Adaptation to sub-optimal hosts is a driver of viral diversification in the ocean
Marine cyanophages are viruses that infect oceanic cyanobacteria, thus affecting global ecological processes. Cyanophages of the Myoviridae family are of great interest since they include generalist viruses capable of infection of a wide range of hosts including those from different cyanobacterial genera. While the influence of phages on host evolution has been studied previously, it is not known how the infection of distinct hosts influences the evolution of cyanophage populations. In marine systems this question is of special interest as the abundance of different Synechococcus and Prochlorococcus hosts constantly changes, temporally and spatially. Here, using an experimental evolution approach, we investigated the adaptation of multiple cyanophage populations to three distinct cyanobacterial hosts. We show that when infecting an \"optimal\" host, whose infection is the most efficient, phage populations accumulated only a few mutations. However, when infecting \"sub-optimal\" hosts, different, largely host-specific sets of mutations, spread in the phage populations, leading to rapid diversification into distinct subpopulations. The mutations included insertions, deletions, SNPs and codon adaptations. Most of the mutations were found in genes encoding for proteins responsible for host recognition, attachment and infection, regardless of their evolutionary conservation. Based on our results, we propose a model demonstrating how shifts in bacterial abundance, which lead to infection of \"sub-optimal\" hosts, act as a driver for rapid diversification of phage populations.