Is bacterial DMS consumption dependent on methylamines in marine waters?
Lead Research Organisation:
Plymouth Marine Laboratory
Department Name: Plymouth Marine Lab
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.
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.
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
Airs R
(2023)
Correction to: Seasonal measurements of the nitrogenous osmolyte glycine betaine in marine temperate coastal waters
in Biogeochemistry
Airs R
(2022)
Seasonal measurements of the nitrogenous osmolyte glycine betaine in marine temperate coastal waters
in Biogeochemistry
Cree C
(2018)
Measurement of methylamines in seawater using solid phase microextraction and gas chromatography
in Limnology and Oceanography: Methods
Dall'Osto M
(2019)
Simultaneous Detection of Alkylamines in the Surface Ocean and Atmosphere of the Antarctic Sympagic Environment
in ACS Earth and Space Chemistry
Dixon JL
(2020)
Seasonal Changes in Microbial Dissolved Organic Sulfur Transformations in Coastal Waters.
in Microorganisms
Downes P
(2020)
Phosphorus dynamics in the Barents Sea
in Limnology and Oceanography
Jameson E
(2019)
Deltaproteobacteria (Pelobacter) and Methanococcoides are responsible for choline-dependent methanogenesis in a coastal saltmarsh sediment.
in The ISME journal
Mausz M
(2022)
Microbial uptake dynamics of choline and glycine betaine in coastal seawater
in Limnology and Oceanography
Description | A new research collaboration between this grant and the NERC Changing Arctic Ocean programme, specifically ChAOS (PI: Christian Mearz), enabled research under this proposal to be undertaken on a cruise (July 2019) in the Barents Sea. This has revealed exciting preliminary data showing highly variable concentrations (<1 to >30 nM) of the climate positive gas DMS on a south to north transect. We think this variability is a direct consequence of both the amount of primary productivity and phytoplankton species that were growing. For example, at a station north of Svalbard (>81oN) where the ship had to create a hole in the ice in order to sample the seawater, exceptionally high concentrations of DMS were measured (>30 nM) along with very abundant large chain forming pigment rich diatoms. This cruise also enabled us to undertake a series of methylamine addition experiments designed to test the novel hypothesis that 'availability of methylamines controls the loss of DMS in surface waters'. A series of preliminary methylamine addition experiments were also conducted in 2018. Recent stable tracer analysis of S compounds has revealed that the microbial consumption of DMS and dissolved DMSP and DMSO increases when the organic N compound trimethylamine is added. This has prompted a new emerging hypothesis that far more bacterial species use DMS/P/O as carbon and sulphur sources compared to those that specifically oxidise DMS to DMSO. |
Exploitation Route | Award still active so too early to state as not all outcomes are kown. |
Sectors | Environment |
Title | Barents Sea Arctic: Bacterial productivity & biomass |
Description | Bacterial production was determined using 3H-leucine and samples taken for bacterial enumeration using flow cytomtery back at PML. |
Type Of Material | Database/Collection of data |
Year Produced | 2019 |
Provided To Others? | No |
Impact | Analysis still underway. |
Title | Barents Sea Arctic: Concentrations of DMS, DMSP and DMSO |
Description | At 6 stations in the Barents Sea CTD profiles (to the 1% PAR depth) were taken of concentrations of DMS, DMSP and DMSO. |
Type Of Material | Database/Collection of data |
Year Produced | 2019 |
Provided To Others? | No |
Impact | Preliminary results shown (poster and oral presentation) at the Annual Changing Arctic Ocean meeting, Potsdam, Germany, 2020 and at Nansen Legacy meeting, Norway, November 2019. |
Title | Barents Sea Arctic: rates of primary productivity and phytoplankton species. |
Description | Rates of primary productivity were determined using 14C-sodium bicarbonate. Samples were also taken for determining phytoplankton species and abundance. |
Type Of Material | Database/Collection of data |
Year Produced | 2019 |
Provided To Others? | No |
Impact | Analysis - still underway. |
Title | Barents Sea: Methylamine addition experiments |
Description | A series of methylamine addition experiments were completed in order to test the hypothesis that ' methylamines control the loss of DMS in seawater'. Stable sulphur tracer samples were collected tfor analysis back at PML, along with samples for N-Osmolytes, methylamines and DNA. |
Type Of Material | Database/Collection of data |
Year Produced | 2019 |
Provided To Others? | No |
Impact | None yet as samples waiting for analysis. |
Title | DMSP/DMS model developmets |
Description | The DMSP/DMS model published in 2012 (Polimene at al 2012) was modified extending DMSP production to all the functional types described in the ERSEM model. The model was implemented at L4 station in the Western English Channel and simulation were qualitatively compared with available literature data (Archer et al 2009) |
Type Of Material | Computer model/algorithm |
Year Produced | 2019 |
Provided To Others? | No |
Impact | This exercise provided a preliminary assessment of model capability to simulate DMSP dynamics in a coastal area |
Title | L4 time series - DMS/Methylamines |
Description | Preliminary Tedlar incubation methylamine addition experiments (with stable S tracers d3-DMS, d6-DMSP, 13C2-DMSO) have been undertake at station L4. Routine sampling will commence in ~September 2019 as detailed in the proposal. |
Type Of Material | Database/Collection of data |
Year Produced | 2018 |
Provided To Others? | No |
Impact | None yet - too early in the research proposal. |
URL | https://www.pml.ac.uk/Research/Projects/Bacterial_DMS |
Description | Arctic water column biogeochemistry |
Organisation | University of Leeds |
Department | School of Earth and Environment |
Country | United Kingdom |
Sector | Academic/University |
PI Contribution | Water column measurements of DMS, particulate and dissolved DMSP, DMSO and , methylamines, particulate N osmolytes, rates of S transformations, primary production, bacterial production, activity of extracellular enzymes, uptake and excretion of inorganic P, phytoplankton biomass and biodiversity, bacterial numbers, bacterial species diversity to two CHAOS Arctic ocean research cruises in the Barents Sea. |
Collaborator Contribution | Supporting water column measurements e.g. temp, salinity, chlorophylla etc and the opportunity and infrastructure to participate in two Arctic Ocean research cruises. |
Impact | Outputs will include data sets and manuscripts - still in preparation. |
Start Year | 2018 |
Description | Nansen Legacy Science Meeting |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Study participants or study members |
Results and Impact | Annual science meeting of the Nansen Legacy project, opened to UK Arctic research community |
Year(s) Of Engagement Activity | 2020 |
Description | Participation in ECSA focus meeting: Coasts and Estuaries of Southwest England |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Postponed from 2020 due to Covid. Rescheduled for 2021. Talk entitled "Marine Biogeochemistry of N-osmolytes. |
Year(s) Of Engagement Activity | 2020,2021 |
Description | UK-Russia join Arctic event |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Study participants or study members |
Results and Impact | UK-Russia Arctic session for promoting collaboration between researchers |
Year(s) Of Engagement Activity | 2020 |