Long-term stability and Red Queen-like strain dynamics in marine viruses

Abstract

Viruses that infect microorganisms dominate marine microbial communities numerically, with impacts ranging from host evolution to global biogeochemical cycles^1,2. However, virus community dynamics, necessary for conceptual and mechanistic model development, remains difficult to assess. Here, we describe the long-term stability of a viral community by analysing the metagenomes of near-surface 0.02-0.2 μm samples from the San Pedro Ocean Time-series³ that were sampled monthly over 5 years. Of 19,907 assembled viral contigs (>5 kb, mean 15 kb), 97% were found in each sample (by >98% ID metagenomic read recruitment) to have relative abundances that ranged over seven orders of magnitude, with limited temporal reordering of rank abundances along with little change in richness. Seasonal variations in viral community composition were superimposed on the overall stability; maximum community similarity occurred at 12-month intervals. Despite the stability of viral genotypic clusters that had 98% sequence identity, viral sequences showed transient variations in single-nucleotide polymorphisms (SNPs) and constant turnover of minor population variants, each rising and falling over a few months, reminiscent of Red Queen dynamics⁴. The rise and fall of variants within populations, interpreted through the perspective of known virus-host interactions⁵, is consistent with the hypothesis that fluctuating selection acts on a microdiverse cloud of strains, and this succession is associated with ever-shifting virus-host defences and counterdefences. This results in long-term virus-host coexistence that is facilitated by perpetually changing minor variants.