Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy

Bacteriophages are viruses capable of recognizing with high specificity, propagating inside of, and destroying their bacterial hosts. The phage lytic life cycle makes phages attractive as tools to selectively kill pathogenic bacteria with minimal impact on the surrounding microbiome. To effectively...

Full description

Bibliographic Details
Main Authors: Steven Gayder, Michael Parcey, Darlene Nesbitt, Alan J. Castle, Antonet M. Svircev
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/9/1449
_version_ 1797552973393428480
author Steven Gayder
Michael Parcey
Darlene Nesbitt
Alan J. Castle
Antonet M. Svircev
author_facet Steven Gayder
Michael Parcey
Darlene Nesbitt
Alan J. Castle
Antonet M. Svircev
author_sort Steven Gayder
collection DOAJ
description Bacteriophages are viruses capable of recognizing with high specificity, propagating inside of, and destroying their bacterial hosts. The phage lytic life cycle makes phages attractive as tools to selectively kill pathogenic bacteria with minimal impact on the surrounding microbiome. To effectively harness the potential of phages in therapy, it is critical to understand the phage–host dynamics and how these interactions can change in complex populations. Our model examined the interactions between the plant pathogen <i>Erwinia amylovora</i>, the antagonistic epiphyte <i>Pantoea agglomerans</i>, and the bacteriophages that infect and kill both species. <i>P. agglomerans</i> strains are used as a phage carrier; their role is to deliver and propagate the bacteriophages on the plant surface prior to the arrival of the pathogen. Using liquid cultures, the populations of the pathogen, carrier, and phages were tracked over time with quantitative real-time PCR. The jumbo <i>Myoviridae</i> phage ϕEa35-70 synergized with both the <i>Myoviridae</i> ϕEa21-4 and <i>Podoviridae</i> ϕEa46-1-A1 and was most effective in combination at reducing <i>E. amylovora</i> growth over 24 h. Phage ϕEa35-70, however, also reduced the growth of <i>P. agglomerans</i>. Phage cocktails of ϕEa21-4, ϕEa46-1-A1, and ϕEa35-70 at multiplicities of infections (MOIs) of 10, 1, and 0.01, respectively, no longer inhibited growth of <i>P. agglomerans</i>. When this cocktail was grown with <i>P. agglomerans</i> for 8 h prior to pathogen introduction, pathogen growth was reduced by over four log units over 24 h. These findings present a novel approach to study complex phage–host dynamics that can be exploited to create more effective phage-based therapies.
first_indexed 2024-03-10T16:09:47Z
format Article
id doaj.art-7f4542b87dd04d15b42d0efb5449f10b
institution Directory Open Access Journal
issn 2076-2607
language English
last_indexed 2024-03-10T16:09:47Z
publishDate 2020-09-01
publisher MDPI AG
record_format Article
series Microorganisms
spelling doaj.art-7f4542b87dd04d15b42d0efb5449f10b2023-11-20T14:36:36ZengMDPI AGMicroorganisms2076-26072020-09-0189144910.3390/microorganisms8091449Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail EfficacySteven Gayder0Michael Parcey1Darlene Nesbitt2Alan J. Castle3Antonet M. Svircev4Centre for Biotechnology, Brock University, St. Catharines, ON L2S 3A1, CanadaCentre for Biotechnology, Brock University, St. Catharines, ON L2S 3A1, CanadaAgriculture and Agri-Food Canada, Vineland Station, ON L0R 2E0, CanadaDepartment of Biological Sciences, Brock University, St. Catharines, ON L2S 3A1, CanadaAgriculture and Agri-Food Canada, Vineland Station, ON L0R 2E0, CanadaBacteriophages are viruses capable of recognizing with high specificity, propagating inside of, and destroying their bacterial hosts. The phage lytic life cycle makes phages attractive as tools to selectively kill pathogenic bacteria with minimal impact on the surrounding microbiome. To effectively harness the potential of phages in therapy, it is critical to understand the phage–host dynamics and how these interactions can change in complex populations. Our model examined the interactions between the plant pathogen <i>Erwinia amylovora</i>, the antagonistic epiphyte <i>Pantoea agglomerans</i>, and the bacteriophages that infect and kill both species. <i>P. agglomerans</i> strains are used as a phage carrier; their role is to deliver and propagate the bacteriophages on the plant surface prior to the arrival of the pathogen. Using liquid cultures, the populations of the pathogen, carrier, and phages were tracked over time with quantitative real-time PCR. The jumbo <i>Myoviridae</i> phage ϕEa35-70 synergized with both the <i>Myoviridae</i> ϕEa21-4 and <i>Podoviridae</i> ϕEa46-1-A1 and was most effective in combination at reducing <i>E. amylovora</i> growth over 24 h. Phage ϕEa35-70, however, also reduced the growth of <i>P. agglomerans</i>. Phage cocktails of ϕEa21-4, ϕEa46-1-A1, and ϕEa35-70 at multiplicities of infections (MOIs) of 10, 1, and 0.01, respectively, no longer inhibited growth of <i>P. agglomerans</i>. When this cocktail was grown with <i>P. agglomerans</i> for 8 h prior to pathogen introduction, pathogen growth was reduced by over four log units over 24 h. These findings present a novel approach to study complex phage–host dynamics that can be exploited to create more effective phage-based therapies.https://www.mdpi.com/2076-2607/8/9/1449fire blightphage carrierbacteriophagesqPCRphage–host dynamicsphage cocktails
spellingShingle Steven Gayder
Michael Parcey
Darlene Nesbitt
Alan J. Castle
Antonet M. Svircev
Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
Microorganisms
fire blight
phage carrier
bacteriophages
qPCR
phage–host dynamics
phage cocktails
title Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
title_full Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
title_fullStr Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
title_full_unstemmed Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
title_short Population Dynamics between <i>Erwinia amylovora</i>, <i>Pantoea agglomerans</i> and Bacteriophages: Exploiting Synergy and Competition to Improve Phage Cocktail Efficacy
title_sort population dynamics between i erwinia amylovora i i pantoea agglomerans i and bacteriophages exploiting synergy and competition to improve phage cocktail efficacy
topic fire blight
phage carrier
bacteriophages
qPCR
phage–host dynamics
phage cocktails
url https://www.mdpi.com/2076-2607/8/9/1449
work_keys_str_mv AT stevengayder populationdynamicsbetweenierwiniaamylovoraiipantoeaagglomeransiandbacteriophagesexploitingsynergyandcompetitiontoimprovephagecocktailefficacy
AT michaelparcey populationdynamicsbetweenierwiniaamylovoraiipantoeaagglomeransiandbacteriophagesexploitingsynergyandcompetitiontoimprovephagecocktailefficacy
AT darlenenesbitt populationdynamicsbetweenierwiniaamylovoraiipantoeaagglomeransiandbacteriophagesexploitingsynergyandcompetitiontoimprovephagecocktailefficacy
AT alanjcastle populationdynamicsbetweenierwiniaamylovoraiipantoeaagglomeransiandbacteriophagesexploitingsynergyandcompetitiontoimprovephagecocktailefficacy
AT antonetmsvircev populationdynamicsbetweenierwiniaamylovoraiipantoeaagglomeransiandbacteriophagesexploitingsynergyandcompetitiontoimprovephagecocktailefficacy