Host/virus interactions in the marine cyanobacterium prochlorococcus

Abstract

Bacterial viruses shape the diversity, metabolic function, and community dynamics of their microbial hosts. As microbes drive many major biogeochemical cycles, viral infection is therefore a phenomenon of global significance. A significant fraction of primary production in the oceans is performed by the picocyanobacteria Prochlorococcus and Synechococcus. The viruses ('cyanophages') that infect these cyanobacteria are unusual in that their genomes contain a large suite of orthologs to host metabolic genes. These orthologs, known as 'auxiliary metabolic genes' ('AMGs'), encode proteins involved in diverse cellular processes, including photosynthesis, carbon and phosphate metabolism, and nucleotide synthesis. They are thought to benefit phage during infection by redirecting host metabolism towards pathways that promote viral replication. While AMGs are widespread in two Prochlorococcus cyanophage families, the podoviruses and myoviruses, they are rare or completely absent in the third family, the siphoviruses. The overarching goal of this thesis is to understand differences in the infection processes of different cyanophages - in particular, between cyanophages that encode AMGs and those that do not. We hypothesize that the latter group utilizes a fundamentally different infection strategy than AMG-encoding cyanophages, and offer several lines of evidence to support this hypothesis. First, we show that siphoviruses that lack AMGs have highly productive infections, and that host photosynthesis is not impaired during infection. This result is somewhat surprising, as evidence suggests that photosynthesis is supported by AMG-encoded proteins during infection by other cyanophages; however, it is consistent with our observations that unlike the podo- and myoviruses, the siphoviruses do not degrade the host genome during infection, and that the host response to siphovirus infection parallels the metabolic changes effected by AMGs in other cyanophages. These results, along with patterns of siphovirus infection kinetics over the diel light cycle, suggest that siphoviruses utilize a mode of infection that is based on modulating, rather than suppressing, host transcription. Finally, we argue that the suite of metabolic changes that occur during siphovirus infection - and that are effected by AMGs in other cyanophages - are induced by a nitrogen-stress-like response in the host during infection, offering new insights into cyanophage/host coevolution.