Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype

ABSTRACT Our ability to predict evolutionary trajectories of pathogens is one of the promising leverages to fight against the pandemic disease, yet few studies have addressed this question in situ, due to the difficulty in monitoring the milestone evolutionary events for a given pathogen and in unde...

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Autores principales:	Songzhe Fu, Qian Yang, Qingyao Wang, Bo Pang, Ruiting Lan, Dawei Wei, Baocheng Qu, Ying Liu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	acute hepatopancreatic necrosis disease (AHPND) Vibrio parahaemolyticus mobile genetic elements (MGEs) evolutionary trajectories ISVal1 Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b5e5aed395614bfbb619b2ea3a9c9779
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spelling	oai:doaj.org-article:b5e5aed395614bfbb619b2ea3a9c97792021-12-02T17:07:26ZContinuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype10.1128/mSystems.01254-202379-5077https://doaj.org/article/b5e5aed395614bfbb619b2ea3a9c97792021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01254-20https://doaj.org/toc/2379-5077ABSTRACT Our ability to predict evolutionary trajectories of pathogens is one of the promising leverages to fight against the pandemic disease, yet few studies have addressed this question in situ, due to the difficulty in monitoring the milestone evolutionary events for a given pathogen and in understanding the evolutionary strategies. In this study, we monitored the real-time evolution of Vibrio parahaemolyticus in response to successive antibiotic treatment in three shrimp farms in North China from 2011 to 2018 by whole-genome sequencing. Results showed that the stepwise emergence of resistance was associated with the antibiotic usage. Genomic analysis of resistant isolates showed that the acquisition of the resistant mobile genetic elements flanked by an insertion sequence (ISVal1) closely mirrored the antibiotics used in shrimp farms since 2014. Next, we also identified 50 insertion sites of ISVal1 in the chromosome, which facilitated the formation of pathogenicity islands (PAIs) and fitness islands in the following years. Further, horizontal transfers of a virulent trh-nik-ure genomic island (GI) and two GIs improving the fitness have been observed in two farms since 2016. In this case study, we proposed that the insertion sequence triggered four major evolutionary events during the outbreaks of shrimp disease in three farms, including horizontal transfer of transposon (HTT) (stage 1), the formation of resistance islands (stage 2) and the PAIs (stage 3), and horizontal transfer of the PAIs (stage 4). This study presented the first in vivo evolutionary trajectories for a given bacterial pathogen, which helps us to understand the emergence mechanisms of new genotypes. IMPORTANCE Most human infectious diseases originate from animals. Thus, how to reduce or prevent pandemic zoonoses before they emerge in people is becoming a critical issue. Continuous genomic surveillance of the evolutionary trajectories of potential human pathogens on farms is a promising strategy to realize early warning. Here, we conducted an 8-year surveillance of Vibrio parahaemolyticus in three shrimp farms. The results showed that the use of antibiotics and horizontal transfer of transposons (HTT) drove the evolution of V. parahaemolyticus, which could be divided into four stages: HTT, formation of resistance islands, formation of pathogenicity islands (PAIs), and horizontal transfer of PAIs. This study presented the first in vivo monitoring of evolutionary trajectories for a given bacterial pathogen, providing valuable information for the prevention of pandemic zoonoses.Songzhe FuQian YangQingyao WangBo PangRuiting LanDawei WeiBaocheng QuYing LiuAmerican Society for Microbiologyarticleacute hepatopancreatic necrosis disease (AHPND)Vibrio parahaemolyticusmobile genetic elements (MGEs)evolutionary trajectoriesISVal1MicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	acute hepatopancreatic necrosis disease (AHPND) Vibrio parahaemolyticus mobile genetic elements (MGEs) evolutionary trajectories ISVal1 Microbiology QR1-502
spellingShingle	acute hepatopancreatic necrosis disease (AHPND) Vibrio parahaemolyticus mobile genetic elements (MGEs) evolutionary trajectories ISVal1 Microbiology QR1-502 Songzhe Fu Qian Yang Qingyao Wang Bo Pang Ruiting Lan Dawei Wei Baocheng Qu Ying Liu Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
description	ABSTRACT Our ability to predict evolutionary trajectories of pathogens is one of the promising leverages to fight against the pandemic disease, yet few studies have addressed this question in situ, due to the difficulty in monitoring the milestone evolutionary events for a given pathogen and in understanding the evolutionary strategies. In this study, we monitored the real-time evolution of Vibrio parahaemolyticus in response to successive antibiotic treatment in three shrimp farms in North China from 2011 to 2018 by whole-genome sequencing. Results showed that the stepwise emergence of resistance was associated with the antibiotic usage. Genomic analysis of resistant isolates showed that the acquisition of the resistant mobile genetic elements flanked by an insertion sequence (ISVal1) closely mirrored the antibiotics used in shrimp farms since 2014. Next, we also identified 50 insertion sites of ISVal1 in the chromosome, which facilitated the formation of pathogenicity islands (PAIs) and fitness islands in the following years. Further, horizontal transfers of a virulent trh-nik-ure genomic island (GI) and two GIs improving the fitness have been observed in two farms since 2016. In this case study, we proposed that the insertion sequence triggered four major evolutionary events during the outbreaks of shrimp disease in three farms, including horizontal transfer of transposon (HTT) (stage 1), the formation of resistance islands (stage 2) and the PAIs (stage 3), and horizontal transfer of the PAIs (stage 4). This study presented the first in vivo evolutionary trajectories for a given bacterial pathogen, which helps us to understand the emergence mechanisms of new genotypes. IMPORTANCE Most human infectious diseases originate from animals. Thus, how to reduce or prevent pandemic zoonoses before they emerge in people is becoming a critical issue. Continuous genomic surveillance of the evolutionary trajectories of potential human pathogens on farms is a promising strategy to realize early warning. Here, we conducted an 8-year surveillance of Vibrio parahaemolyticus in three shrimp farms. The results showed that the use of antibiotics and horizontal transfer of transposons (HTT) drove the evolution of V. parahaemolyticus, which could be divided into four stages: HTT, formation of resistance islands, formation of pathogenicity islands (PAIs), and horizontal transfer of PAIs. This study presented the first in vivo monitoring of evolutionary trajectories for a given bacterial pathogen, providing valuable information for the prevention of pandemic zoonoses.
format	article
author	Songzhe Fu Qian Yang Qingyao Wang Bo Pang Ruiting Lan Dawei Wei Baocheng Qu Ying Liu
author_facet	Songzhe Fu Qian Yang Qingyao Wang Bo Pang Ruiting Lan Dawei Wei Baocheng Qu Ying Liu
author_sort	Songzhe Fu
title	Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
title_short	Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
title_full	Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
title_fullStr	Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
title_full_unstemmed	Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype
title_sort	continuous genomic surveillance monitored the <italic toggle="yes">in vivo</italic> evolutionary trajectories of <named-content content-type="genus-species">vibrio parahaemolyticus</named-content> and identified a new virulent genotype
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/b5e5aed395614bfbb619b2ea3a9c9779
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Continuous Genomic Surveillance Monitored the <italic toggle="yes">In Vivo</italic> Evolutionary Trajectories of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> and Identified a New Virulent Genotype

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