The lifestyles of viruses in the sunlit ocean revealed through isolation, genomics, and infection dynamics
Carlson, Michael Curtis Grier
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In the sunlit ocean, heterotrophic and photosynthetic microbes are prey for earth’s most abundant predators. Viruses are regulators of microbial communities, terminating phytoplankton blooms, altering biogeochemical cycles through cell lysis, and driving evolution through horizontal gene transfer. However, viral infection in the marine environment is unquantified. My research seeks understand infection in the ocean through a model marine host-virus system and through coupled studies of virus diversity and gene expression in the field. The model host were diatoms, which contribute to global biogeochemical cycles, form the base of coastal food webs, and account for approximately one fifth of global photosynthesis. The first chapter details the isolation and characterization of a novel virus that infects the toxigenic diatom Pseudo-nitzschia multiseries. The virus had the largest genome of any single stranded DNA (ssDNA) virus isolated, with a gene complement atypical for ssDNA viruses. The virus had a broad host range, infecting hosts from the distantly related centric and pennate diatom groups. The infection dynamics were host dependent, varying orders of magnitude in burst size from 220 to 9,300 viruses cell-1 and between 12-60 hours in latent period. The second chapter assesses the interactions of numerous Pseudo-nitzschia hosts and natural viral communities by isolating 41 new Pseudo-nitzschia and challenging them with 20 environmental virus samples. Pseudo-nitzschia cultures were infected in 8% of the crosses. Viral infectivity intensified during the summer when the most permissive hosts were isolated, and viral communities were most infective of co-occurring hosts. Genotyping of the Pseudo-nitzschia cultures revealed subgroups of genetically identical hosts that were differentially infected suggesting that diatom diversity is an impediment to viral termination of diatom blooms. In the third chapter, viral infection was measured by comparing viral metagenomes to host metatranscriptomes on a coastal to open ocean transect. A small fraction of the total viral population was actively infecting. Viral groups such as the archeoviruses, virophage, and ssDNA viruses had different distributions and were differentially enriched in particle-associated and free-living metatranscriptomes. Viral expression was not correlated with virus to host ratios suggesting that microbial populations were at different stages of infection. Finally, auxiliary metabolic genes in Synechococcus phage were differentially expressed between stations despite similar community composition suggesting that auxiliary genes help viruses succeed under certain conditions. By linking culture based and culture-independent explorations of viral ecology, this research highlights the diversity of viruses in the ocean and the lifestyles that have made them successful.
- Oceanography