Protistan grazing and viral infection of marine picoplankton: a role for the host cell surface?

The oceans play a major role in determining the world's 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 are also continuously being consumed. There are two major processes that contribute to the consumption of these cells. Firstly, they can be infected and killed by viruses and secondly they can be used as food by small single celled grazing animals called protists. It is the interaction between these two processes of mortality, together with the defence mechanisms that the cyanobacteria have developed, which are the focus of this research project.

We recently observed that a marine Synechococcus strain that was infected with a virus was more susceptible to grazing than the uninfected culture. This distinct preference for preying on phage-infected cells has potentially important ecological implications, as it interferes with phage proliferation by removing infected cells before they burst and could thus indirectly reduce phage abundance.

It is not yet clear what determines the palatability of a prey cell. Cell surface properties are likely to play a role and we have preliminary evidence that lipopolysaccharide (LPS) components of the cell wall are critical in this respect. This proposal will thus compare protist feeding on virus-infected, uninfected and LPS-modified Synechococcus strains in order to specifically elucidate the role of LPS in prey digestibility. Moreover, we will extend our studies to the Atlantic Ocean to investigate whether cultured protists graze differentially on natural Synechococcus populations, and in so doing establish the role of strain selectivity, or preference for cyanophage-infected cells, in this process

Overall, the project will provide fundamentally new mechanistic information on the major biological loss processes that dictate the growth rate and yield of a key marine photoautotroph, information which is critical for defining and understanding controls on marine photosynthesis.

The topic of our research, understanding the mechanism of mortality of a key photosynthetic organism occupying the global ocean has immediate general interest, since the oceans are the largest of the Earth's ecosystems with consequential profound global effects on surface ocean biogeochemistry, including carbon dynamics, as well as the planet's climate. Moreover, the process of biotic mortality is fundamentally important to explaining routes of marine C flow. Furthermore, understanding the underlying mechanisms dictating predator feeding preference, ingestion/digestion of prey and the influence of virus infection on these processes has implications for the survival, replication and distribution of bacterial prey strains in situ and also factors driving bacterial diversity and evolution. Whilst this work is focused on a key environmental microbe these mechanisms are also relevant to the same interactions in bacterial pathogens.

The primary end users of the proposed research will be microbial ecologists working in ocean science, but the work will also be of fundamental use to oceanographers, microbiologists and molecular biologists as well as medical microbiologists and cell biologists. It should be noted that 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 though, as we move into an era in which environmental sustainability is a key concern, that science that addresses ecosystem sustainability issues will be of great interest to the general public and relevant to policy makers, industry, economists and social scientists. The general public is extremely interested in organisms that play a role in C cycling and potentially mediating climate change. 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. Industry is actively looking for scientific breakthroughs that can support innovative mechanisms of carbon sequestration. Thus, whilst the results will primarily provide fundamentally new knowledge on predator-prey interactions, and particularly the relationship between protist grazing and viral infection, more generally the work will help to explain how biotic factors shape the structure of a key component of the marine microbial community. In so doing new insights into mechanisms controlling the growth rate or yield of these organisms will be elucidated, as well as insights into efficiencies of trophic transfer of carbon which has implications for carbon sequestration mechanisms.