Abstract

Temperate phages are viruses of bacteria that can establish two types of infection: a lysogenic infection in which the virus replicates with the host cell without producing virions, and a lytic infection where the host cell is eventually destroyed, and new virions are released. While both lytic and lysogenic infections are routinely observed in the environment, the ecological and evolutionary processes regulating these viral dynamics are still not well understood, especially for uncultivated virus-host pairs. Here, we characterized the long-term dynamics of uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake (Trout Bog Lake, TBL). As no GSB virus has been formally described yet, we first used two complementary approaches to identify new GSB viruses from TBL; one in vitro based on flow cytometry cell sorting, the other in silico based on CRISPR spacer sequences. We then took advantage of existing TBL metagenomes covering the 2005–2018 period to examine the interactions between GSB and their viruses across years and seasons. From our data, GSB populations in TBL were constantly associated with at least 2-8 viruses each, including both lytic and temperate phages. The dominant GSB population in particular was consistently associated with two prophages with a nearly 100% infection rate for >10 years. We illustrate with a theoretical model that such an interaction can be stable given a low, but persistent, level of prophage induction in low-diversity host populations. Overall, our data suggest that lytic and lysogenic viruses can readily co-infect the same host population, and that host strain-level diversity might be an important factor controlling virus-host dynamics including lytic/lysogeny switch.

Highlights

  • Recent advances in metagenome sequencing have enabled high-throughput exploration of the virosphere, leading to a Supplementary information The online version of this article contains supplementary material, which is available to authorized users. * Maureen Berg mberg@lbl.gov * Simon Roux sroux@lbl.gov>200-fold increase in viral genomes available in databases, and uncovering >1,000 new genus-level viral groups [1,2,3,4]

  • We focus on uncultivated viruses infecting green sulfur bacteria (GSB) in a model freshwater lake (Trout Bog Lake, TBL) sampled from 2005 to 2018 by the North Temperate Lakes Microbial Observatory

  • While other bacteria could potentially display fluorescence profiles similar to GSB, targeted metagenomes sequenced from cells identified as “GSB-like” by Fluorescence Activated Cell Sorting (FACS) were near-exclusively composed of GSB sequences, supporting our use of FACS data as a measurement for GSB abundance

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Summary

Introduction

>200-fold increase in viral genomes available in databases, and uncovering >1,000 new genus-level viral groups [1,2,3,4]. The “kill the winner” model places importance on the lytic life stage of viruses, and proposes that when a host is actively growing, host population numbers increase, and lytic infections will be favored over lysogenic infections [15]. In this scenario, lytic viruses suppress host blooms, and maintain diversity in the host population by preventing one host strain from outcompeting all others [9, 16]. We highlight through direct observation and theoretical modeling that host strain-level diversity may be a critical parameter driving these virus-host dynamics

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