A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7

IntroductionShiga toxin-producing Escherichia coli (STEC) O157:H7 is one of the notorious foodborne pathogens causing high mortality through the consumption of contaminated food items. The food safety risk from STEC pathogens could escalate when a group of bacterial cells aggregates to form a biofil...

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Main Authors: Yen-Te Liao, Kan-Ju Ho, Yujie Zhang, Alexandra Salvador, Vivian C. H. Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1302032/full
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author Yen-Te Liao
Kan-Ju Ho
Yujie Zhang
Alexandra Salvador
Vivian C. H. Wu
author_facet Yen-Te Liao
Kan-Ju Ho
Yujie Zhang
Alexandra Salvador
Vivian C. H. Wu
author_sort Yen-Te Liao
collection DOAJ
description IntroductionShiga toxin-producing Escherichia coli (STEC) O157:H7 is one of the notorious foodborne pathogens causing high mortality through the consumption of contaminated food items. The food safety risk from STEC pathogens could escalate when a group of bacterial cells aggregates to form a biofilm. Bacterial biofilm can diminish the effects of various antimicrobial interventions and enhance the pathogenicity of the pathogens. Therefore, there is an urgent need to have effective control measurements. Bacteriophages can kill the target bacterial cells through lytic infection, and some enzymes produced during the infection have the capability to penetrate the biofilm for mitigation compared to traditional interventions. This study aimed to characterize a new Escherichia phage vB_EcoS-UDF157lw (or UDF157lw) and determine its antimicrobial efficacy against E. coli O157:H7.MethodsPhage characterization included biological approaches, including phage morphology, one-step growth curve, stability tests (pH and temperature), and genomic approaches (whole-genome sequencing). Later, antimicrobial activity tests, including productive infection against susceptible bacterial strains, in vitro antimicrobial activity, and anti-biofilm, were conducted.ResultsUDF157lw is a new member of the phages belonging to the Rogunavirus genus, comprising a long and non-contractile tail, isolated from bovine feces and shares close genomic evolutionary similarities with Escherichia phages vB_EcoS-BECP10 and bV_EcoS_AKS96. When used against E. coli O157:H7 (ATCC35150), phage UDF157lw exhibited a latent period of 14 min and a burst size of 110 PFU per infected cell. The phage remained viable in a wide range of pH values (pH 4–11) and temperatures (4–60°C). No virulence genes, such as stx, lysogenic genes, and antibiotic resistance genes, were found. Phage UDF157lw demonstrated high infection efficiencies against different E. coli O157:H7 and generic E. coli strains. In addition, UDF157lw encoded a unique major tail protein (ORF_26) with prominent depolymerase enzyme activity against various E. coli O157:H7 strains, causing large plaque sizes. In contrast to the phage without encoding depolymerase gene, UDF157lw was able to reduce the 24-h and 48-h E. coli O157:H7 biofilm after 1-h phage treatment.DiscussionThe findings of this study provide insights into a new member of the Rogunavirus phages and demonstrate its antimicrobial potential against E. coli O157:H7 in vitro.
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spelling doaj.art-e2290b2908fc4a2fa30f1e7238585d092024-01-22T04:26:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.13020321302032A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7Yen-Te LiaoKan-Ju HoYujie ZhangAlexandra SalvadorVivian C. H. WuIntroductionShiga toxin-producing Escherichia coli (STEC) O157:H7 is one of the notorious foodborne pathogens causing high mortality through the consumption of contaminated food items. The food safety risk from STEC pathogens could escalate when a group of bacterial cells aggregates to form a biofilm. Bacterial biofilm can diminish the effects of various antimicrobial interventions and enhance the pathogenicity of the pathogens. Therefore, there is an urgent need to have effective control measurements. Bacteriophages can kill the target bacterial cells through lytic infection, and some enzymes produced during the infection have the capability to penetrate the biofilm for mitigation compared to traditional interventions. This study aimed to characterize a new Escherichia phage vB_EcoS-UDF157lw (or UDF157lw) and determine its antimicrobial efficacy against E. coli O157:H7.MethodsPhage characterization included biological approaches, including phage morphology, one-step growth curve, stability tests (pH and temperature), and genomic approaches (whole-genome sequencing). Later, antimicrobial activity tests, including productive infection against susceptible bacterial strains, in vitro antimicrobial activity, and anti-biofilm, were conducted.ResultsUDF157lw is a new member of the phages belonging to the Rogunavirus genus, comprising a long and non-contractile tail, isolated from bovine feces and shares close genomic evolutionary similarities with Escherichia phages vB_EcoS-BECP10 and bV_EcoS_AKS96. When used against E. coli O157:H7 (ATCC35150), phage UDF157lw exhibited a latent period of 14 min and a burst size of 110 PFU per infected cell. The phage remained viable in a wide range of pH values (pH 4–11) and temperatures (4–60°C). No virulence genes, such as stx, lysogenic genes, and antibiotic resistance genes, were found. Phage UDF157lw demonstrated high infection efficiencies against different E. coli O157:H7 and generic E. coli strains. In addition, UDF157lw encoded a unique major tail protein (ORF_26) with prominent depolymerase enzyme activity against various E. coli O157:H7 strains, causing large plaque sizes. In contrast to the phage without encoding depolymerase gene, UDF157lw was able to reduce the 24-h and 48-h E. coli O157:H7 biofilm after 1-h phage treatment.DiscussionThe findings of this study provide insights into a new member of the Rogunavirus phages and demonstrate its antimicrobial potential against E. coli O157:H7 in vitro.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1302032/fulllytic bacteriophageRogunavirus genusE. coli O157:H7depolymerase enzymeanti-biofilm activity
spellingShingle Yen-Te Liao
Kan-Ju Ho
Yujie Zhang
Alexandra Salvador
Vivian C. H. Wu
A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
Frontiers in Microbiology
lytic bacteriophage
Rogunavirus genus
E. coli O157:H7
depolymerase enzyme
anti-biofilm activity
title A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
title_full A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
title_fullStr A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
title_full_unstemmed A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
title_short A new Rogue-like Escherichia phage UDF157lw to control Escherichia coli O157:H7
title_sort new rogue like escherichia phage udf157lw to control escherichia coli o157 h7
topic lytic bacteriophage
Rogunavirus genus
E. coli O157:H7
depolymerase enzyme
anti-biofilm activity
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1302032/full
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