Understanding and modelling the Microbial Carbon Pump under changing nutrient concentrations and temperature

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

Abstract

Seawater is a complicated soup of chemicals including dissolved organic material (DOM), such as sugars, fats and amino acids all containing carbon. In fact, there is roughly the same amount of carbon within marine DOM as there is CO2 in the atmosphere. So how did this carbon become DOM, and what controls its production and fate? Atmospheric CO2, dissolves in seawater where small single celled organisms called phytoplankton incorporate it into organic molecules essential for their growth. Some of these organic molecules leak from healthy cells, while more are released when cells die, or are eaten, creating an oceanic pool of DOM.

Many people are familiar with the concept that phytoplankton support marine food webs and that dead cells and detritus generated by different biological processes sink to the seafloor to be buried in sediments. This process effectively transports carbon, originally present as atmospheric CO2, to the seafloor; this is termed the 'Biological Carbon Pump' (BCP).

A separate process, which scientists have only recently become aware of, provides another way of removing and storing atmospheric CO2. The key role in this process is played by even smaller organisms which are numerically the most abundant life form in the oceans: the bacteria. Bacteria quickly act upon the DOM released from phytoplankton and the activities of their associated food web, scavenging parts they can most readily use for growth. Progressively, over weeks and months, sequential scavenging of components of DOM gradually transforms the chemical nature of the remaining material so that the residual molecules contain little else worth taking. These molecules, commonly defined as 'refractory-DOM', are biologically worthless, and are left to travel the Earth's Oceanic currents.

The process described here is called the 'Microbial Carbon Pump' (MCP) and is thought to have slowly accumulated and stored a staggering amount of refractory-DOM over the past millennia, estimated to be 624 gigatonnes. This incredible reservoir of carbon is currently thought to be stable, with abiotic removal processes (e.g. photo degradation) balancing its production. However, recent studies suggest that that the projected decrease in surface ocean inorganic nutrient availability due to climate change could modify MCP activity, increasing refractory-DOM production with respect to its consumption. This implies that marine bacteria have the potential to mitigate the anthropogenic increase in atmospheric CO2 by shunting more carbon into refractory-DOM. This hypothesis, if verified, will radically change the way we think of the capacity of the biosphere to modulate climate, suggesting a previously overlooked climate-active role for marine bacteria.

The only way we have to understand if this mechanism is significant is to use numerical models and run them under changing environmental conditions. However, to date, no ocean or Earth system models account for MCP dynamics.

In this project, we will conduct laboratory experiments to provide the required level of physiological information and understanding needed to enable us to develop the first model describing the MCP and its relationship with nutrient concentration and temperature. This outcome will be the first critical step toward the simulation of the MCP in present and future oceans. To achieve this ambitious goal, the project will bring together a multidisciplinary team of internationally recognised scientists, from chemical analysts to system biology and ecosystem modellers. The project team will be boosted by the partnership with Prof N. Jiao (Xiamen University, China) who first proposed the MCP concept in a seminal paper 7 years ago.

Planned Impact

This proposal provides cutting-edge science to assess the functioning of the Microbial Carbon Pump in relation to changing environmental conditions such as temperature and inorganic nutrient concentration. As such, the proposed research is expected to have its major impact within the academic community (see Academic Beneficiaries section). However, there is an urgent need to inform policymaker's decisions and to heighten the general public's awareness of climate change issues which this project will also address through the mechanisms outlined below.

The main potential impact of this project on policy would be the delivery of a robust, physiologically based, model formulation describing MCP dynamics. This formulation will be embedded in the European Regional Seas Ecosystem Model (ERSEM) significantly improving the capability of this model to simulate the extant ocean carbon cycle and to reliably test future scenarios hypotheses. Indeed, this project will provide the wherewithal to enable an explicit description of one of the largest pools of carbon on Earth, a pool hitherto considered in steady-state and thus ignored. The new version of ERSEM will thus be a valuable tool to provide evidence-based policy advice on marine climate change which is increasingly required by EU governments. The new model will directly benefit the National Partnership for Ocean Prediction (NPOP) and the UK Met Office. Both already use ERSEM to disseminate knowledge and provide consultancy regarding marine ecosystem services, protection, management and insight into climate related issues to both policy makers and the general public.

A number of surveys have shown that public awareness about climate change is increasing. However, although it is widely understood that human-induced climate change is occurring, uncertainty about the impacts and feedbacks remain. For this reason public opinion increasingly looks for science-based answers to climate change questions. The outcomes of our project, highlighting the potential of marine microbes to mitigate the projected increases in atmospheric carbon dioxide, will thus be of broad public interest. High impact scientific publications (Nature, Science, PNAS, GRL etc) will be the natural vehicles to disseminate results. However we will also disseminate the project's findings through less specific literature such as the Marine Climate Change Impacts Partnership (MCCIP) annual report and the PML Annual Review, which is distributed internationally to 800+ recipients. We will also use 'The Conversation' as a platform for science-public dissemination, one that specifically promotes interactions with the public.

