Tracing Interactions Between Picophytoplankton and Phage Through Dissolved Organic Matter

Abstract

This thesis explores for the first time how the mechanism of dissolved organic matter (DOM) release from the biomass of abundant marine phytoplanktons - exudation, mechanical lysis or viral lysis - affects the composition of the released DOM. Experiments were carried out both in lab conditions and in a field-based incubation. For lab culture experiments, two model systems were explored separately: \emph{Synechococcus} WH7803 and phage S-SM1, and \emph{Prochlorococcus} MED4 and phage PHM2. We performed these molecular composition measurements using a broad, untargeted high-resolution mass spectrometry approach, and analyzed the large resulting dataset with a novel computational pipeline that revealed the molecular features that make each of the three types of DOM compositionally distinct. For the \emph{Synechococcus} experiment in particular, we find evidence that the picocyanobacterium \emph{Synechococcus} WH7803, releases a set of unsaturated, oxygen-rich and possibly novel biomolecules into the DOM. When lysed by the virus S-SM1, abundant peptides derived from specific proteolysis of the major light-harvesting protein phycoerythrin are released, implicating phage infection of these abundant cyanobacteria as a potentially major source of dissolved organic nitrogen compounds in the oligotrophic surface ocean. For the other model marine phytoplankton - \emph{Prochlorococcus} MED4, peptides related to photosynthesis were found in its exudate as compared to its mechanical lysate and viral lysate. For the 48-hour field incubation experiment, phosphorus concentration and different seawater types were controlled to explore the dynamics of nutrient-virus-phytoplankton interactions. Decrease of viral content in the seawater and phosphorus addition had the most effect on the microbial community structure as indicated by 16S RNA while only viral concentration had a pronounced impact on the DOM composition. Together, these evidence indicates that DOM released from phytoplankton via three modes - exudation, mechanical lysis and viral lysis is compositionally distinct. Controlled cyanobacteria-virus interactions reveal potentially overlooked compound groups in the natural environment and such compounds could serve as future biomarkers.