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Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage

In microbial communities, viruses compete with each other for host cells to infect. As a consequence of competition for hosts, viruses evolve inhibitory mechanisms to suppress their competitors. One such mechanism is superinfection exclusion, in which a preexisting viral infection prevents a seconda...

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Autores principales: Biggs, Karin R. H., Bailes, Clayton L., Scott, LuAnn, Wichman, Holly A., Schwartz, Elissa J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8310164/
https://www.ncbi.nlm.nih.gov/pubmed/34372595
http://dx.doi.org/10.3390/v13071389
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author Biggs, Karin R. H.
Bailes, Clayton L.
Scott, LuAnn
Wichman, Holly A.
Schwartz, Elissa J.
author_facet Biggs, Karin R. H.
Bailes, Clayton L.
Scott, LuAnn
Wichman, Holly A.
Schwartz, Elissa J.
author_sort Biggs, Karin R. H.
collection PubMed
description In microbial communities, viruses compete with each other for host cells to infect. As a consequence of competition for hosts, viruses evolve inhibitory mechanisms to suppress their competitors. One such mechanism is superinfection exclusion, in which a preexisting viral infection prevents a secondary infection. The bacteriophage ΦX174 exhibits a potential superinfection inhibition mechanism (in which secondary infections are either blocked or resisted) known as the reduction effect. In this auto-inhibitory phenomenon, a plasmid containing a fragment of the ΦX174 genome confers resistance to infection among cells that were once permissive to ΦX174. Taking advantage of this plasmid system, we examine the inhibitory properties of the ΦX174 reduction effect on a range of wild ΦX174-like phages. We then assess how closely the reduction effect in the plasmid system mimics natural superinfection inhibition by carrying out phage–phage competitions in continuous culture, and we evaluate whether the overall competitive advantage can be predicted by phage fitness or by a combination of fitness and reduction effect inhibition. Our results show that viral fitness often correctly predicts the winner. However, a phage’s reduction sequence also provides an advantage to the phage in some cases, modulating phage–phage competition and allowing for persistence where competitive exclusion was expected. These findings provide strong evidence for more complex dynamics than were previously thought, in which the reduction effect may inhibit fast-growing viruses, thereby helping to facilitate coexistence.
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spelling pubmed-83101642021-07-25 Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage Biggs, Karin R. H. Bailes, Clayton L. Scott, LuAnn Wichman, Holly A. Schwartz, Elissa J. Viruses Article In microbial communities, viruses compete with each other for host cells to infect. As a consequence of competition for hosts, viruses evolve inhibitory mechanisms to suppress their competitors. One such mechanism is superinfection exclusion, in which a preexisting viral infection prevents a secondary infection. The bacteriophage ΦX174 exhibits a potential superinfection inhibition mechanism (in which secondary infections are either blocked or resisted) known as the reduction effect. In this auto-inhibitory phenomenon, a plasmid containing a fragment of the ΦX174 genome confers resistance to infection among cells that were once permissive to ΦX174. Taking advantage of this plasmid system, we examine the inhibitory properties of the ΦX174 reduction effect on a range of wild ΦX174-like phages. We then assess how closely the reduction effect in the plasmid system mimics natural superinfection inhibition by carrying out phage–phage competitions in continuous culture, and we evaluate whether the overall competitive advantage can be predicted by phage fitness or by a combination of fitness and reduction effect inhibition. Our results show that viral fitness often correctly predicts the winner. However, a phage’s reduction sequence also provides an advantage to the phage in some cases, modulating phage–phage competition and allowing for persistence where competitive exclusion was expected. These findings provide strong evidence for more complex dynamics than were previously thought, in which the reduction effect may inhibit fast-growing viruses, thereby helping to facilitate coexistence. MDPI 2021-07-17 /pmc/articles/PMC8310164/ /pubmed/34372595 http://dx.doi.org/10.3390/v13071389 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Biggs, Karin R. H.
Bailes, Clayton L.
Scott, LuAnn
Wichman, Holly A.
Schwartz, Elissa J.
Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title_full Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title_fullStr Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title_full_unstemmed Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title_short Ecological Approach to Understanding Superinfection Inhibition in Bacteriophage
title_sort ecological approach to understanding superinfection inhibition in bacteriophage
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8310164/
https://www.ncbi.nlm.nih.gov/pubmed/34372595
http://dx.doi.org/10.3390/v13071389
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