Abstract

Viruses are catalysts of biogeochemical cycling, architects of microbial community structure, and terminators of phytoplankton blooms. Viral lysis of diatoms, a key group of eukaryotic phytoplankton, has the potential to impact carbon export and marine food webs. However, the impact of viruses on diatom abundance and community composition is unknown. Diatom-virus dynamics were explored by sampling every month at two coastal and estuarine locations in Washington state, USA resulting in 41 new isolates of the pennate diatom Pseudo-nitzschia and 20 environmental virus samples. We conducted a total of 820 pair-wise crosses of the Pseudo-nitzschia isolates and viral communities. Viral communities infected Pseudo-nitzschia isolates in 8% of the crosses overall and 16% of crosses when the host and viral communities were isolated from the same sample. Isolates ranged in their permissivity to infection with some isolates not infected by any viral samples and others infected by up to 10 viral communities. Isolates that were infected by the most viral communities also had the highest maximum observed viral titers (as high as 16000 infectious units ml-1). Titers of the viral communities were host dependent, as titers for one viral sample on eight different hosts spanned four orders of magnitude. Sequencing of the Pseudo-nitzschia Internal Transcribed Spacer 1 (ITS1) of the revealed multiple subgroups of hosts with 100% ITS1 identities that were infected by different viral communities. Indeed, we repeatedly isolated groups of isolates with identical ITS1 sequences from the same water sample that displayed different viral infection phenotypes. The interactions between Pseudo-nitzschia and the viral communities highlight the diversity of diatoms and emphasize the complexity and variability of diatom-virus dynamics in the ocean.

Highlights

  • In the ocean, viral infection links microbial community structure, biogeochemical cycling, and microbial evolution (Breitbart, 2012)

  • The patterns of virus-Pseudo-nitzschia interactions suggest diatom communities are extraordinarily diverse with respect to their susceptibility to viruses

  • Because viral infection phenotype was not correlated with host phylogeny as we can measure it with the Internal Transcribed Spacer 1 (ITS1) region, methods that estimate community composition or abundance using these markers do not capture the diversity of the community as “seen” by its viral predators

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Summary

Introduction

Viral infection links microbial community structure, biogeochemical cycling, and microbial evolution (Breitbart, 2012). Viruses regulate marine phytoplankton communities by impacting host abundance and diversity through cell lysis (Weitz and Wilhelm, 2012) Viruses and their hosts are thought to cycle dynamically, with encounter rates favoring infection of dominant microbial taxa, which are removed due to lysis and supplanted by new microbial populations that fill the vacant ecological niche (Thingstad, 2000). Waterbury and Valois (1993), when challenging Synechococcus isolates with environmental viral communities, demonstrated that Synechococcus phage titers over 2 years at the same location were not inversely correlated with Synechococcus abundance and were unimportant in controlling co-occurring cyanobacteria populations These divergent results may be due to the small sample sizes of isolation based studies and the timing of host population cycling: isolated hosts may be in the process of being removed by their co-occurring viruses, or they may represent the supplanting microbial population that is resistant to the dominant viruses in the water. Co-occurring resistance and susceptibility fluctuate in Kill-the-Winner dynamics such that both scenarios are plausible

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