As opportunities arise, we will seek to present our research to UK and international audiences. A public facing webpage will be created and hosted by PML and the project's news and updated results will be promoted via social media channels, e.g. PML's Twitter feed and Marine Ripple Twitter feed (hosted by PML). We will work closely with colleagues in the Communications Group at PML who will help us to gain and co-ordinate press coverage throughout the project.

Publications

10 25 50
 
Description The production of dissolved organic matter (DOM) represents an important route for the removal of atmospheric CO2. DOM is made by plankton and modified by bacteria to a state at which no further degradation proceeds. This final product is termed recalcitrant DOM (rDOM). How this process operates, and the implications of climate change upon it, is unclear. Our results, from very long and technically challenging experiments, have shown that the constitution of the bacteria community plays a critical role in the process. As the remaining food value of the DOM declines we see a switch of the bacteria to exploiting energy through the oxidation of ammonium through to nitrate; this is a very inefficient process and clearly indicates the low food value of DOM which is then used solely for structural materials. The production of nitrate is itself an important event as this nutrient supports the vast microalgal blooms that grow across the oceans. The other important event that we have noted is that the efficiency of rDOM formation is affected by the availability of inorganic nutrients (N and P) that affect the need of the bacteria to waste DOM to extract the organically-bound N and P within it.

We have developed a new mathematical model to describe the events we have seen, a model that is unique, a first of its kind. This model will eventually be made available as part of an educational aid, to be run on PCs and operated by students.

We have additionally developed a new modelling descriptions of plankton viruses. The activity of viruses leads to the release of DOM. Our models have revealed a novel and exciting new take on how viruses affect plankton growth. Traditionally they have been seen as a terminator of blooms of plankton. Our new work shows that after such a large termination, the residual virus load in the water column controls subsequent growth of that species of plankton for some considerable time. This allows other, competitor, plankton to thrive, thus affecting the overall dynamic of plankton ecology and thence of the microbial carbon pump.
Exploitation Route We are working to provide digital-twin forms of models describing the MCP for use in education.
Sectors Education,Environment

 
Title Application of methods developed to examine microbial use of DOM. 
Description Methods developed for this project designed to establish DOM enriched media for microbial cells is being used to test the impact of environmental conditions upon microbial DOM transformation. Conditions will include the impact of temperature and nutrient regime. The extent to which microbial cells access and produce recalcitrant DOM will be related to environmental conditions and used for model development. 
Type Of Material Biological samples 
Year Produced 2020 
Provided To Others? No  
Impact N/A at this stage 
 
Title Culture methods established for enabling analytical examination of phytoplankton DOM 'fingerprints'. 
Description Culturing methods using axenic cell lines established so that the DOM produced by phytoplankton can be extracted, and samples prepared for mass spectrometry analysis. These fingerprints will represent the biochemical complexity of the living cells. Uniquely to this study, this material will not have been exposed to bacterial activity and so will include the full spectrum of material that is available to natural bacterial communities. 
Type Of Material Biological samples 
Year Produced 2019 
Provided To Others? No  
Impact This is a facilitating development for the delivery of the project. 
 
Title DOM degradation experiment 
Description Completed 1 year culture experiments investigating the decomposition of DOM by a single bacterial species (alteromonas) compared to a natural community to compare the extent to which recalcitrant DOM is produced 
Type Of Material Biological samples 
Year Produced 2020 
Provided To Others? No  
Impact These data will allow to investigate DOM degradation and transformation mechanisms 
 
Title DOM degradation experiment under changing nutrient conditions 
Description Completed more than 6 months of natural bacterial community culture to investigate how inorganic nutrient availability influences their ability to access DOM 
Type Of Material Biological samples 
Year Produced 2020 
Provided To Others? No  
Impact These data will allow to investigate the effect of inorganic nutrients on marine DOM degradation and transformation 
 
Title Development of data analysis methods 
Description Python-based software tools for the assignment of DOM spectra and subsequent post-processing. Including Mass defect analysis, Kendrick analysis . 
Type Of Material Improvements to research infrastructure 
Year Produced 2020 
Provided To Others? Yes  
Impact Enables the robust interpretation of mass spectrometric data from seawater sources. 
 
