Molecular prediction of lytic vs lysogenic states for Microcystis phage: Metatranscriptomic evidence of lysogeny during large bloom events

PLoS One. 2017 Sep 5;12(9):e0184146. doi: 10.1371/journal.pone.0184146. eCollection 2017.

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.

MeSH terms

  • Bacteriophages / genetics*
  • Environment
  • Eutrophication*
  • Gene Expression Profiling
  • Gene Expression Regulation, Viral
  • Genome, Viral
  • Lysogeny / genetics*
  • Microcystis / virology*
  • Phylogeny
  • Transcriptome / genetics*

Grant support

This work was supported by the National Natural Science Foundation of China, grants 41471040 and 41230744 to GG, the Division of Integrative Organismal Systems, grant 1451528 to SWW, the Division of Environmental Biology, grant 1240870 to SWW, the Gordon and Betty Moore Foundation, grant EMS#4971 to SWW and by the Kenneth & Blaire Mossman Endowment to SWW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.