When to be temperate: on the fitness benefits of lysis vs. lysogeny

Bacterial viruses, that is ‘bacteriophage’ or ‘phage’, can infect and lyse their bacterial hosts, releasing new viral progeny. In addition to the lytic pathway, certain bacteriophage (i.e. ‘temperate’ bacteriophage) can also initiate lysogeny, a latent mode of infection in which the viral genome is...

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Autores principales: Li, Guanlin, Cortez, Michael H, Dushoff, Jonathan, Weitz, Joshua S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532926/
https://www.ncbi.nlm.nih.gov/pubmed/36204422
http://dx.doi.org/10.1093/ve/veaa042
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author Li, Guanlin
Cortez, Michael H
Dushoff, Jonathan
Weitz, Joshua S
author_facet Li, Guanlin
Cortez, Michael H
Dushoff, Jonathan
Weitz, Joshua S
author_sort Li, Guanlin
collection PubMed
description Bacterial viruses, that is ‘bacteriophage’ or ‘phage’, can infect and lyse their bacterial hosts, releasing new viral progeny. In addition to the lytic pathway, certain bacteriophage (i.e. ‘temperate’ bacteriophage) can also initiate lysogeny, a latent mode of infection in which the viral genome is integrated into and replicated with the bacterial chromosome. Subsequently, the integrated viral genome, that is the ‘prophage’, can induce and restart the lytic pathway. Here, we explore the relationship among infection mode, ecological context, and viral fitness, in essence asking: when should viruses be temperate? To do so, we use network loop analysis to quantify fitness in terms of network paths through the life history of an infectious pathogen that start and end with infected cells. This analysis reveals that temperate strategies, particularly those with direct benefits to cellular fitness, should be favored at low host abundances. This finding applies to a spectrum of mechanistic models of phage–bacteria dynamics spanning both explicit and implicit representations of intra-cellular infection dynamics. However, the same analysis reveals that temperate strategies, in and of themselves, do not provide an advantage when infection imposes a cost to cellular fitness. Hence, we use evolutionary invasion analysis to explore when temperate phage can invade microbial communities with circulating lytic phage. We find that lytic phage can drive down niche competition amongst microbial cells, facilitating the subsequent invasion of latent strategies that increase cellular resistance and/or immunity to infection by lytic viruses—notably this finding holds even when the prophage comes at a direct fitness cost to cellular reproduction. Altogether, our analysis identifies broad ecological conditions that favor latency and provide a principled framework for exploring the impacts of ecological context on both the short- and long-term benefits of being temperate.
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spelling pubmed-95329262022-10-05 When to be temperate: on the fitness benefits of lysis vs. lysogeny Li, Guanlin Cortez, Michael H Dushoff, Jonathan Weitz, Joshua S Virus Evol Research Article Bacterial viruses, that is ‘bacteriophage’ or ‘phage’, can infect and lyse their bacterial hosts, releasing new viral progeny. In addition to the lytic pathway, certain bacteriophage (i.e. ‘temperate’ bacteriophage) can also initiate lysogeny, a latent mode of infection in which the viral genome is integrated into and replicated with the bacterial chromosome. Subsequently, the integrated viral genome, that is the ‘prophage’, can induce and restart the lytic pathway. Here, we explore the relationship among infection mode, ecological context, and viral fitness, in essence asking: when should viruses be temperate? To do so, we use network loop analysis to quantify fitness in terms of network paths through the life history of an infectious pathogen that start and end with infected cells. This analysis reveals that temperate strategies, particularly those with direct benefits to cellular fitness, should be favored at low host abundances. This finding applies to a spectrum of mechanistic models of phage–bacteria dynamics spanning both explicit and implicit representations of intra-cellular infection dynamics. However, the same analysis reveals that temperate strategies, in and of themselves, do not provide an advantage when infection imposes a cost to cellular fitness. Hence, we use evolutionary invasion analysis to explore when temperate phage can invade microbial communities with circulating lytic phage. We find that lytic phage can drive down niche competition amongst microbial cells, facilitating the subsequent invasion of latent strategies that increase cellular resistance and/or immunity to infection by lytic viruses—notably this finding holds even when the prophage comes at a direct fitness cost to cellular reproduction. Altogether, our analysis identifies broad ecological conditions that favor latency and provide a principled framework for exploring the impacts of ecological context on both the short- and long-term benefits of being temperate. Oxford University Press 2020-05-22 /pmc/articles/PMC9532926/ /pubmed/36204422 http://dx.doi.org/10.1093/ve/veaa042 Text en © The Author(s) 2020. Published by Oxford University Press. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Li, Guanlin
Cortez, Michael H
Dushoff, Jonathan
Weitz, Joshua S
When to be temperate: on the fitness benefits of lysis vs. lysogeny
title When to be temperate: on the fitness benefits of lysis vs. lysogeny
title_full When to be temperate: on the fitness benefits of lysis vs. lysogeny
title_fullStr When to be temperate: on the fitness benefits of lysis vs. lysogeny
title_full_unstemmed When to be temperate: on the fitness benefits of lysis vs. lysogeny
title_short When to be temperate: on the fitness benefits of lysis vs. lysogeny
title_sort when to be temperate: on the fitness benefits of lysis vs. lysogeny
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532926/
https://www.ncbi.nlm.nih.gov/pubmed/36204422
http://dx.doi.org/10.1093/ve/veaa042
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