Revealing a mechanistic understanding of the role of viruses and host nutrient status in modulating CO2 fixation in key marine phototrophs

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.

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.