Revealing a mechanistic understanding of the role of viruses and host nutrient status in modulating CO2 fixation in key marine phototrophs
Lead Research Organisation:
Plymouth Marine Laboratory
Department Name: Plymouth Marine Lab
Abstract
The oceans play a major role in determining world climate. In part, this is due to the production of oxygen and the consumption of carbon dioxide by very small, single celled organisms, which are referred to as the photosynthetic picoplankton. Marine cyanobacteria of the closely-related genera Prochlorococcus and Synechococcus are the prokaryotic components of the photosynthetic picoplankton. These cyanobacteria are continually growing and dividing, but they can also be infected and killed by viruses.
Viruses that infect bacteria (bacteriophage) have provided the basis of our current understanding of molecular biology and genetics and have recently assumed a much greater significance with the recognition of the extraordinary abundance of bacteriophages and their central role in many biological processes. Cyanophages are viruses that are specifically capable of infecting a type of bacteria (cyanobacteria) that utilises light as its primary energy source through the process of photosynthesis. The cyanobacterial photosynthetic machinery captures light energy and transfers it to chemical energy which is subsequently used for growth and replication.
Oceanic regions vary considerably in their supply of nutrients e.g. phosphate, nitrogen and iron, that are critical for the growth of cyanobacteria, potentially limiting CO2 fixation by these organisms. The availability of nutrients may also affect cyanophage replication, since during infection cyanophage rely on their hosts to provide them with enough energy and resources to allow them to replicate efficiently.
However, the effect of nutrient availability on marine cyanobacterial CO2 fixation in the presence and absence of phage infection is largely unknown. This is important because marine cyanobacteria are critical contributors to global CO2 fixation and virus infection of these organisms may significantly modulate this contribution.
One exception is that phosphate limitation of marine Synechococcus has been shown to cause an 80% reduction in the number of cyanophage produced with <10% of cells lysing. Cyanophage infect P starved cells but remain inside their hosts without killing them, in a state known as 'pseudolysogeny'. Given that oceanic systems are often depleted in nutrients such as P (as well as nitrogen (N) and iron (Fe)) suggests such infection dynamics are likely widely prevalent in the natural environment.
Hence, in this proposal we will determine the role that nutrient limited growth plays on marine cyanobacteria CO2 fixation rates in the presence and absence of phage infection. We will also assess the role that specific cyanophage genes contribute to the process, and determine the molecular basis regulating 'pseudolysogeny'. Moreover, we will also provide a reliable (experimentally-derived) mathematical formulation describing viral infection which will be incorporated into an Ecosystem Model [ERSEM] providing a substantially improved simulation of oceanic primary production.
Overall, the proposal will therefore provide direct estimates, and a mechanistic basis, for understanding the role of nutrients and cyanophage infection in controlling marine primary production. Data and concepts will subsequently be used in ERSEM to refine control points for marine photosynthesis and subsequent C cycling.
Viruses that infect bacteria (bacteriophage) have provided the basis of our current understanding of molecular biology and genetics and have recently assumed a much greater significance with the recognition of the extraordinary abundance of bacteriophages and their central role in many biological processes. Cyanophages are viruses that are specifically capable of infecting a type of bacteria (cyanobacteria) that utilises light as its primary energy source through the process of photosynthesis. The cyanobacterial photosynthetic machinery captures light energy and transfers it to chemical energy which is subsequently used for growth and replication.
Oceanic regions vary considerably in their supply of nutrients e.g. phosphate, nitrogen and iron, that are critical for the growth of cyanobacteria, potentially limiting CO2 fixation by these organisms. The availability of nutrients may also affect cyanophage replication, since during infection cyanophage rely on their hosts to provide them with enough energy and resources to allow them to replicate efficiently.
However, the effect of nutrient availability on marine cyanobacterial CO2 fixation in the presence and absence of phage infection is largely unknown. This is important because marine cyanobacteria are critical contributors to global CO2 fixation and virus infection of these organisms may significantly modulate this contribution.
One exception is that phosphate limitation of marine Synechococcus has been shown to cause an 80% reduction in the number of cyanophage produced with <10% of cells lysing. Cyanophage infect P starved cells but remain inside their hosts without killing them, in a state known as 'pseudolysogeny'. Given that oceanic systems are often depleted in nutrients such as P (as well as nitrogen (N) and iron (Fe)) suggests such infection dynamics are likely widely prevalent in the natural environment.
