The methylotrophic OM43 clade are Gammaproteobacteria that comprise some of the smallest free-living cells known and have highly streamlined genomes. OM43 represents an important microbial link between marine primary production and remineralization of carbon back to the atmosphere. Bacteriophages shape microbial communities and are major drivers of mortality and global marine biogeochemistry. Recent cultivation efforts have brought the first viruses infecting members of the OM43 clade into culture. Here, we characterize a novel myophage infecting OM43 called Melnitz. Melnitz was isolated independently from water samples from a subtropical ocean gyre (Sargasso Sea) and temperate coastal (Western English Channel) systems. Metagenomic recruitment from global ocean viromes confirmed that Melnitz is globally ubiquitous, congruent with patterns of host abundance. Bacteria with streamlined genomes such as OM43 and the globally dominant SAR11 clade use riboswitches as an efficient method to regulate metabolism. Melnitz encodes a two-piece tmRNA (ssrA), controlled by a glutamine riboswitch, providing evidence that riboswitch use also occurs for regulation during phage infection of streamlined heterotrophs. Virally encoded tRNAs and ssrA found in Melnitz were phylogenetically more closely related to those found within the alphaproteobacterial SAR11 clade and their associated myophages than those within their gammaproteobacterial hosts. This suggests the possibility of an ancestral host transition event between SAR11 and OM43. Melnitz and a related myophage that infects SAR11 were unable to infect hosts of the SAR11 and OM43, respectively, suggesting host transition rather than a broadening of host range. IMPORTANCE Isolation and cultivation of viruses are the foundations on which the mechanistic understanding of virus-host interactions and parameterization of bioinformatic tools for viral ecology are based. This study isolated and characterized the first myophage known to infect the OM43 clade, expanding our knowledge of this understudied group of microbes. The nearly identical genomes of four strains of Melnitz isolated from different marine provinces and the global abundance estimations from metagenomic data suggest that this viral population is globally ubiquitous. Genome analysis revealed several unusual features in Melnitz and related genomes recovered from viromes, such as a curli operon and virally encoded tmRNA controlled by a glutamine riboswitch, neither of which are found in the host. Further phylogenetic analysis of shared genes indicates that this group of viruses infecting the gammaproteobacterial OM43 shares a recent common ancestor with viruses infecting the abundant alphaproteobacterial SAR11 clade. Host ranges are affected by compatible cell surface receptors, successful circumvention of superinfection exclusion systems, and the presence of required accessory proteins, which typically limits phages to singular narrow groups of closely related bacterial hosts. This study provides intriguing evidence that for streamlined heterotrophic bacteria, virus-host transitioning may not be necessarily restricted to phylogenetically related hosts but is a function of shared physical and biochemical properties of the cell.

70% of the world’s surface is covered by oceans; its impact on the global carbon cycle, climate change, and acid-base biochemistry remain crucial to our understanding of the natural world. The oceans act as important buffers against climate change, absorbing 25% of anthropogenic carbon and over 90% of rising temperatures. 90% of the ocean’s biomass is composed of marine microorganisms and their impact on global systems, particularly in the face of anthropogenic climate change, remains an active area of research. Marine microorganisms are critical in the energy cycle and are the foundation for marine life. Warmer waters have led to increasingly stratified and nutrient-depleted water masses at the ocean surface, favouring low-nutrient microbial specialists. One group of these, known as the SAR11 clade, comprise up to 40% of the microbial community and are estimated to convert up to 20% of all global primary production back to atmospheric CO2 as well as being an important biological source of methane. Increasing SAR11 abundance in warming oceans and concomitant increases in remineralisation of CO 2 and methane may create a positive feedback loop for global warming.

A potential brake on the influence of SAR11 carbon remineralisation is their associated viruses, which are predicted to lyse up to 20% of cellular biomass daily. These viruses also encode an enormous array of genetic diversity and its relationship with both physical and biological factors is key to understanding the marine biome’s population dynamics. Predation of cells by viruses is a major driver of carbon export to the deep ocean, but our knowledge of these interactions in the SAR11 clade is limited, in part due to the paucity of host-virus model systems for this clade.

However, studying these microorganisms remains challenging since only a few SAR11 strains have been isolated and cultured for in vitro experimentation. Alternative study methods include obtaining genomes via metagenomics studies and Single-cell Amplified Genomes (SAGs). Therefore, the goal of this project is to extract and explore SAR11 host and associated phage genomes from metagenomic and SAG data. Here, I present a study of 451 SAGs collected from the Tara Ocean expeditions and twelve prokaryotic metagenomic samples from the Bermuda Atlantic Time Series (BATS).

Overall, I summarise the difficulty of obtaining contiguous and high-quality SAR11 genomes from metagenomic data. I conclude possible reasons why existing bioinformatics tools are ineffective at recovering such sequences and suggest improvements through long-read technology. Through SAG data, I identified and evaluated genomic regions associated with phage defence to improve our understanding of SAR11-associated viral dynamics in the oceans. Additionally, I characterised two previously undescribed clades of SAR11, both phylogenetically and ecologically. Our 451 SAGS contained fewer phage sequences than SAGs from other taxa, indicating the SAR11 clade does not conform to the expected statement that 20% of all marine microorganisms are infected at any given time. Lastly, I confirmed that a hypervariable region identified as a putative site for host-virus Red Queen dynamics is present within all clades of SAR11, and concluded these regions are enriched in genes related to cell wall biosynthesis. I hypothesise that these genes are related to phage defence, altering the cell wall receptors and preventing recognition of a host by SAR11 phages, therefore resisting infection. These findings together increase our understanding of additional host-phage interactions SAR11 has and impact current models when calculating SAR11 phage carbon-sequestering via the viral shunt.