Phage strategies facilitate bacterial coexistence under environmental variability

Bacterial communities are often exposed to temporal variations in resource availability, which exceed bacterial generation times and thereby affect bacterial coexistence. Bacterial population dynamics are also shaped by bacteriophages, which are a main cause of bacterial mortality. Several strategie...

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Autores principales: Esther Voigt, Björn C. Rall, Antonis Chatzinotas, Ulrich Brose, Benjamin Rosenbaum
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Publicado: PeerJ Inc. 2021
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spelling oai:doaj.org-article:1b3637c4c546430ab4e548277ec036142021-11-06T15:05:11ZPhage strategies facilitate bacterial coexistence under environmental variability10.7717/peerj.121942167-8359https://doaj.org/article/1b3637c4c546430ab4e548277ec036142021-11-01T00:00:00Zhttps://peerj.com/articles/12194.pdfhttps://peerj.com/articles/12194/https://doaj.org/toc/2167-8359Bacterial communities are often exposed to temporal variations in resource availability, which exceed bacterial generation times and thereby affect bacterial coexistence. Bacterial population dynamics are also shaped by bacteriophages, which are a main cause of bacterial mortality. Several strategies are proposed in the literature to describe infections by phages, such as “Killing the Winner”, “Piggyback the loser” (PtL) or “Piggyback the Winner” (PtW). The two temperate phage strategies PtL and PtW are defined by a change from lytic to lysogenic infection when the host density changes, from high to low or from low to high, respectively. To date, the occurrence of different phage strategies and their response to environmental variability is poorly understood. In our study, we developed a microbial trophic network model using ordinary differential equations (ODEs) and performed ‘in silico’ experiments. To model the switch from the lysogenic to the lytic cycle, we modified the lysis rate of infected bacteria and their growth was turned on or off using a density-dependent switching point. We addressed whether and how the different phage strategies facilitate bacteria coexistence competing for limiting resources. We also studied the impact of a fluctuating resource inflow to evaluate the response of the different phage strategies to environmental variability. Our results show that the viral shunt (i.e. nutrient release after bacterial lysis) leads to an enrichment of the system. This enrichment enables bacterial coexistence at lower resource concentrations. We were able to show that an established, purely lytic model leads to stable bacterial coexistence despite fluctuating resources. Both temperate phage models differ in their coexistence patterns. The model of PtW yields stable bacterial coexistence at a limited range of resource supply and is most sensitive to resource fluctuations. Interestingly, the purely lytic phage strategy and PtW both result in stable bacteria coexistence at oligotrophic conditions. The PtL model facilitates stable bacterial coexistence over a large range of stable and fluctuating resource inflow. An increase in bacterial growth rate results in a higher resilience to resource variability for the PtL and the lytic infection model. We propose that both temperate phage strategies represent different mechanisms of phages coping with environmental variability. Our study demonstrates how phage strategies can maintain bacterial coexistence in constant and fluctuating environments.Esther VoigtBjörn C. RallAntonis ChatzinotasUlrich BroseBenjamin RosenbaumPeerJ Inc.articleBacteria phage interactionsVirusTemperate phagesPopulation dynamicsBiodiversityMicrobial ecologyMedicineRENPeerJ, Vol 9, p e12194 (2021)
institution DOAJ
collection DOAJ
language EN
topic Bacteria phage interactions
Virus
Temperate phages
Population dynamics
Biodiversity
Microbial ecology
Medicine
R
spellingShingle Bacteria phage interactions
Virus
Temperate phages
Population dynamics
Biodiversity
Microbial ecology
Medicine
R
Esther Voigt
Björn C. Rall
Antonis Chatzinotas
Ulrich Brose
Benjamin Rosenbaum
Phage strategies facilitate bacterial coexistence under environmental variability
description Bacterial communities are often exposed to temporal variations in resource availability, which exceed bacterial generation times and thereby affect bacterial coexistence. Bacterial population dynamics are also shaped by bacteriophages, which are a main cause of bacterial mortality. Several strategies are proposed in the literature to describe infections by phages, such as “Killing the Winner”, “Piggyback the loser” (PtL) or “Piggyback the Winner” (PtW). The two temperate phage strategies PtL and PtW are defined by a change from lytic to lysogenic infection when the host density changes, from high to low or from low to high, respectively. To date, the occurrence of different phage strategies and their response to environmental variability is poorly understood. In our study, we developed a microbial trophic network model using ordinary differential equations (ODEs) and performed ‘in silico’ experiments. To model the switch from the lysogenic to the lytic cycle, we modified the lysis rate of infected bacteria and their growth was turned on or off using a density-dependent switching point. We addressed whether and how the different phage strategies facilitate bacteria coexistence competing for limiting resources. We also studied the impact of a fluctuating resource inflow to evaluate the response of the different phage strategies to environmental variability. Our results show that the viral shunt (i.e. nutrient release after bacterial lysis) leads to an enrichment of the system. This enrichment enables bacterial coexistence at lower resource concentrations. We were able to show that an established, purely lytic model leads to stable bacterial coexistence despite fluctuating resources. Both temperate phage models differ in their coexistence patterns. The model of PtW yields stable bacterial coexistence at a limited range of resource supply and is most sensitive to resource fluctuations. Interestingly, the purely lytic phage strategy and PtW both result in stable bacteria coexistence at oligotrophic conditions. The PtL model facilitates stable bacterial coexistence over a large range of stable and fluctuating resource inflow. An increase in bacterial growth rate results in a higher resilience to resource variability for the PtL and the lytic infection model. We propose that both temperate phage strategies represent different mechanisms of phages coping with environmental variability. Our study demonstrates how phage strategies can maintain bacterial coexistence in constant and fluctuating environments.
format article
author Esther Voigt
Björn C. Rall
Antonis Chatzinotas
Ulrich Brose
Benjamin Rosenbaum
author_facet Esther Voigt
Björn C. Rall
Antonis Chatzinotas
Ulrich Brose
Benjamin Rosenbaum
author_sort Esther Voigt
title Phage strategies facilitate bacterial coexistence under environmental variability
title_short Phage strategies facilitate bacterial coexistence under environmental variability
title_full Phage strategies facilitate bacterial coexistence under environmental variability
title_fullStr Phage strategies facilitate bacterial coexistence under environmental variability
title_full_unstemmed Phage strategies facilitate bacterial coexistence under environmental variability
title_sort phage strategies facilitate bacterial coexistence under environmental variability
publisher PeerJ Inc.
publishDate 2021
url https://doaj.org/article/1b3637c4c546430ab4e548277ec03614
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AT bjorncrall phagestrategiesfacilitatebacterialcoexistenceunderenvironmentalvariability
AT antonischatzinotas phagestrategiesfacilitatebacterialcoexistenceunderenvironmentalvariability
AT ulrichbrose phagestrategiesfacilitatebacterialcoexistenceunderenvironmentalvariability
AT benjaminrosenbaum phagestrategiesfacilitatebacterialcoexistenceunderenvironmentalvariability
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