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Physiological Interactions between Marine Cyanobacteria and their Viruses

Final Report Summary - PIMCYV (Physiological Interactions between Marine Cyanobacteria and their Viruses)

Cyanobacteria fom the genus Prochlorococcus are extremely abundant in the oceans, as are the viruses (cyanophages) that infect them. How hosts and viruses coexist in nature has remained unclear for many years. Using an experimental evolution approach we selected for cyanobacteria resistant to infection by T7-like podoviruses and used whole genome sequencing to identify the mutations that conferred resistance. This revealed mutations primarily in non-conserved, horizontally transferred genes that localize to a single hypervariable genomic island. Viruses have a diminished capacity to attach to the mutants, indicating altered cell surface properties. The mutations often imposed a fitness cost to the host, manifested by significantly lower growth rates or a previously unrecognized mechanism of hypersensitivity to other viruses. Over time, many of the resistant strains continued to evolve towards an improved growth rate and a narrowing of the resistance range. This indicates that slow-growing resistant strains are likely replaced in the oceans by newly emerging faster growing cells with altered resistant ranges. Surprisingly, counter mutations in phages that enable them to “reinfect” resistant hosts are rare. Therefore we propose that phages retain sufficient hosts for long-term coexistence through both counter-mutations as well as mutations in the host that change their susceptibility to phages, a phenomenon we term “passive host-switching”. Combined, our findings indicate that phages are a selective pressure enhancing the diversity of cell-surface genes found in genomic islands. This diversity emerges as an important genomic mechanism that serves to reduce the effective host population size for infection by a given phage, facilitating long-term coexistence, and leading to a complex and dynamic network of interactions between phages and their cyanobacterial hosts in nature.