Title Experimental investigation of the microbial degradation of DOM underway. 
Description Processes designed to provide axenic DOM-enriched culture media have been successfully developed. The first experiments designed to investigate microbial degradation and transformation of DOM in culture are underway. The growth of a single bacterial species is being compared to a microbial community, in terms of their capacity to access and transform DOM. Experiments will be performed for up to 1 year and test the hypothesis that a microbial community is essential for recalcitrant DOM formation. 
Type Of Material Biological samples 
Year Produced 2020 
Provided To Others? No  
Impact N/A at this stage 
 
Title Investigations into the spectrum of DOM compounds produced by phytoplankton cells. 
Description Experiments are underway to examine the range of DOM compounds produced by phytoplankton cells, and how this ranges relates to physiological status. This 'fingerprint' will be examined using sophisticated analytical tools and modelling approaches that will also support related experiments in this project. Preliminary runs suggested that there are substantial shifts in this spectrum as the cells pass through healthy growth stages into resource limitation. The hypothesis was raised that phytoplankton themselves are a source of recalcitrant material to marine systems. 
Type Of Material Biological samples 
Year Produced 2020 
Provided To Others? No  
Impact n/a at this stage 
 
Title Low-light-adapted Synechococcus cultivation 
Description We have successfully managed to culture a low-light-adapted strain of marine Synechococcus, which has taken us several months to optimise for maximal growth through trial and error. This strain would not grow when we first acquired it into our lab, but through careful cultivation it is now growing well. 
Type Of Material Cell line 
Year Produced 2019 
Provided To Others? No  
Impact Successful growth of Synechococcus will add enormous scientific value to our research project as it will allow us to include an ecologically-relevant representative of oceanic realms into our experimental systems. This will further enhance the global significance of our results and ouptuts as Synechococcus species are ubiquitous. 
 
Title Analysis of chemical data 
Description Developed preliminary procedures for the analysis of complex mass-spectrometry data sets from different DOM degradation experiments 
Type Of Material Data analysis technique 
Year Produced 2020 
Provided To Others? No  
Impact These procedures allow to assess changes in the chemical structure of DOM as consequence of bacterial consumption and transformation. 
 
Title DOC simulations at BATS 
Description Simulations of dissolved organic carbon (DOC) have been carried out in the Sargasso Sea (BATS station). Model simulation have been compared with available data 
Type Of Material Computer model/algorithm 
Year Produced 2019 
Provided To Others? No  
Impact The aim of this exercise is to evaluate the capability of the ERSEM model to simulate DOC production and transformation with particular emphasis on recalcitrant DOC production and microbial carbon sequestration. This exercise could lead to a re-parameterization and recalibration of the ERSEM model potentially improving its capability to simulate important aspects of the marine carbon cycle (e.g. DOC production, consumption and transformation) 
 
Title Datasets describing the influence of DOM and nutrient (N and P) additions on microbial community composition and diversity 
Description In depth Illumina MiSeq of 16S rRNA genes (V4 region) of the microbial community in a series of experiments designed to investigate the influence of DOM and nutrient (N and P) additions on community composition and diversity. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact Initial results show addition of DOM and inorganic nutrients influence the succession of microbial community over time. 
 
Title Virus model 
Description FLYNN KJ, Kimmance SA, Clark DR, Mitra A, Polimene L, Wilson W (2021) Modelling the effects of traits and abiotic factors on viral lysis in phytoplankton. Frontiers in Marine Science 8, 460 DOI: 10.3389/fmars.2021.667184 
Type Of Material Computer model/algorithm 
Year Produced 2021 
Provided To Others? Yes  
Impact FLYNN KJ, Kimmance SA, Clark DR, Mitra A, Polimene L, Wilson W (2021) Modelling the effects of traits and abiotic factors on viral lysis in phytoplankton. Frontiers in Marine Science 8, 460 DOI: 10.3389/fmars.2021.667184 
 
Title new model formulation describing viral lysis in ERSEM 
Description A new model formulation has been developed and implemented in the primary production module of the ERSEM model. According to experimental evidences, viral lysis is assumed to increase with the growth rate of the phytoplankton host. This implies an inverse relationship between nutrient limitation and lysis. 
Type Of Material Computer model/algorithm 
Year Produced 2019 
Provided To Others? No  
Impact The new formulation implies reduced viral lysis in the oligotrophic region of the ocean. This has the potential to affect the way we simulate carbon cycle in the ocean, notably primary production and dissolved organic carbon production and fate. 
 
Description Collaboration with Xiamen University on the theme "microbial carbon sequestration" (International workshop held in November 2018) 
Organisation Xiamen University
Country China 
Sector Academic/University 
PI Contribution MCP project presented to project partner (Xiamen University) in a international wokshop held in China (Xiamen, November 2018)
Collaborator Contribution Xiamen University is one of the world leading institutions in the field of microbial ocean carbon sequestration. They provide useful feedback on how to conduct our experimental work and develop new model formulations.
Impact This collaboration resulted in 4 shared publication (so far).
Start Year 2018
 
Description MCP project web site delivered 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A public facing website describing the rationale of the project and the a scientific activities which will be carried out was published.
The website is meant to describe project activities and outcomes to a wider scientific community.
Year(s) Of Engagement Activity 2018
 
Description You Tube video describing MCP-related concepts and project activities 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact The audio podcast explains in simple terms the rationale of the project and the potential climate-active role of the Microbial Carbon Pump
Simple animations help to deliver the message. The video is meant to explain the potential of the microbial carbon sequestration and its global implications to a general audience
The video had 404 views so far.
Year(s) Of Engagement Activity 2018