Synergistic Effects of Combined Viral and Protistan Predation on Marine Cyanobacterium Synechococcus Physiology

Sheri Floge, Wake Forest University, Winston-Salem, NC, United States, Cristina Howard-Varona, Ohio State University Main Campus, Microbiology, Columbus, OH, United States, Simon Roux, Joint Genome Institute, Environmental Genomics, Walnut Creek, CA, United States, Benjamin Bowen, Lawrence Berkeley National Laboratory, Joint Genome Institute, Berkeley, United States, Rebecca Lau, Lawrence Berkeley National Lab, Berkeley, CA, United States, Sarah M Schwenck, Scripps Institution of Oceanography, La Jolla, CA, United States, Samuel Schwartz, Wake Forest University, Biochemistry and Molecular Biology, Winston-Salem, NC, United States, Tanja Woyke, DOE Joint Genome Institute, Walnut Creek, CA, United States, Trent Northen, Lawrence Berkeley National Laboratory, Berkeley, United States and Matthew B Sullivan, Ohio State University Main Campus, Microbiology, Columbus, United States
The fate of carbon in ocean ecosystems is controlled by myriad individual interactions within a highly interconnected planktonic food web, the sheer complexity of which has hindered predictive understanding of global carbon cycling. The marine cyanobacterium, Synechococcus, is one of the most abundant photoautotrophs on the planet and has been implicated, along with it’s viral and protistan predators, as a key player in carbon cycling within oligotrophic ocean waters. While viral impacts on Synechococcus are well studied, little is known about potential antagonistic or synergistic effects of combined predation by viruses and protists. To address this knowledge gap, we used a combination of transcriptomics and metabolomics to examine the response of Synechococcus strain WH8102 to infection by the lytic myovirus S-SSM5, predation by the single-celled dinoflagellate grazer Oxyrrhis marina (CCMP3375) and combined viral and grazer predation. Viral infection resulted in increased expression of genes involved in central carbon metabolism, photosynthesis, and nucleotide metabolism, and the release of a range of dissolved compounds from intact cells during early stages of infection. Among these compounds were nucleotides, amino acids, and B vitamins. While the presence of the grazer alone had no measurable impact upon gene expression, combined viral and grazer predation induced transcriptional changes in excess of those observed with viral infection alone. Our data suggest that the combined effects of viral and grazer predation can be greater than the sum of individual interactions and illustrate the importance of understanding net impacts of multiple microbial interactions when linking cellular physiology to global scale biogeochemical processes.