Is bacterial DMS consumption dependent on methylamines in marine waters?

Lead Research Organisation: Plymouth University
Department Name: Sch of Geog Earth & Environ Sciences

Abstract

Dimethylsulfide (DMS) is a key ingredient in the cocktail of gases that makes up the 'smell of the sea'. Around 300 million tons of DMS are formed each year by single-celled organisms in the surface ocean. A small proportion (up to 16%) of this DMS is released into the atmosphere, forming cloud-seeding compounds which can influence our weather and climate. When it rains, sulfur compounds are deposited back into the soils of our continents. However, most of the DMS formed in the oceans stays there, facing consumption by marine microbes and conversion to another sulfur compound - dimethylsulfoxide (DMSO). DMSO is usually the most abundant organic sulfur compound in the oceans and represents a major pool of the essential life elements sulfur and carbon.

Seawater contains a rich mixture of important chemical nutrients that support the entire oceanic food web. The dissolved organic nitrogen pool is a chemical 'drive thru' which contains the highly reactive N-osmolytes: glycine betaine, choline and trimethylamine N-oxide. These chemicals are used by microorganisms to protect them from changes in their environmental conditions, such as variability in the saltiness of the surrounding seawater, and to protect their cells from chemical or physical damage. When N-osmolytes breakdown they can release gases such as methylamines into the atmosphere which can influence the climate.

We have found a previously unrecognised and intriguing link between the bacterial breakdown of organic nitrogen compounds, like methylamines, and organic sulfur compounds like DMS. This link is provided by a bacterial enzyme called trimethylamine monooxygenase (Tmm). Tmm simultaneously removes both methylamines and DMS from seawater (converting it to DMSO). In fact we think this production of DMSO doesn't happen without the presence of methylamines. We estimate that up to 20% of all bacteria in our oceans contain this particular enzyme. The research we want to carry out will firstly investigate this link between DMS removal and methylamine availability in 'model' micro-organisms in the laboratory, checking that this link is active and how it is controlled in key marine bacteria commonly found in the global oceans. We will next determine the importance of this process compared to other biological processes that consume DMS in seawater and put names to the microbes using this enzyme to remove DMS.

We will study the microbial processes linking the organic sulfur and nitrogen cycles in the English Channel at a station that is sampled weekly as part of the Western Channel Observatory which is coordinated by Plymouth Marine Laboratory. This is a long-standing time series site for which a wealth of oceanographic and biological data are available (algal diversity, temperature, nutrients etc.; http://www.westernchannelobservatory.org.uk), which we will be able to use. A global model of particles in the atmosphere has recently suggested that changes in the location of DMS emissions, through climate-driven changes in the phytoplankton species distributions, could strongly influence our climate. We therefore want to investigate the link between DMS removal, the availability of organic nitrogen compounds like methylamines and phytoplankton species, which we can do at station L4, where phytoplankton species succession is understood and can be easily sampled.

We will compare this temperate coastal region to one of the Earth's DMS hotspots - the Southern Ocean. The atmosphere above this remote and isolated ocean is pristine in comparison to the heavily polluted air of the Northern Hemisphere. Here, the connection between DMS produced in the oceans and our climate is thought to be the strongest. Given the important role of DMS, identifying the role of marine microorganisms and the pathways of DMS removal from seawater will provide key information that will improve our future understanding of how the sulfur cycle influences our climate.

Planned Impact

This project will provide crucial understanding of how microbes drive biogeochemical cycling of dimethylsulfide through a hitherto unrecognised co-oxidative pathway that links the organic nitrogen and sulfur biogeochemical cycles. The specific outcomes of this research are connected to other, overarching areas of environmental science (environmental & climate change, biogeochemistry), microbiology (metabolism of organic sulphur compounds, regulation of metabolic and co-oxidative pathways) and atmospheric science (pathways affecting production of secondary organic aerosols). As such, the impacts of this fundamental research will be relevant for a number of different audiences including marine scientists, microbiologists, modellers, atmospheric and climate scientists, policy makers, as well as the general public.

