Cyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant marine photosynthetic prokaryotes. Cyanophages, viruses infecting cyanobacteria, are a major cause of bacterial mortality, affecting cyanobacterial evolution and ecology. An open question regarding the ecology of cyanophages is how different hosts shape viral evolution. To investigate this, we conducted a long-term evolutionary experiment to reveal the genomic basis for the adaptation of marine cyanophages to different hosts.
We used a single cyanophage isolate as the ancestor for a viral population which was used to infect three different cyanobacterial hosts: WH8102 (Synechococcus), MED4 (Prochlorococcus) and MIT9515 (Prochlorococcus). We cultured the viral populations for a year, at the presence of naïve bacterial hosts, to avoid co-evolutionary dynamics. We sequenced and analyzed DNA of evolved viral populations, accompanied by fitness assays.
Our analysis indicates that the ancestral population infects MIT9515 most efficiently and is less adapted to WH8102. Throughout the evolutionary course populations adapted to their corresponding hosts, in part at the cost of narrowing their host range. Mutations accumulated mostly in genes responsible for phage-host attachment. Clustering of the viral populations, according to their pairwise genetic distance and to their phenotypic profiles, show that populations evolved on MIT9515 are highly similar to the ancestral phage, and that populations that evolved on other hosts have diverged to alternative trajectories.
Based on our results, we suggest that increase in the abundance of non-optimal cyanobacterial hosts can act as a driver of diversifying viral evolution, leading to the emergence of distinct viral sub-populations.