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

Abstract

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 (~40% each), while cellular fraction metagenomes had mostly sporadic species (~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.

TrackingMicrocystisviruses and infection dynamics across distinct phases of aMicrocystis-dominated bloom

“…4A). In contrast, non-colony associated hosts may sustain infection relationships with more members of the viral “seed bank”, 8,14,23 thus maintaining a higher overall Microcystis vOTU assemblage diversity.…”

“…This trend of majority low abundance and few high abundance populations is common in microbial virus assemblages, which tend to have long tailed rank-abundance curves like their bacterial and archaeal hosts. 10,14,49 The top most numerically abundant Microcystis vOTUs that emerged on the bloom peaks (labeled in Fig. 2A-B) are discussed in the context of assemblage evenness and turnover in later sections.…”

Contrasting drivers of abundant phage and prokaryotic communities revealed in diverse coastal ecosystems

“…1 ). Although most known phages are smaller than 0.22 µm, viral sequences comprised a substantial portion of the classified reads in these samples (Supplementary Dataset 1 ; average of 23.7%, 3.57% average of total reads), and phages in cellular size fractions of other studies have been shown to correspond to an abundant and putatively active subset of the total phage community [ 16 , 17 ]. We thus referred to the phages of this study as belonging to the abundant subset of the total phage community.…”

“…Our analysis focused on the phages of the Caudoviricetes class as representative of phage patterns due to the very few representatives of other types of phages in the data. These Caudoviricetes phages were detected in a cellular fraction of seawater (>0.22 µm), which is known to exclude some rare but persistent viruses of the environment [ 9 , 17 ] but nevertheless corresponds to the abundant and potentially active or lysogenic subset of the phage community which may be responsible for the infective interactions that drive prokaryotic communities [ 16 ]. Considering these phages are potentially more directly interacting with the prokaryotic community than those in the viral fraction, we expected that phage community patterns would closely align with that of prokaryotes.…”

“…We focused on phages detected in metagenomes of cellular size fractions of seawater (>0.22 µm), as they represent the putatively abundant or active members of the phage community as indicated in previous studies [ 16 , 17 ]. Given the intrinsic link of phages to their hosts, our null hypothesis was that factors shaping the communities of these abundant phages would mirror those shaping prokaryotic communities, and this similarity would be most visible at global scales between the oceans since the spatial separation and chemical differences between oceans are so large.…”