DiMethylsulfonioPropionate cycling In Terrestrial environments (DMSP InTerrest)

Marine-dwelling microbes and plants produce 8 billion tonnes of dimethylsulfoniopropionate (DMSP) per year in Earth's surface oceans alone, via enzymes we have identified. Organisms produce DMSP to protect against salinity, cold, turgor pressure, oxidative and drought stresses, and predation. DMSP released into the environment is also widely taken up by microbes for these anti-stress properties, and used as a key nutrient via distinct degradation pathways. DMSP has critically important roles in global sulfur and carbon cycling, signalling, and as a major source of climate-active gases (CAG) e.g. dimethylsulfide (DMS) and the foul-smelling gas methanethiol (MeSH). Each year millions of tonnes of DMS, the characteristic smell of the seaside and a potent foraging cue guiding diverse organisms (gulls, seals, zooplankton, etc) to food, is released from DMSP via microbial DMSP lyase enzymes that we also identified. Some DMS is released and oxidised to form aerosols and cloud condensation nuclei in the atmosphere, which reduce the global radiation budget and 'cool' local climate. Critically, these sulfate aerosols return to land in rain - the primary transfer of biogenic sulfur from the oceans to land. DMSP synthesis and degradation are thought to occur only in marine settings, so DMSP cycling in terrestrial environments has largely been unexplored.

We challenged this dogma by revealing that DMSP synthesis is widespread in the plant Kingdom, ranging from common plants like grass, to agriculturally-important crops like maize, cabbage and sugarcane. Furthermore, our preliminary work shows that DMSP levels surpassing those in seawater exist in soils in which these key agricultural and bioenergy crops grow. Our work shows such soils liberate significant quantities of DMS and MeSH - processes ignored in climate models. We have also isolated novel bacteria and fungi from maize and sugarcane soils that utilise DMSP as a carbon source and show inducible DMSP-dependent DMS or MeSH production. Critically, these bacteria lack known DMSP degradation genes in their genomes, and thus likely possess novel DMSP catabolic enzymes and/or pathways. We have therefore uncovered a potentially large and virtually unexplored research area with profound implications for biogeochemical cycling. Our findings urgently require detailed study to establish the importance and influence of terrestrial DMSP cycling on the climate.

We wish to answer the fundamentally important questions of how microbes associated to terrestrial plants degrade DMSP, and the ecological and global importance of the process, especially relating to CAG production. We will test the hypothesis that plant-made DMSP is a key nutrient for CAG-producing microbes. In an everyday context, are microbes degrading DMSP responsible for the rotten MeSH smell associated with cabbage fields, or the sweet DMS smell associated with sweetcorn? We will study microbial DMSP degradation and concomitant CAG production associated to plants known to produce low (maize) and high (sugarcane) levels of DMSP, which together cover >0.2 billion ha. Collaborations are in place to sample these plants, as are the model DMSP-producing bacteria we isolated to study microbial DMSP degradation mechanisms in terrestrial environments. Our major aims are to elucidate the enzymes, pathways, and mechanisms of DMSP degradation in terrestrial microbes and use this knowledge to define the magnitude of the process and factors regulating it. Furthermore, we will use cutting-edge microbial ecology, modelling and process work to answer fundamental ecological questions: what are the key microbes that degrade DMSP and emit CAG in terrestrial environments, and how do they influence the climate?

We see our proposal as addressing a major new challenge that will reveal the importance of DMSP in terrestrial environments, uncovering new and unexpected research fields with far-reaching implications for current and future climate models.