Organosulfur cycling in abundant anoxic marine sediments: a case study of saltmarsh sediments

There is abundant oxygen in Earth's atmosphere, oceans and many soils, and this has enabled the evolution of multicellular life. The surface ocean is oxygen-rich because photosynthetic organisms (primary producers) are abundant. Some of these photosynthetic organisms make important molecules that can be released to the atmosphere. Once there, they can react and form clouds, generating rain and acidity in water vapour, and thus are important in climatology and sulfur cycling. The most well-known of these is dimethyl sulfide (DMS), which is derived from the action of marine microorganisms catabolising dimethylsulfoniopropionate (DMSP). An estimated several billion tonnes of DMSP is made each year by marine algae, corals, plants, and, as shown by us, marine bacteria. DMSP has other key roles in marine ecosystems, serving as an osmoprotectant, a nutrient for marine microbes, and, like DMS, it is a chemoattractant for many organisms that link it with food. DMSP and DMS are so abundant in marine environments that the characteristic smell associated with the seaside comes from DMS itself.

It is widely believed that only surface waters make significant amounts of DMSP and DMS via photosynthetic organisms. Our discovery that heterotrophic bacteria produce DMSP challenges this belief, since they do not require light. Furthermore, we have shown that large quantities of DMSP (orders of magnitude greater than in surface oceans), DMS and other organosulfur molecules exist in mud that is devoid of oxygen, and is instead filled with reduced iron (termed ferruginous) and reduced sulfur (termed euxinic). This was interesting and important, because we don't know how these molecules are produced or consumed in these very different environments, what organisms are involved and what role these molecules play in the microbial communities living there. Given that marine sediments cover over 70 % of Earth's surface, this topic is of global significance. Moreover, for 85% of Earth's history the ocean was likely free of oxygen, and only contained dissolved iron or sulfur. Were these molecules important in these past oceans? What role did they play?

As environmental conditions (including climate) likely affect DMSP/DMS production, and vice versa, it is key to understand and predict these effects. Current estimates of DMSP/DMS production are likely inaccurate due to i) a lack of integrated studies combining molecular, biogeochemical, process and modelling data; and ii) ignorance as to the input from bacterial DMSP-production, particularly from marine sediments.

Questions we will explore are: Why is there lots of DMS but none of its related metabolite, methanethiol (MeSH), in iron-rich sediments, while in sulfide-rich sediments it is the opposite? How are organisms making these molecules, and why? What role do these molecules play in bacterial communities in the mud? How significant is the production of these molecules on a global scale?

Our project is divided into several work packages. We will carry out a detailed, year-long study at Warham saltmarsh, which has ferruginous and euxinic sediment pools in close proximity. We will take samples and analyse the geochemistry and microbiology of sediments where we have identified these key patterns. We will determine what organisms are there, and what they are doing, using a series of molecular microbiology techniques, including 'omics work (on microbial community DNA & RNA) and stable isotope probing, which allows us to identify organisms actively cycling DMSP. We will then isolate and grow these microorganisms in the lab to understand how the production and consumption of these climatologically important molecules varies in response to the environmental changes we impose. Finally, we will model these changes and extrapolate to determine how important these environments are to the production and consumption of these molecules, which will be a definitive window to both the past and future.

We will provide a step-change in knowledge of the cycling of the climatologically important compounds dimethylsulfoniopropionate (DMSP), methanethiol and dimethyl sulfide (DMS). Current flux models of these molecules assume that they are solely produced and cycled in oxic and photic settings, but our new work shows that this is untrue. We find that marine bacteria are key producers of DMSP in marine sediment and have identified many of the key genes involved in the production and cycling of DMSP and other organosulfur compounds. This is important because DMSP and DMS are likely made in massive amounts in anoxic sediments, and have key roles in sulfur and nutrient cycling, signalling pathways and climate, yet very little is known about this microbial cycling in sediments. Our proposal is driven by the need to understand the amount, role and flux of these organosulfur molecules in anoxic sediments, which will better inform estimates of where they are made and how they are released to the environment.

Our research may benefit wider society through our models for DMSP/DMS dynamics which will inform policymakers on the potential environmental consequences of changes in DMSP/DMS production under future climate scenarios.

Our work will be of great interest to scientists including microbiologists, molecular ecologists, computational biologists, biological modellers and biochemists due to the range and quality of data generated. DMSP/DMS research is well-represented in recent high impact journals and is a well-publicised area of NERC research. We are confident our project will interest a wide scientific audience. We will disseminate our findings in the best international journals and strive to include publications in journals that have wider audiences.

The media and general public find our NERC-funded work on DMSP/DMS and sediment biogeochemistry interesting e.g., Todd's 2007 Science paper led to appearances on TV, radio interviews and press reports throughout the world, and Turchyn has been on several popular science radio shows, such as the BBC's Naked Scientist. We will continue to disseminate our findings to the public through e.g., UEA and Cambridge press offices, our websites, Twitter and NERC.

Our outreach focuses on delivering outcomes to the younger generation through various schemes (See Pathways to Impact document). These include the writing of articles, opening a project YouTube channel and Twitter account where we will place updates of our fieldwork, publications, conferences, videos for non-experts on field sampling, and relevant scientific information on saltmarsh biogeochemistry. We will produce two short research videos, one at the project's start explaining 'why it matters' and 'what we will do', and one near the end of the project to highlight our findings. We will also create displays at the Norfolk Wildlife Trust Education and Visitor Centre at Cley Marsh and Sedgwick Museum of Earth Sciences, Cambridge, which combined get 200,000 visitors per year.

DMSP/DMS research has applications of interest to industry. The co-products of DMSP lyase enzymes, hydroxypropionate or acrylate, are high-value chemicals in the plastics industry. Also, DMSP is an antistress compound and osmolyte in environments with high salt and sulfur levels, and DMS is a desirable flavour in e.g., beer and wine. By hosting summer internships through SfAM, Microbiology Soc. and UEA internship programmes, we will investigate these industrially applicable research areas. For example, through NERC-funded interns we have generated transgenic Arabidopsis plant lines that produce DMSP, which interns can help characterise for salt/cold tolerance, etc. As part of our impact plan and through such intern positions, we will explore the potential of these ideas that are enabled by our research. These internships provide excellent training opportunities for local students. All of Todd's NERC-funded interns have gone on to do PhDs.