Academic audiences will benefit from this research through a better understanding of a previously unrecognised pathway that links the fate of organic nitrogen and dimethyl sulphide (DMS) in the marine environment. This pathway also contributes to controlling emissions of DMS which plays a major role in atmospheric chemistry and the production of precursors of secondary atmospheric aerosols which affect climate. Climate scientists will benefit from the new knowledge gained that will be incorporated into models with an increased capability to better predict DMS concentrations in seawater and resulting emissions to the atmosphere. The Polar Regions are experiencing particularly strong climate change, and at the same time are hot spots for DMS cycling. In the Antarctic region the sensitivity to, and potential feedbacks of altered atmospheric DMS fluxes for regional climate control are particularly high, and an essential component for modelling regional and global future climate change. Beneficiaries include organizations such as the Intergovernmental Panel for Climate Change (IPCC). Models like the one used in this research are already used by the National Centre for Ocean Forecasting (NCOF), the UK Met Office (PML is in routine communication with these organizations) to underpin knowledge dissemination and provide consultancy regarding marine ecosystem services, protection and management of the marine environment to both policy makers and the general public. The new model code will be readily available for all the above cited organizations (NCOF, UK Met Office) giving them the possibility to use the refined version of ERSEM to aid dissemination of scientific knowledge and inform policymakers.

Policy makers will benefit from the research through the improved capabilities of future climate modelling based on the insights from the research as described above. Climate change is undoubtedly the biggest and most important challenge faced by humanity and policy needs to be formulated and enacted in order to avoid dangerous levels of climate change to occur. Through improving climate forecasting, our research will contribute to the knowledge base on which policy makers can make informed decisions that will steer the direction of the UK, European and global economic and environmental strategies for the next decades.

The general public will benefit from this research through better informed environmental policy (above) and better climate predictions. It is essential to communicate the outcomes of complex environmental processes to the public in order to generate a better overall public understanding of science. We will use a wide variety of methods to engage with general public end-users, including a detailed project website, regular updates by social media such as the Twitter accounts of institutions and investigators involved (e.g @WarwickLifeSci, @PlymouthMarine, @HSchafer_lab, @Chen_group), publications in popular magazines (e.g. Microbiology Today, Planet Earth, the Conversation), as well as presentations to the public through presentations during Open Days and public science events.

Publications

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Description Methylamines, which are compounds produced by marine primary production , have the potential to contribute to climate-regulation processes. Our analyses have shown that these compounds were abundant in Arctic Ocean samples during a summer bloom period, indicating the importance of understanding their cycling and global role in climate reactions. We have also developed the analytical method so that the volume of sample required for detection of methylamines at the low nmolar level is reduced from 1 L to 10 mL.
Exploitation Route The research provides evidence for the abundance of these molecules in the Arctic Ocean and mirrors their detection in the Antarctic. This data can provide a basis for further forensic investigations of the conditions leading to the production of methylamines and their abundance, further constraining the role within marine systems.
Sectors Environment

 
Title Measurement of dissolved methylamines in seawater 
Description The methylamines form part of the marine organic nitrogen pool. Although they are ubiquitous in marine systems, little is known about their distribution, production and fate in the marine environment. Analytical methods have been developed for their analysis in marine waters, but these have employed custom-made apparatus, limiting data to a few studies. We developed a method developed for the determination of methylamines in seawater which combines headspace solid phase micro-extraction (SPME) and gas chromatography with selective nitrogen detection. The gaseous methylamines are pre-concentrated from water samples (approximately 1 L) at elevated temperature, onto a polydimethylsiloxane/divinylbenzene SPME fibre. The analytes are then thermally desorbed from the fibre in a gas chromatograph containing a CP-Volamine column and a nitrogen-phosphorus detector. The method can be routinely calibrated down to 1 nM for all three methylamines using matrix-matched external standards. Limits of detection are determined operationally and have ranged from 0.4-2.9 nM during two sampling campaigns. The method has been used on seawater samples from the English Channel and Southern Ocean where concentrations up to 20 and 5.6 nM were measured, respectively; these values are consistent with previously reported levels. The method is suitable for the analysis of methylamines, and other low molecular weight amines, as it is sensitive, robust, and the necessary equipment is widely-available. 
Type Of Material Technology assay or reagent 
Year Produced 2018 
Provided To Others? Yes  
Impact The method has been deployed on 2 Antarctic research cruises and is being applied to samples from both the Arctic and Antarctic Oceans and European coastal waters. 
 
Description Inaugural Professorial Lecture; Nitrogen - the wicked element 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Inaugural professorial lecture on 6th June 2022. Almost 200 people attended in person or online, including guests from North America, Asia and Europe.
Year(s) Of Engagement Activity 2022
URL https://www.plymouth.ac.uk/research/professorial-mark-fitzsimons