Abstract

Microcystis aeruginosa is a freshwater bloom-forming cyanobacterium capable of producing the potent hepatotoxin, microcystin. Despite increased interest in this organism, little is known about the viruses that infect it and drive nutrient mobilization and transfer of genetic material between organisms. The genomic complement of sequenced phage suggests these viruses are capable of integrating into the host genome, though this activity has not been observed in the laboratory. While analyzing RNA-sequence data obtained from Microcystis blooms in Lake Tai (Taihu, China), we observed that a series of lysogeny-associated genes were highly expressed when genes involved in lytic infection were down-regulated. This pattern was consistent, though not always statistically significant, across multiple spatial and temporally distinct samples. For example, samples from Lake Tai (2014) showed a predominance of lytic virus activity from late July through October, while genes associated with lysogeny were strongly expressed in the early months (June–July) and toward the end of bloom season (October). Analyses of whole phage genome expression shows that transcription patterns are shared across sampling locations and that genes consistently clustered by co-expression into lytic and lysogenic groups. Expression of lytic-cycle associated genes was positively correlated to total dissolved nitrogen, ammonium concentration, and salinity. Lysogeny-associated gene expression was positively correlated with pH and total dissolved phosphorous. Our results suggest that lysogeny may be prevalent in Microcystis blooms and support the hypothesis that environmental conditions drive switching between temperate and lytic life cycles during bloom proliferation.

Highlights

  • Viruses are one of the most potent drivers of nutrient cycles, horizontal gene transfer, and microbial evolution in aquatic ecosystems [1, 2]

  • In the remaining 33 samples, 16 showed more abundant expression of gp091 relative to gp135, with a ratio ranging from 1.21 to 79-fold, implying that lytic infection was dominant. These samples were collected during the earlier months (June and July) of the bloom season, with the exception of T09_1, T10_7, and T10_9, which were collected during September and October

  • We surveyed community metatranscriptomes from natural populations of M. aeruginosa at “bloom densities” to describe the physiology and ecology of Microcystis, and in the process identified active phage infections by the Microcystis phage Ma-LMM01. We have analyzed this data in light of available nutrient concentrations, toxin levels, and environmental conditions to predict how lake chemistry and climate influenced Microcystis phage gene expression

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Summary

Introduction

Viruses are one of the most potent drivers of nutrient cycles, horizontal gene transfer, and microbial evolution in aquatic ecosystems [1, 2]. Bacteriophage play an important role in microbial communities by lysing primary producers and heterotrophic bacteria, releasing nutrients from biomass [3] Due to their density-dependent infection, viruses are thought to reduce the competitive advantages of some of the most prolific organisms–the “killthe-winner” hypothesis [4]. Phage genomes can encode auxiliary metabolic genes that serve to augment host metabolism during infection, considerably altering the functional potential of entire populations within the microbial community [5, 6]. Despite their recognized importance, much of the potential of viruses remains uncharacterized, highlighting a crucial need for examination of the role they play across ecosystems. The availability of Ma-LMM01’s full genome sequence has led to analyses of distribution (via PCR and qPCR-based techniques) and some characterization of its genetic regulation [31, 32]

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