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Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture

SIMPLE SUMMARY: Vibrio bacteria are ubiquitous and abundant in coastal waters and sediments, and some species are pathogens to humans and marine organisms, leading to foodborne diseases and pandemic infections in humans and mass mortality and economic losses in marine aquaculture. However, the misus...

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Autores principales: Li, Xuejing, Liang, Yantao, Wang, Zhenhua, Yao, Yanyan, Chen, Xiaoli, Shao, Anran, Lu, Longfei, Dang, Hongyue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9687132/
https://www.ncbi.nlm.nih.gov/pubmed/36421384
http://dx.doi.org/10.3390/biology11111670
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author Li, Xuejing
Liang, Yantao
Wang, Zhenhua
Yao, Yanyan
Chen, Xiaoli
Shao, Anran
Lu, Longfei
Dang, Hongyue
author_facet Li, Xuejing
Liang, Yantao
Wang, Zhenhua
Yao, Yanyan
Chen, Xiaoli
Shao, Anran
Lu, Longfei
Dang, Hongyue
author_sort Li, Xuejing
collection PubMed
description SIMPLE SUMMARY: Vibrio bacteria are ubiquitous and abundant in coastal waters and sediments, and some species are pathogens to humans and marine organisms, leading to foodborne diseases and pandemic infections in humans and mass mortality and economic losses in marine aquaculture. However, the misuse and overuse of antibiotics have led to the emergence and spread of antibiotic-resistant bacteria and resistance genes in marine aquacultural settings and adjacent coastal environments. Bacterial pathogens may also acquire antibiotic resistance via gene mutations and horizontal gene transfers in such environments, making bacterial infectious diseases extremely difficult or even impossible to treat using conventional antibiotic-based therapies. Consequently, phage therapy has received increasing attention in recent years. This study describes the characterization of phage vB_VnaS-L3 from Vibrio natriegens, and explores its potential application as a biocontrol agent to replace antibiotics against pathogenic V. natriegens in juvenile Pacific abalones aquaculture. Our findings showed that phage vB_VnaS-L3 could be a potential alternate biocontrol and prophylactic agent that could effectively inhibit the growth of pathogenic V. natriegens, significantly reduce the mortality of juvenile abalones, and maintain abalone feeding capacity. ABSTRACT: Phage-based pathogen control (i.e., phage therapy) has received increasing scientific attention to reduce and prevent the emergence, transmission, and detrimental effects of antibiotic resistance. In the current study, multidrug-resistant Vibrio natriegens strain AbY-1805 was isolated and tentatively identified as a pathogen causing the death of juvenile Pacific abalones (Haliotis discus hannai Ino). In order to apply phage therapy, instead of antibiotics, to treat and control V. natriegens infections in marine aquaculture environments, a lytic phage, vB_VnaS-L3, was isolated. It could effectively infect V. natriegens AbY-1805 with a short latent period (40 min) and high burst size (~890 PFU/cell). Treatment with vB_VnaS-L3 significantly reduced the mortality of juvenile abalones and maintained abalone feeding capacity over a 40-day V. natriegens challenge experiment. Comparative genomic and phylogenetic analyses suggested that vB_VnaS-L3 was a novel marine Siphoviridae-family phage. Furthermore, vB_VnaS-L3 had a narrow host range, possibly specific to the pathogenic V. natriegens strains. It also exhibited viability at a wide range of pH, temperature, and salinity. The short latent period, large burst size, high host specificity, and broad environmental adaptation suggest that phage vB_VnaS-L3 could potentially be developed as an alternative antimicrobial for the control and prevention of marine animal infections caused by pathogenic V. natriegens.
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spelling pubmed-96871322022-11-25 Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture Li, Xuejing Liang, Yantao Wang, Zhenhua Yao, Yanyan Chen, Xiaoli Shao, Anran Lu, Longfei Dang, Hongyue Biology (Basel) Article SIMPLE SUMMARY: Vibrio bacteria are ubiquitous and abundant in coastal waters and sediments, and some species are pathogens to humans and marine organisms, leading to foodborne diseases and pandemic infections in humans and mass mortality and economic losses in marine aquaculture. However, the misuse and overuse of antibiotics have led to the emergence and spread of antibiotic-resistant bacteria and resistance genes in marine aquacultural settings and adjacent coastal environments. Bacterial pathogens may also acquire antibiotic resistance via gene mutations and horizontal gene transfers in such environments, making bacterial infectious diseases extremely difficult or even impossible to treat using conventional antibiotic-based therapies. Consequently, phage therapy has received increasing attention in recent years. This study describes the characterization of phage vB_VnaS-L3 from Vibrio natriegens, and explores its potential application as a biocontrol agent to replace antibiotics against pathogenic V. natriegens in juvenile Pacific abalones aquaculture. Our findings showed that phage vB_VnaS-L3 could be a potential alternate biocontrol and prophylactic agent that could effectively inhibit the growth of pathogenic V. natriegens, significantly reduce the mortality of juvenile abalones, and maintain abalone feeding capacity. ABSTRACT: Phage-based pathogen control (i.e., phage therapy) has received increasing scientific attention to reduce and prevent the emergence, transmission, and detrimental effects of antibiotic resistance. In the current study, multidrug-resistant Vibrio natriegens strain AbY-1805 was isolated and tentatively identified as a pathogen causing the death of juvenile Pacific abalones (Haliotis discus hannai Ino). In order to apply phage therapy, instead of antibiotics, to treat and control V. natriegens infections in marine aquaculture environments, a lytic phage, vB_VnaS-L3, was isolated. It could effectively infect V. natriegens AbY-1805 with a short latent period (40 min) and high burst size (~890 PFU/cell). Treatment with vB_VnaS-L3 significantly reduced the mortality of juvenile abalones and maintained abalone feeding capacity over a 40-day V. natriegens challenge experiment. Comparative genomic and phylogenetic analyses suggested that vB_VnaS-L3 was a novel marine Siphoviridae-family phage. Furthermore, vB_VnaS-L3 had a narrow host range, possibly specific to the pathogenic V. natriegens strains. It also exhibited viability at a wide range of pH, temperature, and salinity. The short latent period, large burst size, high host specificity, and broad environmental adaptation suggest that phage vB_VnaS-L3 could potentially be developed as an alternative antimicrobial for the control and prevention of marine animal infections caused by pathogenic V. natriegens. MDPI 2022-11-17 /pmc/articles/PMC9687132/ /pubmed/36421384 http://dx.doi.org/10.3390/biology11111670 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Li, Xuejing
Liang, Yantao
Wang, Zhenhua
Yao, Yanyan
Chen, Xiaoli
Shao, Anran
Lu, Longfei
Dang, Hongyue
Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title_full Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title_fullStr Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title_full_unstemmed Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title_short Isolation and Characterization of a Novel Vibrio natriegens—Infecting Phage and Its Potential Therapeutic Application in Abalone Aquaculture
title_sort isolation and characterization of a novel vibrio natriegens—infecting phage and its potential therapeutic application in abalone aquaculture
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9687132/
https://www.ncbi.nlm.nih.gov/pubmed/36421384
http://dx.doi.org/10.3390/biology11111670
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