolic enzymes, in North Sea water. Metagenomic analysis of natural seawater suggested that Rhodobacterales (Roseobacter group) and SAR11 bacteria were the major microorganisms degrading DMSP via demethylation and, to a lesser extent, DddP-driven DMSP lysis pathways. However, neither Rhodobacterales and SAR11 bacteria nor their DMSP catabolic genes were prominently labelled in DNA-SIP experiments, suggesting they use DMSP as a sulfur source and/or in signalling pathways, and not primarily for carbon requirements. Instead, DNA-SIP identified gammaproteobacterial Oceanospirillales, e.g. Amphritea, and their DMSP lyase DddD as the dominant microorganisms/enzymes using DMSP as a carbon source. Supporting this, most gammaproteobacterial (with DddD) but few alphaproteobacterial seawater isolates grew on DMSP as sole carbon source and produced DMS. Furthermore, our DNA-SIP strategy also identified Methylophaga and other Piscirickettsiaceae as key bacteria likely using the DMS, generated from DMSP lysis, as a carbon source.ConclusionsThis is the first study to use DNA-SIP with 13C-labelled DMSP and, in a novel way, it identifies the dominant microbes utilising DMSP and DMS as carbon sources. It highlights that whilst metagenomic analyses of marine environments can predict microorganisms/genes that degrade DMSP and DMS based on their abundance, it cannot disentangle those using these important organosulfur compounds for their carbon requirements. Note, the most abundant DMSP degraders, e.g. Rhodobacterales with DmdA, are not always the key microorganisms using DMSP for carbon and releasing DMS, which in this coastal system were Oceanospirillales containing DddD.98tW24pEex88JAHxuSH5r1Video abstract.

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.

Recent insights into oceanic dimethylsulfoniopropionate biosynthesis and catabolism.

Dimethylsulfoniopropionate (DMSP), a globally important organosulfur compound is produced in prodigious amounts (2.0Pg sulfur) annually in the marine environment by phytoplankton, macroalgae, heterotrophic bacteria, some corals and certain higher plants. It is an important marine osmolyte and a major precursor molecule for the production of climate-active volatile gas dimethyl sulfide (DMS). DMSP synthesis take place via three pathways: a transamination 'pathway-' in some marine bacteria and algae, a Met-methylation 'pathway-' in angiosperms and bacteria and a decarboxylation 'pathway-' in the dinoflagellate, Crypthecodinium. The enzymes DSYB and TpMMT are involved in the DMSP biosynthesis in eukaryotes while marine heterotrophic bacteria engage key enzymes such as DsyB and MmtN. Several marine bacterial communities import DMSP and degrade it via cleavage or demethylation pathways or oxidation pathway, thereby generating DMS, methanethiol, and dimethylsulfoxonium propionate, respectively. DMSP is cleaved through diverse DMSP lyase enzymes in bacteria and via Alma1 enzyme in phytoplankton. The demethylation pathway involves four different enzymes, namely DmdA, DmdB, DmdC and DmdD/AcuH. However, enzymes involved in the oxidation pathway have not been yet identified. We reviewed the recent advances on the synthesis and catabolism of DMSP and enzymes that are involved in these processes.

Abundance and Diversity of Dimethylsulfoniopropionate Degradation Genes of Roseobacter Group in the Northern South China Sea

Bacterial degradation of dimethylsulfoniopropionate (DMSP) plays a significant role in ecosystem productivity and global climate. In this study, the abundance and diversity of Roseobacter group DMSP degradation genes were explored in spatial scale of the South China Sea (SCS). Quantitative PCR showed that a higher abundance of dmdA (DMSP demethylase) and dddP (DMSP lyase) genes was detected above 75 m than deep water, especially in surface water. A high ratio of dmdA/dddP existed in all sites and increased with water depth, indicating that demethylation was the main degradation pathway in the Roseobacter group. High-throughput sequencing analysis showed that distribution of dmdA gene had a significant layering structure in the northern SCS, and high taxonomic diversity of dmdA gene was observed in near-surface waters (25 and 50 m). DmdA gene in the Roseobacter group, such as Leisingera, Nioella, Roseobacter, Roseovarius, Donghicola, Phaeobacter, and Tateyamaria, had remarkable specificity due to the effect of different sites and water depths. Different ecological strategies of DMSP degradation may be used by members of the bacterial community harboring demethylation genes. In addition, many dmdA sequences were affiliated with unidentified bacteria, indicating that the SCS reserved high diversity of DMSP-degrading bacteria. Canonical correspondence analysis (CCA) suggested that temperature and depth were the most important factors to determine the taxonomic distribution of DMSP degradation genes in the Roseobacter group, as well as their abundance. This study highlighted the understanding of the role of Roseobacter group in DMSP degradation in the tropical ocean.

Reaction mechanism of the PuDddK dimethylsulfoniopropionate lyase and cofactor effects of various transition metal ions.

