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The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli

Prophage sequences are present in most bacterial genomes and account for up to 20% of its host genome. Integration of temperate phages may have an impact on the expression of host genes, while some prophages could turn into the lytic cycle and affect bacterial host biological characteristics. We inv...

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Autores principales: Li, Dezhi, Liang, Wei, Hu, Qingyue, Ren, Jianluan, Xue, Feng, Liu, Qing, Tang, Fang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9701743/
https://www.ncbi.nlm.nih.gov/pubmed/36452923
http://dx.doi.org/10.3389/fmicb.2022.1049341
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author Li, Dezhi
Liang, Wei
Hu, Qingyue
Ren, Jianluan
Xue, Feng
Liu, Qing
Tang, Fang
author_facet Li, Dezhi
Liang, Wei
Hu, Qingyue
Ren, Jianluan
Xue, Feng
Liu, Qing
Tang, Fang
author_sort Li, Dezhi
collection PubMed
description Prophage sequences are present in most bacterial genomes and account for up to 20% of its host genome. Integration of temperate phages may have an impact on the expression of host genes, while some prophages could turn into the lytic cycle and affect bacterial host biological characteristics. We investigated the role of spontaneous induction prophages in avian pathogenic Escherichia coli (APEC), which is the causative agent of avian colibacillosis in poultry, and considered a potential zoonotic bacterium related to the fact it serves as an armory of extraintestinal pathogenic E. coli. We found that APEC strain DE458 had a high spontaneous induction rate in vivo and in vitro. The released phage particles, phi458, were isolated, purified, and sequenced, and the deletion mutant, DE458Δphi458, was constructed and characterized. Biofilm formation of DE458Δphi458 was strongly decreased compared to that of the wild-type strain (p < 0.01). In addition, while the addition of DNase (100 μg/ml) did not affect prophage release but could digest eDNA, it significantly reduced the biofilm production of DE458 biofilm to a level close to that of DE458Δphi458. Compared to DE458, the adhesion and invasion abilities of DE458Δphi458 increased by approximately 6–20 times (p < 0.05). The virulence of DE458Δphi458 was enhanced by approximately 10-fold in chickens based on a 50% lethal dose. Furthermore, avian infection assays showed that the bacterial loads of DE458Δphi458 in the lung and liver were increased by 16.5- and 10-fold (p < 0.05), respectively, compared with those of the WT strain. The qRT-PCR revealed that deletion of phi458 led to upregulation of type I fimbriate-related gene fimH and curli-related gene csgC by 3- and 2.8-fold, respectively (p < 0.01). Our study revealed that phi458 promoted biofilm formation by spontaneously inducing and decreasing virulence by repressing virulence genes.
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spelling pubmed-97017432022-11-29 The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli Li, Dezhi Liang, Wei Hu, Qingyue Ren, Jianluan Xue, Feng Liu, Qing Tang, Fang Front Microbiol Microbiology Prophage sequences are present in most bacterial genomes and account for up to 20% of its host genome. Integration of temperate phages may have an impact on the expression of host genes, while some prophages could turn into the lytic cycle and affect bacterial host biological characteristics. We investigated the role of spontaneous induction prophages in avian pathogenic Escherichia coli (APEC), which is the causative agent of avian colibacillosis in poultry, and considered a potential zoonotic bacterium related to the fact it serves as an armory of extraintestinal pathogenic E. coli. We found that APEC strain DE458 had a high spontaneous induction rate in vivo and in vitro. The released phage particles, phi458, were isolated, purified, and sequenced, and the deletion mutant, DE458Δphi458, was constructed and characterized. Biofilm formation of DE458Δphi458 was strongly decreased compared to that of the wild-type strain (p < 0.01). In addition, while the addition of DNase (100 μg/ml) did not affect prophage release but could digest eDNA, it significantly reduced the biofilm production of DE458 biofilm to a level close to that of DE458Δphi458. Compared to DE458, the adhesion and invasion abilities of DE458Δphi458 increased by approximately 6–20 times (p < 0.05). The virulence of DE458Δphi458 was enhanced by approximately 10-fold in chickens based on a 50% lethal dose. Furthermore, avian infection assays showed that the bacterial loads of DE458Δphi458 in the lung and liver were increased by 16.5- and 10-fold (p < 0.05), respectively, compared with those of the WT strain. The qRT-PCR revealed that deletion of phi458 led to upregulation of type I fimbriate-related gene fimH and curli-related gene csgC by 3- and 2.8-fold, respectively (p < 0.01). Our study revealed that phi458 promoted biofilm formation by spontaneously inducing and decreasing virulence by repressing virulence genes. Frontiers Media S.A. 2022-11-14 /pmc/articles/PMC9701743/ /pubmed/36452923 http://dx.doi.org/10.3389/fmicb.2022.1049341 Text en Copyright © 2022 Li, Liang, Hu, Ren, Xue, Liu and Tang. 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 Microbiology
Li, Dezhi
Liang, Wei
Hu, Qingyue
Ren, Jianluan
Xue, Feng
Liu, Qing
Tang, Fang
The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title_full The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title_fullStr The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title_full_unstemmed The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title_short The effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic Escherichia coli
title_sort effect of a spontaneous induction prophage, phi458, on biofilm formation and virulence in avian pathogenic escherichia coli
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9701743/
https://www.ncbi.nlm.nih.gov/pubmed/36452923
http://dx.doi.org/10.3389/fmicb.2022.1049341
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