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A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection

The inappropriate use of antibiotics has led to the emergence of multidrug-resistant strains. Bacteriophages (phages) have gained renewed attention as promising alternatives or supplements to antibiotics. In this study, a lytic avian pathogenic Escherichia coli (APEC) phage designated as PEC9 was is...

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Autores principales: Yao, Lan, Bao, Yinli, Hu, Jiangang, Zhang, Beibei, Wang, Zhiyang, Wang, Xinyu, Guo, Weiqi, Wang, Di, Qi, Jingjing, Tian, Mingxing, Bao, Yanqing, Li, Haihua, Wang, Shaohui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10513416/
https://www.ncbi.nlm.nih.gov/pubmed/37743864
http://dx.doi.org/10.3389/fcimb.2023.1253815
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author Yao, Lan
Bao, Yinli
Hu, Jiangang
Zhang, Beibei
Wang, Zhiyang
Wang, Xinyu
Guo, Weiqi
Wang, Di
Qi, Jingjing
Tian, Mingxing
Bao, Yanqing
Li, Haihua
Wang, Shaohui
author_facet Yao, Lan
Bao, Yinli
Hu, Jiangang
Zhang, Beibei
Wang, Zhiyang
Wang, Xinyu
Guo, Weiqi
Wang, Di
Qi, Jingjing
Tian, Mingxing
Bao, Yanqing
Li, Haihua
Wang, Shaohui
author_sort Yao, Lan
collection PubMed
description The inappropriate use of antibiotics has led to the emergence of multidrug-resistant strains. Bacteriophages (phages) have gained renewed attention as promising alternatives or supplements to antibiotics. In this study, a lytic avian pathogenic Escherichia coli (APEC) phage designated as PEC9 was isolated and purified from chicken farm feces samples. The morphology, genomic information, optimal multiplicity of infection (MOI), one-step growth curve, thermal stability, pH stability, in vitro antibacterial ability and biofilm formation inhibition ability of the phage were determined. Subsequently, the therapeutic effects of the phages were investigated in the mice model. The results showed that PEC9 was a member of the siphovirus-like by electron microscopy observation. Biological characterization revealed that it could lyse two serotypes of E. coli, including O1 (9/20) and O2 (6/20). The optimal multiplicity of infection (MOI) of phage PEC9 was 0.1. Phage PEC9 had a latent period of 20 min and a burst period of 40 min, with an average burst size of 68 plaque-forming units (PFUs)/cell. It maintained good lytic activity at pH 3-11 and 4-50°C and could efficiently inhibit the bacterial planktonic cell growth and biofilm formation, and reduce bacterial counts within the biofilm, when the MOI was 0.01, 0.1, and 1, respectively. Whole-genome sequencing showed that PEC9 was a dsDNA virus with a genome of 44379 bp and GC content of 54.39%. The genome contains 56 putative ORFs and no toxin, virulence, or resistance-related genes were detected. Phylogenetic tree analysis showed that PEC9 is closely related to E. coli phages vB_EcoS_Zar3M, vB_EcoS_PTXU06, SECphi18, ZCEC10, and ZCEC11, but most of these phages exhibit different gene arrangement. The phage PEC9 could successfully protect mice against APEC infection, including improved survival rate, reduced bacterial loads, and organ lesions. To conclude, our results suggest that phage PEC9 may be a promising candidate that can be used as an alternative to antibiotics in the control of APEC infection.
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spelling pubmed-105134162023-09-22 A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection Yao, Lan Bao, Yinli Hu, Jiangang Zhang, Beibei Wang, Zhiyang Wang, Xinyu Guo, Weiqi Wang, Di Qi, Jingjing Tian, Mingxing Bao, Yanqing Li, Haihua Wang, Shaohui Front Cell Infect Microbiol Cellular and Infection Microbiology The inappropriate use of antibiotics has led to the emergence of multidrug-resistant strains. Bacteriophages (phages) have gained renewed attention as promising alternatives or supplements to antibiotics. In this study, a lytic avian pathogenic Escherichia coli (APEC) phage designated as PEC9 was isolated and purified from chicken farm feces samples. The morphology, genomic information, optimal multiplicity of infection (MOI), one-step growth curve, thermal stability, pH stability, in vitro antibacterial ability and biofilm formation inhibition ability of the phage were determined. Subsequently, the therapeutic effects of the phages were investigated in the mice model. The results showed that PEC9 was a member of the siphovirus-like by electron microscopy observation. Biological characterization revealed that it could lyse two serotypes of E. coli, including O1 (9/20) and O2 (6/20). The optimal multiplicity of infection (MOI) of phage PEC9 was 0.1. Phage PEC9 had a latent period of 20 min and a burst period of 40 min, with an average burst size of 68 plaque-forming units (PFUs)/cell. It maintained good lytic activity at pH 3-11 and 4-50°C and could efficiently inhibit the bacterial planktonic cell growth and biofilm formation, and reduce bacterial counts within the biofilm, when the MOI was 0.01, 0.1, and 1, respectively. Whole-genome sequencing showed that PEC9 was a dsDNA virus with a genome of 44379 bp and GC content of 54.39%. The genome contains 56 putative ORFs and no toxin, virulence, or resistance-related genes were detected. Phylogenetic tree analysis showed that PEC9 is closely related to E. coli phages vB_EcoS_Zar3M, vB_EcoS_PTXU06, SECphi18, ZCEC10, and ZCEC11, but most of these phages exhibit different gene arrangement. The phage PEC9 could successfully protect mice against APEC infection, including improved survival rate, reduced bacterial loads, and organ lesions. To conclude, our results suggest that phage PEC9 may be a promising candidate that can be used as an alternative to antibiotics in the control of APEC infection. Frontiers Media S.A. 2023-09-07 /pmc/articles/PMC10513416/ /pubmed/37743864 http://dx.doi.org/10.3389/fcimb.2023.1253815 Text en Copyright © 2023 Yao, Bao, Hu, Zhang, Wang, Wang, Guo, Wang, Qi, Tian, Bao, Li and Wang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Yao, Lan
Bao, Yinli
Hu, Jiangang
Zhang, Beibei
Wang, Zhiyang
Wang, Xinyu
Guo, Weiqi
Wang, Di
Qi, Jingjing
Tian, Mingxing
Bao, Yanqing
Li, Haihua
Wang, Shaohui
A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title_full A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title_fullStr A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title_full_unstemmed A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title_short A lytic phage to control multidrug-resistant avian pathogenic Escherichia coli (APEC) infection
title_sort lytic phage to control multidrug-resistant avian pathogenic escherichia coli (apec) infection
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10513416/
https://www.ncbi.nlm.nih.gov/pubmed/37743864
http://dx.doi.org/10.3389/fcimb.2023.1253815
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