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

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

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

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

Bacteria are important dimethylsulfoniopropionate producers in coastal sediments

Dimethylsulfoniopropionate (DMSP) and its catabolite dimethyl sulfide (DMS) are key marine nutrients, with roles in global sulfur cycling, atmospheric chemistry, signalling and, potentially, climate regulation. DMSP production was previously thought to be an oxic and photic process, mainly confined to the surface oceans. However, here we show that DMSP concentrations and DMSP/DMS synthesis rates were higher in surface marine sediment from e.g., saltmarsh ponds, estuaries and the deep ocean than in the overlying seawater. A quarter of bacterial strains isolated from saltmarsh sediment produced DMSP (up to 73 mM), and previously unknown DMSP-producers were identified. Most DMSP-producing isolates contained dsyB, but some alphaproteobacteria, gammaproteobacteria and actinobacteria utilised a methionine methylation pathway independent of DsyB, previously only associated with higher plants. These bacteria contained a methionine methyltransferase ‘mmtN’ gene - a marker for bacterial DMSP synthesis via this pathway. DMSP-producing bacteria and their dsyB and/or mmtN transcripts were present in all tested seawater samples and Tara Oceans bacterioplankton datasets, but were far more abundant in marine surface sediment. Approximately 108 bacteria per gram of surface marine sediment are predicted to produce DMSP, and their contribution to this process should be included in future models of global DMSP production. We propose that coastal and marine sediments, which cover a large part of the Earth’s surface, are environments with high DMSP and DMS productivity, and that bacteria are important producers within them

Short-Lived Trace Gases in the Surface Ocean and the Atmosphere

The two-way exchange of trace gases between the ocean and the atmosphere is important for both the chemistry and physics of the atmosphere and the biogeochemistry of the oceans, including the global cycling of elements. Here we review these exchanges and their importance for a range of gases whose lifetimes are generally short compared to the main greenhouse gases and which are, in most cases, more reactive than them. Gases considered include sulphur and related compounds, organohalogens, non-methane hydrocarbons, ozone, ammonia and related compounds, hydrogen and carbon monoxide. Finally, we stress the interactivity of the system, the importance of process understanding for modeling, the need for more extensive field measurements and their better seasonal coverage, the importance of inter-calibration exercises and finally the need to show the importance of air-sea exchanges for global cycling and how the field fits into the broader context of Earth System Science

Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process

Dimethylsulphoniopropionate (DMSP) is one of the Earth’s most abundant organosulphur molecules, a signalling molecule, a key nutrient for marine microorganisms, and the major precursor for gaseous dimethyl sulphide (DMS). DMS, another infochemical in signalling pathways, is important in global sulphur cycling2, and affects the Earth’s albedo, and potentially climate, via sulphate aerosol and cloud condensation nuclei production. It was thought that only eukaryotes produce significant amounts of DMSP, but here we demonstrate that many marine heterotrophic bacteria also produce DMSP, likely using the same methionine (Met) transamination pathway as macroalgae and phytoplankton10. We identify the first DMSP synthesis gene in any organism, dsyB, which encodes the key methyltransferase enzyme of this pathway and is a reliable reporter for bacterial DMSP synthesis in marine alphaproteobacteria. DMSP production and dsyB transcription are upregulated by increased salinity, nitrogen limitation and lower temperatures in our model DMSP-producing bacterium Labrenzia aggregata LZB033. With significant numbers of dsyB homologues in marine metagenomes, we propose that bacteria likely make a significant contribution to oceanic DMSP production. Furthermore, since DMSP production is not solely associated with obligate phototrophs, the process need not be confined to the photic zones of marine environments, and as such may have been underestimate

Re-visiting the CLAW hypothesis

4 pagesOver the last twenty years, large and continued research efforts have been invested in deciphering whether oceanic plankton contribute to the regulation of climate by the production and release of cloud-seeding atmospheric sulfur. Our recent research using globally spread observations and satellite derived data suggest that biogenic sulfur from the oceans represents a major source of cloud forming aerosols over much of the pristine southern hemisphere oceans. These climate-cooling sulfur emissions respond positively to incoming solar radiation over seasonal cycles, but show a weak response to anthropogenic global warming foreseen for the current centuryPeer reviewe

Preferential uptake of NH4 + over NO3 2 - in marine ecosystem models: A simple and more consistent parameterization

Here we present and analyse the behaviour of four different parameterizations of the preferential uptake of NH4+ over NO32 -. The first three (Wroblewski-Fasham, Spitz, Hurtt and Armstrong) are commonly used in current marine ecosystem models. However, they show either formulational inconsistencies (e.g. Wroblewski-Fasham), unrealistic features (e.g. Spitz) or structural rigidity (e.g. Hurtt and Armstrong). We therefore suggest a newer parameterization by slightly modifying the Wroblewski-Fasham formulation that easily overcome these deficiencies and could be used in the next generation of marine ecosystem models