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Temperate infection in a virus-host system previously known for virulent dynamics.

ABSTRACT: The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate phase in healthy hosts to a lethal lytic stage as host cells become physiologically stressed. Using this system as a model for temperate infection dynamics, we present a template to diagnose temperate infection in other virus-host systems by integrating experimental, theoretical, and environmental approaches. Finding temperate dynamics in such an established virulent host-virus model system indicates that temperateness may be more pervasive than previously considered, and that the role of viruses in bloom formation and decline may be governed by host physiology rather than by host-virus densities.

SUBMITTER: Knowles B

PROVIDER: S-EPMC7493887 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Temperate infection in a virus-host system previously known for virulent dynamics.

Knowles Ben B Bonachela Juan A JA Behrenfeld Michael J MJ Bondoc Karen G KG Cael B B BB Carlson Craig A CA Cieslik Nick N Diaz Ben B Fuchs Heidi L HL Graff Jason R JR Grasis Juris A JA Halsey Kimberly H KH Haramaty Liti L Johns Christopher T CT Natale Frank F Nissimov Jozef I JI Schieler Brittany B Thamatrakoln Kimberlee K Frede Thingstad T T Våge Selina S Watkins Cliff C Westberry Toby K TK Bidle Kay D KD

Nature communications 20200915 1

The blooming cosmopolitan coccolithophore Emiliania huxleyi and its viruses (EhVs) are a model for density-dependent virulent dynamics. EhVs commonly exhibit rapid viral reproduction and drive host death in high-density laboratory cultures and mesocosms that simulate blooms. Here we show that this system exhibits physiology-dependent temperate dynamics at environmentally relevant E. huxleyi host densities rather than virulent dynamics, with viruses switching from a long-term non-lethal temperate ...[more]

PMID: 32934228

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Project description:Positive single-strand ribonucleic acid [(+)ssRNA] viruses can cause multiple outbreaks, for which comprehensive tailored therapeutic strategies are still missing. Virus and host cell dynamics are tightly connected, generating a complex dynamics that conveys in virion assembly to ensure virus spread in the body. Starting from the knowledge of relevant processes in (+ss)RNA virus replication, transcription, translation, virions budding and shedding, and their respective energy costs, we built up a systems thinking (ST)-based diagram of the virus-host interaction, comprehensive of stocks, flows, and processes as well-described in literature. In ST approach, stocks and flows are expressed by a proxy of the energy embedded and transmitted, respectively, whereas processes are referred to the energy required for the system functioning. In this perspective, healthiness is just a particular configuration, in which stocks relevant for the system (equivalent but not limited to proteins, RNA, DNA, and all metabolites required for the survival) are constant, and the system behavior is stationary. At time of infection, the presence of additional stocks (e.g., viral protein and RNA and all metabolites required for virion assembly and spread) confers a complex network of feedbacks leading to new configurations, which can evolve to maximize the virions stock, thus changing the system structure, output, and purpose. The dynamic trajectories will evolve to achieve a new stationary status, a phenomenon described in microbiology as integration and symbiosis when the system is resilient enough to the changes, or the system may stop functioning and die. Application of external driving forces, acting on processes, can affect the dynamic trajectories adding a further degree of complexity, which can be captured by ST approach, used to address these new configurations. Investigation of system configurations in response to external driving forces acting is developed by computational analysis based on ST diagrams, with the aim at designing novel therapeutic approaches.

Project description:We used microarray analysis to investigate whole genome transcriptome dynamics of the marine cyanobacterium Prochlorococcus sp. strain MED4 and the T7-like podovirus P-SSP7 over a time course during the 8 hour latent period of lytic infection prior to cell lysis. Manuscript Summary: Interactions between bacterial hosts and their viruses (phages) lead to reciprocal genome evolution through a dynamic co-evolutionary process1-5. Phage-mediated transfer of host genes – often located in genome islands – has had a major impact on microbial evolution1, 4, 6. Furthermore, phage genomes have clearly been shaped by the acquisition of genes from their hosts2, 3, 5. Here we investigate whole-genome expression of a host and phage, the marine cyanobacterium Prochlorococcus and a T7-like cyanophage during lytic infection, to gain insight into these co-evolutionary processes. While most of the phage genome was linearly transcribed over the course of infection, 4 phage-encoded bacterial metabolism genes were part of the same expression cluster, even though they are physically separated on the genome. These genes — encoding photosystem II D1 (psbA), high-light inducible protein (hli), transaldolase (talC) and ribonucleotide reductase (nrd) — are transcribed together with phage DNA replication genes and appear to make up a functional unit involved in energy and deoxynucleotide production needed for phage replication in resource-poor oceans. Also unique to this system was the upregulation of numerous genes in the host during infection. These may be host stress response genes, and/or genes induced by the phage. Many of these host genes are located in genome islands and have homologues in cyanophage genomes. We hypothesize that phage have evolved to utilize upregulated host genes, leading to their stable incorporation into phage genomes and their subsequent transfer back to hosts in genome islands. Thus activation of host genes during infection may be directing the co-evolution of gene content in both host and phage genomes. Keywords: time course, viral infection, marine cyanobacteria, podovirus, bacteriophage, stress response

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Temperate infection in a virus-host system previously known for virulent dynamics.

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Temperate infection in a virus-host system previously known for virulent dynamics.

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