Prevalence of Viral Frequency-Dependent Infection in Coastal Marine Prokaryotes Revealed Using Monthly Time Series Virome Analysis

Abstract

ABSTRACT Viruses infecting marine prokaryotes have a large impact on the diversity and dynamics of their hosts. Model systems suggest that viral infection is frequency dependent and constrained by the virus-host encounter rate. However, it is unclear whether frequency-dependent infection is pervasive among the abundant prokaryotic populations with different temporal dynamics. To address this question, we performed a comparison of prokaryotic and viral communities using 16S rRNA amplicon and virome sequencing based on samples collected monthly for 2 years at a Japanese coastal site, Osaka Bay. Concurrent seasonal shifts observed in prokaryotic and viral community dynamics indicated that the abundance of viruses correlated with that of their predicted host phyla (or classes). Cooccurrence network analysis between abundant prokaryotes and viruses revealed 6,423 cooccurring pairs, suggesting a tight coupling of host and viral abundances and their “one-to-many” correspondence. Although stable dominant species, such as SAR11, showed few cooccurring viruses, a fast succession of their viruses suggests that viruses infecting these populations changed continuously. Our results suggest that frequency-dependent viral infection prevails in coastal marine prokaryotes regardless of host taxa and temporal dynamics. IMPORTANCE There is little room for doubt that viral infection is prevalent among abundant marine prokaryotes regardless of their taxa or growth strategy. However, comprehensive evaluations of viral infections in natural prokaryotic communities are still technically difficult. In this study, we examined viral infection in abundant prokaryotes by monitoring the monthly dynamics of prokaryotic and viral communities at a eutrophic coastal site, Osaka Bay. We compared the community dynamics of viruses with those of their putative hosts based on genome-based in silico host prediction. We observed frequent cooccurrence among the predicted virus-host pairs, suggesting that viral infection is prevalent in abundant prokaryotes regardless of their taxa or temporal dynamics. This likely indicates that frequent lysis of the abundant prokaryotes via viral infection has a considerable contribution to the biogeochemical cycling and maintenance of prokaryotic community diversity.

Keywords

• frequency-dependent selection
• K/r strategy
• marine prokaryotes
• marine viruses
• virome