Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria

ABSTRACT Encounters among bacteria and their viral predators (bacteriophages) are among the most common ecological interactions on Earth. These encounters are likely to occur with regularity inside surface-bound communities that microbes most often occupy in natural environments. Such communities, t...

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Autores principales:	Emilia L. Simmons, Matthew C. Bond, Britt Koskella, Knut Drescher, Vanni Bucci, Carey D. Nadell
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bacteriophages biofilm computational biology confocal microscopy ecology microfluidics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4ebda95fb4c241b09835dc0e6b827db1
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spelling	oai:doaj.org-article:4ebda95fb4c241b09835dc0e6b827db12021-12-02T19:46:20ZBiofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria10.1128/mSystems.00877-192379-5077https://doaj.org/article/4ebda95fb4c241b09835dc0e6b827db12020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00877-19https://doaj.org/toc/2379-5077ABSTRACT Encounters among bacteria and their viral predators (bacteriophages) are among the most common ecological interactions on Earth. These encounters are likely to occur with regularity inside surface-bound communities that microbes most often occupy in natural environments. Such communities, termed biofilms, are spatially constrained: interactions become limited to near neighbors, diffusion of solutes and particulates can be reduced, and there is pronounced heterogeneity in nutrient access and physiological state. It is appreciated from prior theoretical work that phage-bacteria interactions are fundamentally different in spatially structured contexts, as opposed to well-mixed liquid culture. Spatially structured communities are predicted to promote the protection of susceptible host cells from phage exposure, and thus weaken selection for phage resistance. The details and generality of this prediction in realistic biofilm environments, however, are not known. Here, we explore phage-host interactions using experiments and simulations that are tuned to represent the essential elements of biofilm communities. Our simulations show that in biofilms, phage-resistant cells—as their relative abundance increases—can protect clusters of susceptible cells from phage exposure, promoting the coexistence of susceptible and phage-resistant bacteria under a large array of conditions. We characterize the population dynamics underlying this coexistence, and we show that coexistence is recapitulated in an experimental model of biofilm growth measured with confocal microscopy. Our results provide a clear view into the dynamics of phage resistance in biofilms with single-cell resolution of the underlying cell-virion interactions, linking the predictions of canonical theory to realistic models and in vitro experiments of biofilm growth. IMPORTANCE In the natural environment, bacteria most often live in communities bound to one another by secreted adhesives. These communities, or biofilms, play a central role in biogeochemical cycling, microbiome functioning, wastewater treatment, and disease. Wherever there are bacteria, there are also viruses that attack them, called phages. Interactions between bacteria and phages are likely to occur ubiquitously in biofilms. We show here, using simulations and experiments, that biofilms will in most conditions allow phage-susceptible bacteria to be protected from phage exposure, if they are growing alongside other cells that are phage resistant. This result has implications for the fundamental ecology of phage-bacteria interactions, as well as the development of phage-based antimicrobial therapeutics.Emilia L. SimmonsMatthew C. BondBritt KoskellaKnut DrescherVanni BucciCarey D. NadellAmerican Society for Microbiologyarticlebacteriophagesbiofilmcomputational biologyconfocal microscopyecologymicrofluidicsMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriophages biofilm computational biology confocal microscopy ecology microfluidics Microbiology QR1-502
spellingShingle	bacteriophages biofilm computational biology confocal microscopy ecology microfluidics Microbiology QR1-502 Emilia L. Simmons Matthew C. Bond Britt Koskella Knut Drescher Vanni Bucci Carey D. Nadell Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
description	ABSTRACT Encounters among bacteria and their viral predators (bacteriophages) are among the most common ecological interactions on Earth. These encounters are likely to occur with regularity inside surface-bound communities that microbes most often occupy in natural environments. Such communities, termed biofilms, are spatially constrained: interactions become limited to near neighbors, diffusion of solutes and particulates can be reduced, and there is pronounced heterogeneity in nutrient access and physiological state. It is appreciated from prior theoretical work that phage-bacteria interactions are fundamentally different in spatially structured contexts, as opposed to well-mixed liquid culture. Spatially structured communities are predicted to promote the protection of susceptible host cells from phage exposure, and thus weaken selection for phage resistance. The details and generality of this prediction in realistic biofilm environments, however, are not known. Here, we explore phage-host interactions using experiments and simulations that are tuned to represent the essential elements of biofilm communities. Our simulations show that in biofilms, phage-resistant cells—as their relative abundance increases—can protect clusters of susceptible cells from phage exposure, promoting the coexistence of susceptible and phage-resistant bacteria under a large array of conditions. We characterize the population dynamics underlying this coexistence, and we show that coexistence is recapitulated in an experimental model of biofilm growth measured with confocal microscopy. Our results provide a clear view into the dynamics of phage resistance in biofilms with single-cell resolution of the underlying cell-virion interactions, linking the predictions of canonical theory to realistic models and in vitro experiments of biofilm growth. IMPORTANCE In the natural environment, bacteria most often live in communities bound to one another by secreted adhesives. These communities, or biofilms, play a central role in biogeochemical cycling, microbiome functioning, wastewater treatment, and disease. Wherever there are bacteria, there are also viruses that attack them, called phages. Interactions between bacteria and phages are likely to occur ubiquitously in biofilms. We show here, using simulations and experiments, that biofilms will in most conditions allow phage-susceptible bacteria to be protected from phage exposure, if they are growing alongside other cells that are phage resistant. This result has implications for the fundamental ecology of phage-bacteria interactions, as well as the development of phage-based antimicrobial therapeutics.
format	article
author	Emilia L. Simmons Matthew C. Bond Britt Koskella Knut Drescher Vanni Bucci Carey D. Nadell
author_facet	Emilia L. Simmons Matthew C. Bond Britt Koskella Knut Drescher Vanni Bucci Carey D. Nadell
author_sort	Emilia L. Simmons
title	Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
title_short	Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
title_full	Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
title_fullStr	Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
title_full_unstemmed	Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria
title_sort	biofilm structure promotes coexistence of phage-resistant and phage-susceptible bacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/4ebda95fb4c241b09835dc0e6b827db1
work_keys_str_mv	AT emilialsimmons biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria AT matthewcbond biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria AT brittkoskella biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria AT knutdrescher biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria AT vannibucci biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria AT careydnadell biofilmstructurepromotescoexistenceofphageresistantandphagesusceptiblebacteria
_version_	1718376024462327808

Biofilm Structure Promotes Coexistence of Phage-Resistant and Phage-Susceptible Bacteria

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