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Variability and host density independence in inductions-based estimates of environmental lysogeny

Nature Microbiology volume 2, Article number: 17064 (2017) Cite this article

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Abstract

Temperate bacterial viruses (phages) may enter a symbiosis with their host cell, forming a unit called a lysogen. Infection and viral replication are disassociated in lysogens until an induction event such as DNA damage occurs, triggering viral-mediated lysis. The lysogen–lytic viral reproduction switch is central to viral ecology, with diverse ecosystem impacts. It has been argued that lysogeny is favoured in phages at low host densities. This paradigm is based on the fraction of chemically inducible cells (FCIC) lysogeny proxy determined using DNA-damaging mitomycin C inductions. Contrary to the established paradigm, a survey of 39 inductions publications found FCIC to be highly variable and pervasively insensitive to bacterial host density at global, within-environment and within-study levels. Attempts to determine the source(s) of variability highlighted the inherent complications in using the FCIC proxy in mixed communities, including dissociation between rates of lysogeny and FCIC values. Ultimately, FCIC studies do not provide robust measures of lysogeny or consistent evidence of either positive or negative host density dependence to the lytic–lysogenic switch. Other metrics are therefore needed to understand the drivers of the lytic–lysogenic decision in viral communities and to test models of the host density-dependent viral lytic–lysogenic switch.

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Figure 1: Locations and global linear regression of data from meta-analysis of 39 published studies based on chemical induction of lysogens.
Figure 2: Reported fractions of chemically inducible cells (FCIC, %) in freshwater, saltwater and sediment environments, showing a lack of negative host density dependence, and soils, showing positive host density dependence (cells per ml or g of sample).
Figure 3: Relationships between FCIC and host density at the within-study level and the truncated distribution of published FCIC values.
Figure 4: FCIC variability between technical replicates, within sites and between sites, with significant impacts of excluding values ≤0 in most sites.
Figure 5: Effect of dilution on variability in FCIC.

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Acknowledgements

The authors thank R. Young for microbiological insight and guidance. Canadian Institute for Advanced Research Integrated Microbial Biodiversity Program Fellowship Award 141679, National Science Foundation grants OISE-1243541 and DEB-1046413, a Gordon and Betty Moore Foundation Investigator Award GBMF-3781 (to F.R.) and National Science Foundation grants OCE-1538567 (to L.W.K.), IOS-1456301 and DEB-1555854 (to M.B.) funded this work. The authors thank G. Gueiros and K. Furby for critiquing the manuscript.

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  1. Ben Knowles

    Present address: †Present address: Department of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, New Jersey 08901, USA.,

Authors and Affiliations

  1. Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Ben Knowles, Lance Boling, Ana Cobián-Güemes, Juris Grasis, Andreas F. Haas, Linda Wegley Kelly, Lauren Paul, Gregory Peters, Nate Robinett, Anca Segall, Cynthia Silveira & Forest Rohwer

  2. Department of Mathematics and Statistics, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Barbara Bailey, Ben Felts, Antoni Luque & Jim Nulton

  3. College of Marine Science, University of South Florida, 140 Seventh Avenue South, St Petersburg, 33701, Florida, USA

    Mya Breitbart

  4. Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, V6T 1Z4, British Columbia, Canada

    Javier del Campo

  5. Computational Science Research Center, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Rob Edwards & Antoni Luque

  6. Department of Computer Science, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Rob Edwards

  7. Viral Information Institute, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Rob Edwards, Antoni Luque, Anca Segall & Forest Rohwer

  8. Department of Mechanical Engineering, San Diego State University, 5500 Campanile Drive, San Diego, 92182, California, USA

    Parag Katira

  9. Scripps Institution of Oceanography, University of California San Diego, 950 Gilman Drive, 92903, California, USA

    Stuart Sandin

  10. Rainbow Rock, Ocean View, 96737, Hawaii, USA

    Merry Youle

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Contributions

B.K. and F.R. designed, conducted and wrote up the study. B.B., L.B., M.B., A.C.-G., J.d.C., R.E., B.F., J.G., A.H., P.K., L.W.K., A.L., J.N., G.P., L.P., N.R., S.S., A.S., C.S. and M.Y. contributed data, analysis and manuscript preparation.

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Correspondence to Ben Knowles or Forest Rohwer.

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Knowles, B., Bailey, B., Boling, L. et al. Variability and host density independence in inductions-based estimates of environmental lysogeny. Nat Microbiol 2, 17064 (2017). https://doi.org/10.1038/nmicrobiol.2017.64

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