The microbial cleavage of dimethylsulfoniopropionate (DMSP) produces volatile dimethyl sulfide (DMS) via the lyase pathway, playing a crucial role in the global sulfur cycle. Herein, the DMSP decomposition catalyzed by PuDddK (a DMSP lyase) devised with various transition metal ion cofactors are investigated using density functional calculations. The PuDddK reaction has been demonstrated to employ a concerted β-elimination mechanism, where the substrate α-proton abstraction by the deprotonated Tyr64 occurs simultaneously with the Cβ-S bond cleavage and Cα = Cβ double bond formation. The PuDddK enzymes with diverse divalent metal ions (Ni2+, Mn2+, Fe2+, Co2+, Zn2+, and Cu2+) incorporated prefer DMSP as a monodentate ligand. The cases of Ni2+, Mn2+, Fe2+, Co2+, and Zn2+ with the same 3His-1Glu ligands have close reaction energy barriers, indicating that the lyase activity may be hardly affected by the divalent transition metal type with the same ligand type and number. The coordination loss of one histidine in Cu2+, forming a 2His-1Glu architecture, leads to a lower activity, revealing that the 3His-1Glu ligand set used by DddK appears to be a scaffold capable of more efficiently catalyzing the DMSP decomposition. Further analysis reveals that the inactivation of Fe3+-dependent PuDddK is derived from an electron transfer from the Tyr64 phenolate to Fe3+, with the implication that the PuDddK activity may be primarily affected by the redox effects induced by a strongly oxidizing transition metal ion (like Fe3+).

Distribution and Dimethylsulfoniopropionate Degradation of Dimethylsulfoniopropionate‐Consuming Bacteria in the Yellow Sea and East China Sea

AbstractThe fate of dimethylsulfoniopropionate (DMSP), the precursor of the climatologically important gas dimethylsulfide (DMS), depends on the structure of marine communities. DMSP degradation by DMSP‐consuming bacteria (DCB) is an important sink of dissolved DMSP (DMSPd) in seawater. DMSP cleavage and demethylation are two DMSPd consumption pathways, and the DMSPd cleavage pathway involves DMSP lyase activity (DLA). Here, we studied the distribution of DMS, DMSP, DCB, and DLA in the seawater of the Yellow Sea and East China Sea in the summer of 2013 and the degradation of DMSPd by DCB. High DCB abundances, as well as DMS and dissolved, particulate, total DMSP (DMSPd,p,t) concentrations were observed near the Hongzhou Bay, which may be due to the high productivity of dinoflagellates. The spatial distribution of DCB abundance was most likely the result of the regional hydrography including upwelling near Hangzhou Bay and the discharge of Yangtze Diluted Water (YDW). The DLA along the YDW decreased from coastal water to open sea. The DMSPd consumption by DCB Bacillus sp. YES023 isolated from the seawater was accompanied by DMS production (≤8.2% of DMSPd consumption). Bacillus sp. YES023 could also grow using glycine betaine, acrylic acid, dimethylsulfoxide, monomethylamine, or dimethylamine as a sole carbon source. Glycine betaine and acrylic acid were the most favorable substrates for overall growth. These results help our understanding of bacterial catabolism and the degradation pathways of methyl sulfur compounds in the ocean.

Dimethyl sulfide mediates microbial predator-prey interactions between zooplankton and algae in the ocean.

Phytoplankton are key components of the oceanic carbon and sulfur cycles1. During bloom events, some species can emit large amounts of the organosulfur volatile dimethyl sulfide (DMS) into the ocean and consequently the atmosphere, where it can modulate aerosol formation and affect climate2,3. In aquatic environments, DMS plays an important role as a chemical signal mediating diverse trophic interactions. Yet, its role in microbial predator-prey interactions remains elusive with contradicting evidence for its role in either algal chemical defence or in the chemo-attraction of grazers to prey cells4,5. Here we investigated the signalling role of DMS during zooplankton-algae interactions by genetic and biochemical manipulation of the algal DMS-generating enzyme dimethylsulfoniopropionate lyase (DL) in the bloom-forming alga Emiliania huxleyi6. We inhibited DL activity in E. huxleyi cells in vivo using the selective DL-inhibitor 2-bromo-3-(dimethylsulfonio)-propionate7 and overexpressed the DL-encoding gene in the model diatom Thalassiosira pseudonana. We showed that algal DL activity did not serve as an anti-grazing chemical defence but paradoxically enhanced predation by the grazer Oxyrrhis marina and other microzooplankton and mesozooplankton, including ciliates and copepods. Consumption of algal prey with induced DL activity also promoted O. marina growth. Overall, our results demonstrate that DMS-mediated grazing may be ecologically important and prevalent during prey-predator dynamics in aquatic ecosystems. The role of algal DMS revealed here, acting as an eat-me signal for grazers, raises fundamental questions regarding the retention of its biosynthetic enzyme through the evolution of dominant bloom-forming phytoplankton in the ocean.