From Field Metagenomes to Mutant Genomes: Coevolution of Cyanophages and Synechococcus in Estuarine Ecosystems

Picocyanobacteria, represented by Prochlorococcus and Synechococcus, are major photosynthetic organisms
in aquatic ecosystems, and their viruses (cyanophages) significantly
impact cyanobacterial ecology and evolution. Here, we combined metagenomics
of Synechococcus communities along four representative
estuaries in China and whole-genome analyses of laboratory-evolved Synechococcus mutants to link viral diversity to host adaptation
and evolution. We assembled 83 cyanophage genomes (mainly cyanomyoviruses),
with expanded auxiliary metabolic genes encoding glycosyltransferases
and radical S-adenosyl methionine proteins involved in amino acid
and lipopolysaccharide metabolism. Metagenome-assembled cyanobacterial
genomes revealed mutations predominantly in membrane-associated functions
linked to phage infection. In parallel, we identified genetic pathways
conferring phage resistance in 18 evolved Synechococcus mutant strains that are resistant to phage infection. Notably, mutations
in carbohydrate (rfbA) and photosynthetic energy
transfer (cpeT) of Synechococcus mutants recurred in both cultured isolates and recovered metagenomes.
These results indicate that cyanophages in estuaries leverage broader
metabolic toolkits, while Synechococcus repeatedly
evolves resistance. Together, these findings outline a reciprocal
adaptive landscape that helps explain the persistence and turnover
of picocyanobacterial populations in estuarine environments.