VIRAL GENOMIC DIVERSITY AND THE EVOLUTION OF HOST RESISTANCE IN MICROMONAS-VIRUS SYSTEMS FROM THE TROPICAL NORTH PACIFIC OCEAN
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2024
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Abstract
Viruses in the ocean outnumber microbes by approximately an order of magnitude. These pathogens shape microbial communities via manipulation of host metabolism, through the mortality of host cells, and by causing evolutionary change in the host population. While the dynamics of cyanobacteria and their phages have provided a foundation of knowledge on coevolutionary dynamics through the lens of genetics and phenotypic selection, there is a smaller foundation for marine eukaryotic phytoplankton and their associated viruses. The important role of eukaryotic phytoplankton in marine primary production and biogeochemical cycling merits further investigations into how these phytoplankton interact with their pathogens. The question of how viruses evolve to successfully infect their hosts may be answered in part by examination of viral gene content and the evolutionary origins of such genes. Furthermore, virus-induced mortality selects for host phenotypes that are resistant to lysis. It has been hypothesized that the evolution of resistance results in a fitness cost that could alter phytoplankton productivity, but the magnitude of this cost, and how it varies under different resource regimes, is not clear. Such selection is presumably tied to genomic change in resistant cells, but resistance mutations and their mechanistic effects are poorly understood. We sought to examine questions on the dynamics of marine viruses infecting eukaryotic hosts using isolates of the common and ecologically relevant alga Micromonas commoda and strains of its double-stranded DNA viruses in the genus Prasinovirus. These isolates represent the first prasinophyte-prasinovirus systems isolated from the North Pacific Subtropical Gyre. Through four new genomic assemblies of Micromonas commoda virus strains, we found 61 putative genes not seen in other prasinoviruses. Additionally, 192 putative genes varied in occurrence among the four virus strains, despite the fact that they have overlapping host ranges. Across prasinoviruses, 25% of gene content is strongly correlated with host genus, and the functions of these genes suggests that successful lytic infection is achieved through a diversity of genetic strategies. We subsequently used experimental evolution to create 88 resistant M. commoda cell lines and found a large decrease in fitness, particularly when cells were grown at a higher light level. This fitness cost attenuated after 15 months even while cell populations maintained resistance, suggesting compensatory mutations can ameliorate the cost of resisting infection. The genomes of resistant cell lines had a larger number of non-synonymous variants than susceptible control lines. The genes affected by such variants were dependent on the identity of the ancestral cell line, and indicated a diverse suite of mechanisms of resistance among closely related isolates. Both resistance mutations and viral gene content imply that host stress responses, such as programmed cell death, are an important site of coevolutionary antagonism, as are genes potentially related to viral attachment and entry. This work demonstrates a complex network of coevolutionary strategies among marine eukaryotes and their viruses.
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Biological oceanography, cost of resistance, host-pathogen interaction, narine virus, virus of eukaryotes
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139 pages
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