A multidisciplinary study of DMSP production and lysis - from enzymes to organisms to process modelling.

Lead Research Organisation: Plymouth Marine Laboratory
Department Name: Plymouth Marine Lab

Abstract

A billion tonnes of the compatible solute dimethylsulfoniopropionate (DMSP) is made each year by marine phytoplankton, seaweeds, corals, coastal plants and, as shown by us, marine bacteria. DMSP has key roles in marine ecosystems when released into the environment, serving as an osmoprotectant and key nutrient for marine microbial communities. DMSP is also the main precursor of the climate-cooling gas dimethylsulfide (DMS). Many organisms cleave DMSP, producing ~300 million tonnes of DMS annually, ~10 % of which is released into the air. DMS oxidises in the atmosphere, producing aerosols that can lead to increased cloud cover and potential effects on climate, or be returned to land in rain, a key step in the global sulfur cycle. DMSP and DMS are also chemoattractants for many organisms which associate them with food.

Despite the importance of DMSP, knowledge of how and why it is produced is quite superficial. We know that DMSP and DMS production is highly variable between and within the different groups of producers, but the reasons for this variability are not understood, mainly because genes encoding DMSP synthesis enzymes have yet to be identified and DMSP lyases have only just been identified in a DMSP-producing organism.

Our preliminary work has identified dsy genes which encode key DMSP synthesis enzymes in bacteria, diatoms, dinoflagellates, corals and haptophytes - the major groups of marine DMSP-producers. Variability in DMSP/DMS production may stem from their different Dsy enzymes.

Our aim is to establish "why some organisms make more DMSP than others and the contribution of different organisms to global DMSP and DMS production".

It is possible that variability in DMSP production in different organisms stems from the differing efficiencies or expression of their Dsy enzymes. To test this, we will use biochemical techniques to characterise the different Dsy enzymes of the major classes of DMSP-producers.

We will study how diverse, model DMSP-producers express their DMSP and DMS synthesis enzymes in response to varying conditions, since the expression level may govern the amount of DMSP produced. This may shed light on the effects of climate change, e.g., if Dsy and DMSP lyase expression is increased by higher temperatures. For the important DMSP/DMS-producing algae Emiliania huxleyi and Symbiodinium, we will precisely locate the Dsy enzymes within the cell as this will help in understanding the role(s) of DMSP in these organisms. By relating cellular location and Dsy enzymology data to DMSP (and synthesis intermediates) and DMS concentrations, production rates in key DMSP producers and the conditions that enhance accumulation, we will more fully understand why high variability in DMSP and DMS production exists.

As future changes in environmental conditions will likely affect DMSP/DMS production, and potentially climate, and vice versa, it is important to understand and predict these effects. Current estimates of DMSP/DMS production are likely inaccurate due to a lack of integrated studies combining molecular, biogeochemical, process and modelling data. Here, we will carry out a detailed, year-long study at the coastal site L4 in the English Channel (chosen for its location and range of contextual data). We will study the diversity and expression of key genes in DMSP/DMS synthesis, DMSP synthesis rates, group-specific phytoplankton DMSP production, bulk standing stocks of DMSP (and synthesis intermediates) and DMS and microbial diversity over a seasonal succession. Our studies will tell us which organisms produce DMSP/DMS, production rates and concentrations, the genes used and under what conditions. Using these data, we will input critical state and rate parameters into a new model for DMSP/DMS dynamics, allowing the contribution of different taxa to global production of DMSP/DMS to be more accurately predicted, along with any possible effects of climate change.

Planned Impact

We show for the first time that marine bacteria can produce dimethylsulfoniopropionate (DMSP), and identify the key gene in DMSP synthesis in these bacteria and all the major classes of DMSP-producing algae. Many of these microbes also lyse DMSP, making the climate-active gas dimethylsulfide (DMS). Our work is important because DMSP/DMS are made in large amounts globally and have key roles in sulfur and nutrient cycling, signalling pathways and climate. The proposed project is driven by the need for a mechanistic understanding of these 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 DMSP/DMS production in marine environments.

Our work will be of interest to scientists including microbiologists, molecular ecologists, computational biologists, biological modellers and biochemists due to the range of data generated. The resources generated from the English Channel will be invaluable and complement existing biological knowledge of important ecosystems.

DMSP/DMS research is well-represented in recent high impact journals and has been a well-funded and publicised area of NERC research, e.g. a special report on microbial DMS production in Planet Earth (2009). Here the editor highlighted the phrase "It is astonishing that we still do not know of a single gene for DMSP synthesis", emphasising the potential impact of our work. Thus, we are confident our project will be of interest to a wide scientific audience. We will disseminate our findings in the best international peer-reviewed journals and strive to include other publications in journals that have wider audiences, e.g. Microbiology Today.

There is evidence that the media/general public found our previous NERC-funded work into DMSP/DMS 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 e.g. UEA, PML, our websites, Twitter and NERC.

Our outreach component of Pathways to Impact focuses on delivering its outcomes mainly to our younger generation. This will be done through SAW (Science Art Writing) and Research Network events (ResNet), and will involve local schools. We will host students in our labs and continue our outreach work to students around Devon and East Anglia via visits, talks and student projects. The posting of material outlining our work on our websites and Twitter will allow us to reach a wider audience.

There are potential commercial and policy outputs from our work. DMSP/DMS research has applications of interest to industry. The co-products of DMSP lyase enzymes, hydroxypropionate or acrylate are high-value chemicals, e.g. in the plastics industry. Also, DMSP is an antistress compound and osmolyte in environments with high salt/sulfur levels, and DMS is a desirable flavour in e.g. beer, wine or other foodstuffs. The ability of the organisms to produce both DMSP/DMS without expensive feedstock addition clearly offers potential benefits to industry. Knowing factors controlling DMSP/DMS production in different producers may allow for optimisation of the processes. The use of genetics and metabolic engineering could be used to improve yield and efficiency and/or introduce pathways into other organisms, e.g. one could potentially engineer methanogenic bacteria or crops to produce these products. As part of our impact plan, we will explore the potential of these ideas through interactions with chemists and industry.