Hence, in this proposal we will determine the role that nutrient limited growth plays on marine cyanobacteria CO2 fixation rates in the presence and absence of phage infection. We will also assess the role that specific cyanophage genes contribute to the process, and determine the molecular basis regulating 'pseudolysogeny'. Moreover, we will also provide a reliable (experimentally-derived) mathematical formulation describing viral infection which will be incorporated into an Ecosystem Model [ERSEM] providing a substantially improved simulation of oceanic primary production.
Overall, the proposal will therefore provide direct estimates, and a mechanistic basis, for understanding the role of nutrients and cyanophage infection in controlling marine primary production. Data and concepts will subsequently be used in ERSEM to refine control points for marine photosynthesis and subsequent C cycling.
Planned Impact
This project addresses a fundamental question relating to the marine carbon cycle, namely what role do viruses play in modulating CO2 fixation in numerically abundant marine cyanobacteria. The work is therefore of utmost relevance to NERC's strategic aims, particularly Biodiversity Science and Climate Change themes. Indeed, a recent Science and Technology Committee report to the House of Commons about investigating the oceans highlighted the importance of "blue skies research" in marine science. It is clear as we move into an era in which environmental sustainability is a key concern, that science that addresses ecosystem sustainability issues is of great interest to the general public and relevant to policy makers, industry, economists and social scientists. Decisions taken by policymakers, for example in the Department of Energy and Climate Change (DECC), are informed by research into microbial ecology as microbial activity has continuous and far-reaching effects on the climate.
An important impact of this project on policy will be the delivery of a more accurate, physiologically-based (and therefore more reliable) version of the European Regional Seas Ecosystem Model (ERSEM). This will be able to properly simulate the extant ocean carbon cycle and to reliably test future scenarios hypotheses. Such models are increasingly required by scientific organizations such as the Intergovernmental Panel for Climate Change (IPCC), which aim to inform policy makers' decisions in relation to marine ecosystem management. ERSEM is already used by the National Centre for Ocean Forecasting (NCOF) and 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. All these organizations (and their stakeholders) will therefore benefit from the outcomes of this project. 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.
Industry is actively looking for scientific breakthroughs that can support innovative mechanisms of carbon sequestration. Thus, whilst the results of this project will primarily provide fundamentally new knowledge on predator-prey interactions, and particularly the relationship between photosynthesis and cyanophage infection, more generally the work will help to explain how viruses shape the function of a key component of the marine microbial community. In so doing, new insights into mechanisms controlling the CO2 fixation potential of these organisms will be elucidated, which has implications for efficiencies of trophic transfer of carbon and hence of carbon sequestration mechanisms.
A variety of methods will be used to engage with end-users, including a detailed project website, regular updates in social media (such as PML and Warwick's twitter accounts https://twitter.com/PMLGroup; https://twitter.com/WarwickLifeSci), publications in popular magazines (e.g. Planet Earth), and visits and exhibitions at local schools.
An important impact of this project on policy will be the delivery of a more accurate, physiologically-based (and therefore more reliable) version of the European Regional Seas Ecosystem Model (ERSEM). This will be able to properly simulate the extant ocean carbon cycle and to reliably test future scenarios hypotheses. Such models are increasingly required by scientific organizations such as the Intergovernmental Panel for Climate Change (IPCC), which aim to inform policy makers' decisions in relation to marine ecosystem management. ERSEM is already used by the National Centre for Ocean Forecasting (NCOF) and 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. All these organizations (and their stakeholders) will therefore benefit from the outcomes of this project. 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.
Industry is actively looking for scientific breakthroughs that can support innovative mechanisms of carbon sequestration. Thus, whilst the results of this project will primarily provide fundamentally new knowledge on predator-prey interactions, and particularly the relationship between photosynthesis and cyanophage infection, more generally the work will help to explain how viruses shape the function of a key component of the marine microbial community. In so doing, new insights into mechanisms controlling the CO2 fixation potential of these organisms will be elucidated, which has implications for efficiencies of trophic transfer of carbon and hence of carbon sequestration mechanisms.
A variety of methods will be used to engage with end-users, including a detailed project website, regular updates in social media (such as PML and Warwick's twitter accounts https://twitter.com/PMLGroup; https://twitter.com/WarwickLifeSci), publications in popular magazines (e.g. Planet Earth), and visits and exhibitions at local schools.
People |
ORCID iD |
Luca Polimene (Principal Investigator) | |
Ruth Airs (Co-Investigator) |
Publications

