DiMethylSulfonioPropionate cycling In Terrestrial environments (DMSP InTerrest)
Lead Research Organisation:
University of East Anglia
Department Name: Biological Sciences
Abstract
Marine-dwelling microbes and plants produce 8 billion tonnes of dimethylsulfoniopropionate (DMSP) per year in Earth's surface oceans alone, via enzymes we have identified. Organisms produce DMSP to protect against salinity, cold, turgor pressure, oxidative and drought stresses, and predation. DMSP released into the environment is also widely taken up by microbes for these anti-stress properties, and used as a key nutrient via distinct degradation pathways. DMSP has critically important roles in global sulfur and carbon cycling, signalling, and as a major source of climate-active gases (CAG) e.g. dimethylsulfide (DMS) and the foul-smelling gas methanethiol (MeSH). Each year millions of tonnes of DMS, the characteristic smell of the seaside and a potent foraging cue guiding diverse organisms (gulls, seals, zooplankton, etc) to food, is released from DMSP via microbial DMSP lyase enzymes that we also identified. Some DMS is released and oxidised to form aerosols and cloud condensation nuclei in the atmosphere, which reduce the global radiation budget and 'cool' local climate. Critically, these sulfate aerosols return to land in rain - the primary transfer of biogenic sulfur from the oceans to land. DMSP synthesis and degradation are thought to occur only in marine settings, so DMSP cycling in terrestrial environments has largely been unexplored.
We challenged this dogma by revealing that DMSP synthesis is widespread in the plant Kingdom, ranging from common plants like grass, to agriculturally-important crops like maize, cabbage and sugarcane. Furthermore, our preliminary work shows that DMSP levels surpassing those in seawater exist in soils in which these key agricultural and bioenergy crops grow. Our work shows such soils liberate significant quantities of DMS and MeSH - processes ignored in climate models. We have also isolated novel bacteria and fungi from maize and sugarcane soils that utilise DMSP as a carbon source and show inducible DMSP-dependent DMS or MeSH production. Critically, these bacteria lack known DMSP degradation genes in their genomes, and thus likely possess novel DMSP catabolic enzymes and/or pathways. We have therefore uncovered a potentially large and virtually unexplored research area with profound implications for biogeochemical cycling. Our findings urgently require detailed study to establish the importance and influence of terrestrial DMSP cycling on the climate.
We wish to answer the fundamentally important questions of how microbes associated to terrestrial plants degrade DMSP, and the ecological and global importance of the process, especially relating to CAG production. We will test the hypothesis that plant-made DMSP is a key nutrient for CAG-producing microbes. In an everyday context, are microbes degrading DMSP responsible for the rotten MeSH smell associated with cabbage fields, or the sweet DMS smell associated with sweetcorn? We will study microbial DMSP degradation and concomitant CAG production associated to plants known to produce low (maize) and high (sugarcane) levels of DMSP, which together cover >0.2 billion ha. Collaborations are in place to sample these plants, as are the model DMSP-producing bacteria we isolated to study microbial DMSP degradation mechanisms in terrestrial environments. Our major aims are to elucidate the enzymes, pathways, and mechanisms of DMSP degradation in terrestrial microbes and use this knowledge to define the magnitude of the process and factors regulating it. Furthermore, we will use cutting-edge microbial ecology, modelling and process work to answer fundamental ecological questions: what are the key microbes that degrade DMSP and emit CAG in terrestrial environments, and how do they influence the climate?
We see our proposal as addressing a major new challenge that will reveal the importance of DMSP in terrestrial environments, uncovering new and unexpected research fields with far-reaching implications for current and future climate models.
We challenged this dogma by revealing that DMSP synthesis is widespread in the plant Kingdom, ranging from common plants like grass, to agriculturally-important crops like maize, cabbage and sugarcane. Furthermore, our preliminary work shows that DMSP levels surpassing those in seawater exist in soils in which these key agricultural and bioenergy crops grow. Our work shows such soils liberate significant quantities of DMS and MeSH - processes ignored in climate models. We have also isolated novel bacteria and fungi from maize and sugarcane soils that utilise DMSP as a carbon source and show inducible DMSP-dependent DMS or MeSH production. Critically, these bacteria lack known DMSP degradation genes in their genomes, and thus likely possess novel DMSP catabolic enzymes and/or pathways. We have therefore uncovered a potentially large and virtually unexplored research area with profound implications for biogeochemical cycling. Our findings urgently require detailed study to establish the importance and influence of terrestrial DMSP cycling on the climate.
We wish to answer the fundamentally important questions of how microbes associated to terrestrial plants degrade DMSP, and the ecological and global importance of the process, especially relating to CAG production. We will test the hypothesis that plant-made DMSP is a key nutrient for CAG-producing microbes. In an everyday context, are microbes degrading DMSP responsible for the rotten MeSH smell associated with cabbage fields, or the sweet DMS smell associated with sweetcorn? We will study microbial DMSP degradation and concomitant CAG production associated to plants known to produce low (maize) and high (sugarcane) levels of DMSP, which together cover >0.2 billion ha. Collaborations are in place to sample these plants, as are the model DMSP-producing bacteria we isolated to study microbial DMSP degradation mechanisms in terrestrial environments. Our major aims are to elucidate the enzymes, pathways, and mechanisms of DMSP degradation in terrestrial microbes and use this knowledge to define the magnitude of the process and factors regulating it. Furthermore, we will use cutting-edge microbial ecology, modelling and process work to answer fundamental ecological questions: what are the key microbes that degrade DMSP and emit CAG in terrestrial environments, and how do they influence the climate?
