Diverse Marine T4-like Cyanophage Communities Are Primarily Comprised of Low-Abundance Species Including Species with Distinct Seasonal, Persistent, Occasional, or Sporadic Dynamics

Cyanophages exert important top-down controls on their cyanobacteria hosts; however, concurrent analysis of both phage and host populations is needed to better assess phage-host interaction models. We analyzed picocyanobacteria Prochlorococcus and Synechococcus and T4-like cyanophage communities in Pacific Ocean surface waters using five years of monthly viral and cellular fraction metagenomes. Cyanophage communities contained thousands of mostly low-abundance (<2% relative abundance) species with varying temporal dynamics, categorized as seasonally recurring or non-seasonal and occurring persistently, occasionally, or sporadically (detected in >= 85%, 15-85%, or <15% of samples, respectively). Viromes contained mostly seasonal and persistent phages (similar to 40% each), while cellular fraction metagenomes had mostly sporadic species (similar to 50%), reflecting that these sample sets capture different steps of the infection cycle-virions from prior infections or within currently infected cells, respectively. Two groups of seasonal phages correlated to Synechococcus or Prochlorococcus were abundant in spring/summer or fall/winter, respectively. Cyanophages likely have a strong influence on the host community structure, as their communities explained up to 32% of host community variation. These results support how both seasonally recurrent and apparent stochastic processes, likely determined by host availability and different host-range strategies among phages, are critical to phage-host interactions and dynamics, consistent with both the Kill-the-Winner and the Bank models.

Automated summary

Cyanophages play an important role in regulating their cyanobacteria hosts, but combining analysis of both phage and host populations is necessary for understanding their interactions. Through analyzing five years of metagenomic data, we found that cyanophages exhibit temporal dynamics and are categorized into recurring or non-seasonal groups, which occur persistently, occasionally, or sporadically. The seasonal variation in cyanophage communities is influenced by host availability and different host-range strategies among phages, ultimately impacting the structure of the host community. This study supports the importance of considering both seasonal and stochastic processes in phage-host interactions.