Archer S
(2017)
Limitation of dimethylsulfoniopropionate synthesis at high irradiance in natural phytoplankton communities of the Tropical Atlantic
in Limnology and Oceanography

Barlow R
(2023)
Latitudinal variability and adaptation of phytoplankton in the Atlantic Ocean
in Journal of Marine Systems

Brotas V
(2022)
Complementary Approaches to Assess Phytoplankton Groups and Size Classes on a Long Transect in the Atlantic Ocean
in Frontiers in Marine Science

Kwon Y
(2020)
A marine carbon monoxide (CO) model with a new parameterization of microbial oxidation
in Ecological Modelling

Leles S
(2021)
Differences in physiology explain succession of mixoplankton functional types and affect carbon fluxes in temperate seas
in Progress in Oceanography

Llewellyn CA
(2020)
Synthesis, Regulation and Degradation of Carotenoids Under Low Level UV-B Radiation in the Filamentous Cyanobacterium Chlorogloeopsis fritschii PCC 6912.
in Frontiers in microbiology

Sabadel A
(2017)
Determination of picomolar dissolved free amino acids along a South Atlantic transect using reversed-phase high-performance liquid chromatography
in Marine Chemistry

Steele DJ
(2018)
Occurrence of chlorophyll allomers during virus-induced mortality and population decline in the ubiquitous picoeukaryote Ostreococcus tauri.
in Environmental microbiology

Sun X
(2023)
Coupling ecological concepts with an ocean-colour model: Phytoplankton size structure
in Remote Sensing of Environment

Valente A
(2022)
A compilation of global bio-optical in situ data for ocean colour satellite applications - version three
in Earth System Science Data
Description | In this project we have developed a new model formulation describing viral lysis in phytoplankton. The new formulation is based on experimental evidences suggesting the virus activity is proportional to the growth rate of the phytoplankton host. This implies that viral lysis is reduced under nutrient limitation which negatively affects phytoplankton net growth. When implemented in a widely used marine ecosystem model (ERSEM), the new formulation significantly change the simulations of gross primary production, bacteria and dissolved organic carbon (DOC) dynamics in a reference oligotrophic system (the Bermuda Atlantic Time Series station). These results might lead to a reparameterization and recalibration of the ERSEM model, potentially improving its capability to simulate important aspects (e.g. carbon fixation and DOC production) of the marine carbon cycle. |
Exploitation Route | After appropriate tests and publication, the new model formulation will be integrated in the ERSEM version publicly available to the scientific community |
Sectors | Education Environment |
Description | Elucidating the consequences of picocyanobacterial lipid remodelling for global marine primary production estimates |
Amount | £174,533 (GBP) |
Funding ID | NE/V000462/1 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 03/2021 |
End | 10/2024 |
Description | NERC Discovery |
Amount | £800,000 (GBP) |
Funding ID | NE/R010382/1 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 04/2018 |
End | 04/2021 |
Title | Design of sampling protocols |
Description | Protocols for sampling for particulate organic nitrogen, particulate organic phosphorus, CHN, and pigments designed, documented and shared with project team in Warwick. |
Type Of Material | Technology assay or reagent |
Year Produced | 2017 |
Provided To Others? | Yes |
Impact | Design and recording of protocols ensures sampling conducted according to best practice. |
Title | Synechecoccus cell numbers required for POC/PON |
Description | We have determined the number of Synececoccus cells required to obtain reliable data for POC/PON measurements |
Type Of Material | Technology assay or reagent |
Year Produced | 2017 |
Provided To Others? | No |
Impact | This research enables design and implementation of experiments within the project. |
Title | Synechecoccus cell numbers required for pigments analysis |
Description | We have determined the number of Synechococcus cells required from experiments to obtain reliable pigment data from HPLC analysis. |
Type Of Material | Technology assay or reagent |
Year Produced | 2017 |
Provided To Others? | No |
Impact | This research enables project experiments to be designed and carried out. |
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 | Model Simulations at BATS |
Description | The European Regional Seas Ecosystem Model (ERSEM) was implemented at the BATS site in the Sargasso Sea. The model was run with and without the formulation describing viral lysis on phytoplankton. Simulation were compared with in situ primary production (C14) data |
Type Of Material | Computer model/algorithm |
Year Produced | 2019 |
Provided To Others? | No |
Impact | This exercise provided a preliminary assessment of the effect of the current parameterization of phytoplankton lysis on model primary production |
Title | Model simulating cyanobacteria growth dynamics in a chemostat |
Description | The primary producers module of the European Regional Seas Ecosystem Model has been adapted to simulate growth dynamics of cyanobacteria in a chemostat. The model is meant to reproduce different cellular physiological conditions (e.g. nutrient and light limitation) and to relate them to the mortality rate induced by viral infection |
Type Of Material | Computer model/algorithm |
Year Produced | 2018 |
Provided To Others? | No |
Impact | The model will be used to develop a robust (experimentally based) formulation describing the effect of the host nutritional status on viral infection. |
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 | Bergen collaboration |
Organisation | Spanish National Research Council (CSIC) |
Department | Institute of Marine Sciences |
Country | Spain |
Sector | Public |
PI Contribution | Shipping of kit to Bergen for experiment. Analysis of samples for N-osmolytes. Data interpretation. |
Collaborator Contribution | Sampling opportunity in international Bergen experiment looking at biological and physical control of trace gas and precursor production. |
Impact | Still in progress |
Start Year | 2017 |
Description | "Closer Look" film for BBC Countryfile |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Public/other audiences |
Results and Impact | Footage prepared with Countryfile team, covered local water based activities in the Southwest, well being and marine science. |
Year(s) Of Engagement Activity | 2020 |