We see our proposal as addressing a major new challenge that will reveal the importance of DMSP in terrestrial environments, uncovering new and unexpected research fields with far-reaching implications for current and future climate models.
Organisations
- University of East Anglia (Lead Research Organisation)
- Friedrich Schiller University Jena (FSU) (Collaboration)
- Ocean University of China (Collaboration, Project Partner)
- Centre for Research on Ecology and Forestry Applications (Project Partner)
- Shandong University (Project Partner)
- University of Vienna (Project Partner)
Publications
Carrión O
(2023)
DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
in Nature Microbiology
Carrión O
(2023)
Molecular discoveries in microbial DMSP synthesis.
in Advances in microbial physiology
Hopkins F
(2023)
The biogeochemistry of marine dimethylsulfide
in Nature Reviews Earth & Environment
Li C
(2023)
Aerobic methylation of hydrogen sulfide to dimethylsulfide in diverse microorganisms and environments
in The ISME Journal
Li CY
(2023)
Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria.
in The ISME journal
Li CY
(2023)
Dimethylsulfoniopropionate and its catabolites are important chemical signals mediating marine microbial interactions.
in Trends in microbiology
Liu J
(2024)
A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation
in Marine Life Science & Technology
Stirrup R
(2023)
Aminolipids elicit functional trade-offs between competitiveness and bacteriophage attachment in Ruegeria pomeroyi.
in The ISME journal
Description | Collaboration with Georg Pohnert at University of Jena |
Organisation | Friedrich Schiller University Jena (FSU) |
Country | Germany |
Sector | Academic/University |
PI Contribution | In collaboration with our project partners, we have identified the enzymes that cleave DMSOP, a newly discovered marine organosulfur compounds, into DMSO and acrylate. |
Collaborator Contribution | Georg Pohnert' s group, from University of Jena, has analysed the metabolites of DMSOP in different algal species. |
Impact | A paper submitted to Nature Microbiology, which is currently under review. |
Start Year | 2020 |
Description | Collaboration with Yu-Zhong Zhang |
Organisation | Ocean University of China |
Country | China |
Sector | Academic/University |
PI Contribution | In collaboration with our project partners, we have identified the enzymes that cleave DMSOP, a newly discovered marine organosulfur compounds, into DMSO and acrylate. |
Collaborator Contribution | Yu-Zhong Zhang's group has resolved the crystal structures and determined the kinetic parameters of the enzymes that cleave DMSOP. |
Impact | A paper submitted to Nature Microbiology, which is currently under review. |
Start Year | 2020 |
Description | Microbial synthesis of dimethylsulphoniopropionate and dimethylsuphide (Prof. Xiao-Hua Zhang Ocean University, China) |
Organisation | Ocean University of China |
Country | China |
Sector | Academic/University |
PI Contribution | Collaborating with Prof. Xiao-Hua Zhang (Ocean University, China) we are characterising the molecular genetic systems utilised by marine organisms in their catabolism and synthesis of dimethylsulphoniopropionate (DMSP). |
Collaborator Contribution | Prof. Xiao-Hua Zhang (Ocean University, China) has isolated thousands of marine microbes and is screening them for their ability to produce and catabolise dimethylsulphoniopropionate (DMSP). Any positive strains are shipped to UEA for molecular characterisation. |
Impact | There are no output as yet but a full NERC grant will be submitted on this subject in January 2015. |
Start Year | 2013 |
Description | 'Secrets of the Seaside' |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Talk on 'Secrets of the Seaside' for Norwich Science Festival given by Dr Beth Williams detailing DMSP research conducted in Todd's lab. |
Year(s) Of Engagement Activity | 2024 |
Description | A changing perception of marine organosulfur cycling' |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Invited talk at the Microbial Cycling of Volatile Organic Compounds conference, John Innes Centre, Norwich, UK, May 2022. |
Year(s) Of Engagement Activity | 2022 |
Description | Bioacrylate production from algae |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Industry/Business |
Results and Impact | Invited talk at 3rd BBNet Conference, Sheffield, UK, 2024 to present work in our innovative study to generate bioacrylic acid from seaweeds. |
Year(s) Of Engagement Activity | 2024 |
Description | Chair and presenter for the Marine Microbial Ecology session at ISME19 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Chair and invited speaker in the Marine Microbial Ecology session at ISME19 International Conference in South Africa 2024. |
Year(s) Of Engagement Activity | 2024 |
Description | Marvellous Microbes |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Activity stall called 'Marvellous Microbes' for Norwich Science Festival |
Year(s) Of Engagement Activity | 2024 |
Description | Microbial Cycling of Volatile Organic Compounds conference, John Innes Centre, Norwich, UK, May 2022 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Invited talk at the Microbiology Society Annual meeting, Belfast, UK, April 2022. |
Year(s) Of Engagement Activity | 2022 |
Description | Organosulfur cycling by Harmful algae |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Professional Practitioners |
Results and Impact | Invited talk at the Royal Society Theo Murphy Meeting on Algal holobionts. Reading, UK, May 2023 to present work and network with PI studying holobiome research. Discussions resulted in a coordinated review article on the field submitted to New Phytologist. |
Year(s) Of Engagement Activity | 2023 |
Description | Talk on 'Secrets of the Seaside' for Lowestoft First Light Festival |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | Public lecture based on organosulfur cycling, marine microbiology and climate research conducted at Todd's lab. |
Year(s) Of Engagement Activity | 2023 |