This research will benefit wider society through improvements in policy facilitated by our new model for DMSP/DMS dynamics and its feeding into the European Regional Seas Ecosystem Model (ERSEM). These models can inform policymakers on the potential environmental consequences of changes in DMSP/DMS production under future climate scenarios.
 
Description The work is still in progress
Exploitation Route Too early to say
Sectors Environment

 
Description NERC Discovery
Amount £800,000 (GBP)
Funding ID NE/R010382/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 05/2018 
End 04/2021
 
Title DMS model formulation re-coded in the FABM-ERSEM framework 
Description Model formulation describing DMSP and DMS dynamics (Polimene et al., 2012) have been re-coded in the FABM-ERSEM modelling framework. 
Type Of Material Computer model/algorithm 
Year Produced 2017 
Provided To Others? No  
Impact The DMS(P) model developed at PML (Polimene et al., 2012) is now merged into the latest version of FABM-ERSEM developed in the framework of the Shelf Sea Biogeochemistry (SSB) program . The new FABM-ERSEM has increased modularity allowing a more versatile use of the model. The model code is now usable by the whole ERSEM community, within SSB and beyond. This version of the model will be used as developing platform in the project:' A multidisciplinary study of DMSP production and lysis - from enzymes to organisms to process modelling'. 
 
Title DMSP model developmets 
Description The DMSP 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 Sampling at Western CHannel Observatory 
Description DMSP synthesis rates at WCO at different times of year, combined with standing stock concentrations, group specific measuremnets and DNA/RNA sampling. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? No  
Impact None yet 
 
Description Genes to Gases Workshop 
Organisation University of East Anglia
Country United Kingdom 
Sector Academic/University 
PI Contribution Had idea of workshop, consulted UK network, workshop co-convener, presented talk, and led discussion session.
Collaborator Contribution Workshop organiser and co-convener
Impact The Genes to Gases workshop was held in June 2017, at the University of East Anglia. The workshop was multidisciplinary, included researchers from all over the UK, and covered biogeochemistry of trace gases and their precursors (measurement); genes, metabolic pathways, enzymes involved in their production, and modelling. A small group also discussed ideas for a large grant.
Start Year 2017
 
Description Genes to Gases Workshop 
Organisation University of Essex
Department Institute for Social and Economic Research, Essex
Country United Kingdom 
Sector Academic/University 
PI Contribution Had idea of workshop, consulted UK network, workshop co-convener, presented talk, and led discussion session.
Collaborator Contribution Workshop organiser and co-convener
Impact The Genes to Gases workshop was held in June 2017, at the University of East Anglia. The workshop was multidisciplinary, included researchers from all over the UK, and covered biogeochemistry of trace gases and their precursors (measurement); genes, metabolic pathways, enzymes involved in their production, and modelling. A small group also discussed ideas for a large grant.
Start Year 2017
 
Description NAAMES collaboration microlayer sampling 
Organisation University of California, Irvine
Country United States 
Sector Academic/University 
PI Contribution Shipping of microlayer samples from Woods Hole to the UK. Analysis of microlayer samples for N-osmolytes. Data interpretation with international team.
Collaborator Contribution The partners collected microlayer samples for us on board the NAAMES cruise (September 2017) in the North Atlantic. This was an add-on opportunity, and there is a team of international researchers analysing microlayer samples for their specialist parameters, enabling better understanding of the air-sea interface.
Impact Still in progress
Start Year 2017
 
Description Convening Genes for Gases workshop 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Convening workshop to be held in June 2017 entitled "Genes to Gases" for the UK community studying the biogeochemistry of trace gases and the microbial enzymes and pathways involved in their formation.
Year(s) Of Engagement Activity 2017
 
Description External examiner for PhD 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact External examiner for PhD on bacterial DMSP synthesis, UEA.
Year(s) Of Engagement Activity 2018
 
Description Genes to Gases workshop: DMS 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Talk delivered at Genes to Gases workshop: Biogeochemical cycling of DMS and associated compounds in the surface waters:from temperate to polar waters
Year(s) Of Engagement Activity 2017
 
Description Genes to Gases workshop: Discussion session 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact I chaired a discussion session at the Genes to Gases workshop (UEA, June 2017), to identify new interdisciplinary research crossover and priorities.
Year(s) Of Engagement Activity 2017
 
Description Genes to gases workshop: Modelling 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact A talk and discussion on the use of modelling in trace gas research was given at the Genes to Gases workshop.
Year(s) Of Engagement Activity 2017
 
Description Invited to attend ACE data workshop 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited and funded to attend Antarctic CIrcumnavigation Expedition Data Workshop in Lausanne. Outcomes were data integration projects.
Year(s) Of Engagement Activity 2018
 
Description NOSASSO International Workshop 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Researchers from 7 projects within the Circumnavigation Expedition project came together in Plymouth for 3 days to discuss our research approaches and findings together, to get the most value and understanding from our data
Year(s) Of Engagement Activity 2018
 
Description Polar 2018 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Attended Polar 2018 in Davos, and presented posters on: Exploring ocean-atmosphere exchanges in the SOuthern Ocean: the PEGASO and ACE projects; ANtarctic sea ice region as a source of biogenic nitrogen in aerosols.
Year(s) Of Engagement Activity 2018
 
Description Royal Society of Chemistry Invited Lecture 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Gave RSC invited lecture of biogeochemistry of N-osmolytes
Year(s) Of Engagement Activity 2019