Complex temporal dynamics of phage-bacteria populations in an animal-associated marine system

Bacteriophages-bacteria interactions drive rapid evolution of both partners in laboratory studies. To understand how these dynamics unfold in natural environments, we re-sampled a population of Vibrio crassostreae and their phages in an open, animal-associated marine system four years apart. Analysis of over 1000 predominantly virulent phages revealed rapid change of some lineages, but persistence of others, with genomes highly conserved between years. This pattern is consistent with low substitution rates in persistent lineages and may reflect phages overwintering in wild oysters, slow virion decay, and for temperate phages, lysogeny within hosts. Over 600 V. crassostreae strains recovered at both time points assorted into the same major clades. Oyster-associated vibrios have larger genomes and more abundant and diverse mobile genetic elements suggesting that oysters are hotspots for genetic exchange and horizontal gene transfer. Their genomes encode virulence plasmids, prophages carrying anti-phage systems, phage-plasmids, and phage satellites that persist intracellularly as plasmids. Time series analyses revealed weak correlations between phage and bacterial abundances, a pattern compatible with cryptic population dynamics arising from genetic diversity. Together, these results indicate that natural coevolving phage-bacteria populations can exhibit complex dynamics, with rapid replacement of some lineages alongside multi-year persistence of others.