Bacteria make DMSP - how significant is this process?

Globally, a billion tons of the sulfur-containing molecule dimethylsulfoniopropionate (DMSP) is made each year. The common belief was that DMSP is only made by marine eukaryotes, including phytoplankton, seaweeds, a few plants and some corals, but our preliminary work shows that marine bacteria also make DMSP, and at levels similar to those reported for some phytoplankton. For the first time, we have shown that marine bacteria likely use DMSP as an osmoprotectant to buffer cells against the salinity of seawater. The research that we propose will redefine the field of DMSP production and its catabolism.

DMSP is the main precursor of the environmentally important gas dimethylsulfide (DMS). Microbial DMSP lysis generates ~300 million tons of DMS per annum. Much of this DMS is used by bacteria, but ~10 % is released from the seas into the air, giving the seaside its characteristic smell. Once in the atmosphere, chemical products arising from DMS oxidation aid cloud formation over the oceans, to an extent that affects sunlight reaching the Earth's surface, with effects on climate. In turn, these products are delivered back to Earth as rain, representing a key component of the global sulfur cycle. DMS is also a potent chemoattractant for many organisms including seabirds, crustaceans and marine mammals, which associate DMS with food.

Although previous studies have described the pathways for DMSP synthesis, remarkably NONE of the enzymes or corresponding genes have been identified in ANY DMSP-producing organism.

Our preliminary data:
1. show that some marine bacteria make DMSP via the same pathway used by phytoplankton.
2. identified the key gene in bacterial DMSP production "mmtB" - the first gene shown to be involved in DMSP synthesis in any organism.
3. show that our model marine bacterium Labrenzia likely makes DMSP as an osmoprotectant.
4. show that bacteria containing mmtB produce DMSP, and some also contain DMSP lyase genes whose products liberate DMS from DMSP.
5. show that the mmtB gene is abundant in marine environments.

Our project:
The mmtB gene encodes an enzyme that catalyses one of the four predicted steps in DMSP synthesis, but we do not know the identity the other three genes. To fully understand the process of DMSP synthesis in bacteria, we need to identify the missing synthesis genes so that we can study their regulation and enzymology. We will use complementary molecular genetic approaches to identify the unknown DMSP synthesis genes and, in the process, characterise the full complement of genes whose expression is affected by salinity in Labrenzia.
To understand how and why bacteria in the environment produce DMSP and DMS, we will study key model bacteria isolated from marine samples. These bacteria will be grown in microcosms under conditions similar to those of their natural habitat, and their environmental growth conditions will be varied whilst monitoring DMS and DMSP synthesis, at both the process and gene expression level. This will indicate whether environmental factors such as temperature, oxidative stress, etc., affect the production of DMSP and concomitantly the production of the climate-active gas DMS.

The importance of bacterial DMSP production in marine environments will be examined. We will sample selected marine environments and investigate the activity of bacterial DMSP synthesis compared to eukaryotic DMS/DMSP pathways. We will determine if the environmental factors that regulate DMS/DMSP production in our model bacteria have the same effect on natural microbial communities that are present in important marine environments. We will also use a powerful suite of microbial ecology techniques, combined with molecular genetic tools, to identify the microbes and key genes involved in producing DMSP via the MmtB enzyme in these environments. This work will help us in the future to model how changes in the environment impact on the balance of these climate processes.

Our unpublished studies show for the first time that marine bacteria can produce dimethylsulfoniopropionate (DMSP), and that these bacteria also lyse DMSP, generating the climate-cooling gas dimethyl sulfide (DMS). We have also identified the first gene involved in DMSP synthesis in any organism. This project is driven by the need to gain a mechanistic understanding of these microbial pathways, the biodiversity of microbes carrying out these processes and environmental stimuli that regulate DMS/DMSP production. Our work will provide essential data for future modelling of DMS emissions from marine environments. As summarised in Academic Beneficiaries, we feel that this work will be of great interest to a range of scientists including microbiologists, molecular ecologists, computational biologists, biological modellers and biochemists because of the microbial diversity data that we generate on important natural environments that are sensitive to environmental change. The extensive biodatabases and resources that we generate from the natural study sites will be invaluable and perfectly complement the existing microbiological knowledge of important ecosystems. The environments that we will study are not well-characterised in terms of their microbial diversity. Therefore, the metagenomic data and data on the distribution and diversity of genes involved in DMS/DMSP production that will be generated in the project will make a substantial contribution to environmental microbiology. The metabolic pathways we will study and identification of "new genes" will also provide context for the many unidentified genes that are present in microbial genomes and may shed light on microorganisms with the capacity to synthesise DMSP.

Research on biological DMS/DMSP production is well-represented in recent high impact journal publications and has been a well-funded and publicised area of NERC-based research, exemplified in the special report on microbial DMS production in NERC's Planet Earth (Summer 2009). In this report, the editor specifically highlighted the phrase "It is astonishing that we still do not know of a single gene for DMSP synthesis", clearly emphasising the potential impact of our work. Thus, we are confident that this project will be of interest to a wide scientific audience. We will continue to disseminate our findings in the best international peer-reviewed journals, but will also strive to include other publications in journals that have wider and less specialised audiences, such as New Scientist, the Microbiologist, Microbiology Today and Scientific American.

As described in Pathways to Impact, there is clear evidence that the media/general public found our previous NERC-funded work into DMS production to be interesting e.g. the Todd et al (2007) Science paper led to appearances on TV, radio interviews and press reports throughout the world. We will continue to disseminate our findings to the public and media through the UEA Communications Office and NERC.

Our Pathways to Impact focuses on delivering its outcomes mainly to our younger generation. This will be done through the SAW (Science Art Writing) scheme (http://www.sawtrust.org/) and will involve several local primary and secondary schools near UEA. We will also host visits of 6th Form level students in our labs and continue our outreach work to schoolchildren in the Norfolk area through visits, talks and student projects. The posting of material outlining our work on our website will allow us to reach a wider audience that we cannot reach via the above "local" proposals.

We do not envisage any immediate commercial or policy outputs from the work. However, as part of our impact plan, we will explore the potential of our DMSP-producing bacteria as sources for the production of DMSP catabolites that are high value chemicals. This will involve interactions with chemists (Page at UEA) and Industry (e.g. DuPontTM).