Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila

Aeromonas hydrophila is an emerging foodborne pathogen causing human gastroenteritis. Aeromonas species isolated from food such as seafood presented multidrug-resistance (MDR), raising serious concerns regarding food safety and public health. The use of phages to infect bacteria is a defense against...

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Main Authors: Yuting Hou, Zhihao Wu, Li Ren, Yuan Chen, Yong-An Zhang, Yang Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1178876/full
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author Yuting Hou
Zhihao Wu
Li Ren
Yuan Chen
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
author_facet Yuting Hou
Zhihao Wu
Li Ren
Yuan Chen
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
author_sort Yuting Hou
collection DOAJ
description Aeromonas hydrophila is an emerging foodborne pathogen causing human gastroenteritis. Aeromonas species isolated from food such as seafood presented multidrug-resistance (MDR), raising serious concerns regarding food safety and public health. The use of phages to infect bacteria is a defense against drug-resistant pathogens. In this study, phage ZPAH34 isolated from the lake sample exerted lytic activity against MDR A. hydrophila strain ZYAH75 and inhibited the biofilm on different food-contacting surfaces. ZPAH34 has a large dsDNA genome of 234 kb which belongs to a novel jumbo phage. However, its particle size is the smallest of known jumbo phages so far. Based on phylogenetic analysis, ZPAH34 was used to establish a new genus Chaoshanvirus. Biological characterization revealed that ZPAH34 exhibited wide environmental tolerance, and a high rapid adsorb and reproductive capacity. Food biocontrol experiments demonstrated that ZPAH34 reduces the viable count of A. hydrophila on fish fillets (2.31 log) and lettuce (3.28 log) with potential bactericidal effects. This study isolated and characterized jumbo phage ZPAH34 not only enriched the understanding of phage biological entity diversity and evolution because of its minimal virion size with large genome but also was the first usage of jumbo phage in food safety to eliminate A. hydrophila.
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spelling doaj.art-9cdf759750574547ad6ada14bc84a3352023-06-21T09:36:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-06-011410.3389/fmicb.2023.11788761178876Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophilaYuting Hou0Zhihao Wu1Li Ren2Yuan Chen3Yong-An Zhang4Yong-An Zhang5Yang Zhou6Yang Zhou7Yang Zhou8National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Shenzhen Institute of Nutrition and Health, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, ChinaAeromonas hydrophila is an emerging foodborne pathogen causing human gastroenteritis. Aeromonas species isolated from food such as seafood presented multidrug-resistance (MDR), raising serious concerns regarding food safety and public health. The use of phages to infect bacteria is a defense against drug-resistant pathogens. In this study, phage ZPAH34 isolated from the lake sample exerted lytic activity against MDR A. hydrophila strain ZYAH75 and inhibited the biofilm on different food-contacting surfaces. ZPAH34 has a large dsDNA genome of 234 kb which belongs to a novel jumbo phage. However, its particle size is the smallest of known jumbo phages so far. Based on phylogenetic analysis, ZPAH34 was used to establish a new genus Chaoshanvirus. Biological characterization revealed that ZPAH34 exhibited wide environmental tolerance, and a high rapid adsorb and reproductive capacity. Food biocontrol experiments demonstrated that ZPAH34 reduces the viable count of A. hydrophila on fish fillets (2.31 log) and lettuce (3.28 log) with potential bactericidal effects. This study isolated and characterized jumbo phage ZPAH34 not only enriched the understanding of phage biological entity diversity and evolution because of its minimal virion size with large genome but also was the first usage of jumbo phage in food safety to eliminate A. hydrophila.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1178876/fullAeromonas hydrophilaphage ZPAH34genomefoodsbiofilm
spellingShingle Yuting Hou
Zhihao Wu
Li Ren
Yuan Chen
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
Frontiers in Microbiology
Aeromonas hydrophila
phage ZPAH34
genome
foods
biofilm
title Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
title_full Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
title_fullStr Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
title_full_unstemmed Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
title_short Characterization and application of a lytic jumbo phage ZPAH34 against multidrug-resistant Aeromonas hydrophila
title_sort characterization and application of a lytic jumbo phage zpah34 against multidrug resistant aeromonas hydrophila
topic Aeromonas hydrophila
phage ZPAH34
genome
foods
biofilm
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1178876/full
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