Earth's coolest organosulfur molecule: understanding how agriculture can be more cooling to the climate

Billions of tonnes of the organosulfur compound dimethylsulfoniopropionate (DMSP) are made each year by marine algae, corals and bacteria, but plants also make this important molecule, including crops such as maize and tomato. DMSP is key in global sulfur cycling, as it is the main precursor of the climate-active gas dimethylsulfide (DMS). In marine settings, DMS gives the seaside its distinctive smell and is used by many animals and birds as a chemoattractant associated with their algal food. DMS is oxidised in the atmosphere to sulfates that accelerate cloud formation. These clouds affect the amount of sunlight reaching the Earth's surface and this in turn affects the climate by causing a local cooling effect. Sulfur is returned to land in the form of rain, completing the cycle.

Production of DMSP and DMS is traditionally associated with marine environments and the coast. For example, saltmarshes are hotspots of DMSP/DMS synthesis and contribute up to 10% of global DMS emissions. However, new data (including our own) suggest that significant DMSP/DMS production also occurs in agricultural systems. We have recently identified many different crops that produce DMSP. DMSP production likely protects these crop from environmental stresses, such as salinity and nutrient limitations, but this has not been established. We have also found that crop rhizospheres contain more DMSP than is typically found in seawater and that they emit DMS. Moreover, we have isolated crop-associated bacteria that convert DMSP into DMS and promote plant growth. In this project, we will evaluate the importance of DMSP/DMS production in agriculture and assess whether harnessing or manipulating these processes can improve agricultural productivity, boost crop and climate-cooling DMS yields.

We will study the agricultural production and turnover rates of DMSP and DMS by different crops growing in field sites over a season. By building and deploying remote DMS field sensors, we will track DMS production in real-time from crops, giving us high-resolution data on DMS release into the atmosphere from agriculture to inform models. We will also assess the abundance, diversity and potential importance of crop-interacting microbes that degrade plant-made DMSP to release DMS. Together, this will establish whether specific developmental triggers and environmental factors (e.g. agricultural practices, soil chemistry or crop physiology) cause more DMSP production and DMS release into the atmosphere as a direct result of agriculture. Since we are challenging the dogma that DMSP/DMS synthesis is solely a marine process, we will additionally reassess the global budgets for DMSP/DMS using mathematical modelling, so that DMSP/DMS production from agriculture and any potential climate cooling effects can be considered. This work will allow us to better understand and predict the significance of agricultural landscapes for the production of these influential compounds.

Overall, this work will allow us to understand how and why agriculture contributes to global DMSP and DMS production. This will allow us to predict better the impacts of DMSP and DMS on the natural environment, agri-food systems and climate. Harnessing the protective effects of DMSP production in plants and the beneficial traits of growth-promoting microbes may also allow us to improve crop growth and productivity under stressful conditions (e.g. drought and salinity linked to climate change), and enhance future food security and climate-cooling DMS production.

The compatible solute DMSP is key in stress protection and global C and S cycling, where it is the main precursor of the climate-active gas DMS. DMSP is commonly considered a marine molecule, but our recent data show that DMSP is also important in agriculture. We have identified several crops that produce DMSP, and diverse fungi and bacteria (and their DMSP lyase genes generate DMS from DMSP) in these crop rhizospheres. In this project, we will measure DMSP/DMS production in different crop plants, assaying DMSP levels by gas chromatography (GC) and liquid chromatography mass spectrometry. To analyse DMS levels, we will use GC and gas-tight chambers placed over plants, plus remote sensors to provide high-resolution data on DMS flux from fields over a growing season. We will also measure DMSP/DMS levels from different field sites to determine how soil chemistry and agricultural practices (e.g. tillage regime) affect production. We will generate gene probes to terrestrial DMSP/DMS cycling genes and a DMSP-SmartChip, and use qPCR, RT-qPCR and gene amplicon sequencing to determine their gene abundance, diversity, expression and, thus, the potential importance of crop-associated microbial DMS production. We will formulate agricultural budgets for DMSP/DMS production and estimate the impacts of atmospheric DMS release on climate using mathematical models. We will also create transgenic plants over-expressing DMSP synthesis genes and use plant growth-promoting microbial inoculants containing DMSP degraders (DMS producers) to assess whether manipulating DMSP/DMS production can enhance crop stress tolerance, crop yields and DMS production. Thus, we will determine if modifying DMSP/DMS production in agricultural settings has beneficial effects on our climate.

Overall, the project will provide fundamental insights into DMSP/DMS production in agriculture, opening up important new avenues to explore the biological significance of these molecules in agricultural landscapes.