Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis

ABSTRACT Widespread use of antibiotics has enhanced the evolution of highly resilient pathogens and poses a severe risk to human health via coselection of antibiotic resistance genes (ARGs) and virulence factors (VFs). In this study, we rigorously evaluate the abundance relationship and physical lin...

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Autores principales: Yu Pan, Jiaxiong Zeng, Liguan Li, Jintao Yang, Ziyun Tang, Wenguang Xiong, Yafei Li, Sheng Chen, Zhenling Zeng
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:ced6f47d06294de49cf923b342701bdb2021-12-02T19:47:38ZCoexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis10.1128/mSystems.00821-192379-5077https://doaj.org/article/ced6f47d06294de49cf923b342701bdb2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00821-19https://doaj.org/toc/2379-5077ABSTRACT Widespread use of antibiotics has enhanced the evolution of highly resilient pathogens and poses a severe risk to human health via coselection of antibiotic resistance genes (ARGs) and virulence factors (VFs). In this study, we rigorously evaluate the abundance relationship and physical linkage between ARGs and VFs by performing a comprehensive analysis of 9,070 bacterial genomes isolated from multiple species and hosts. The coexistence of ARGs and VFs was observed in bacteria across distinct phyla, pathogenicities, and habitats, especially among human-associated pathogens. The coexistence patterns of gene elements in different habitats and pathogenicity groups were similar, presumably due to frequent gene transfer. A shorter intergenic distance between mobile genetic elements and ARGs/VFs was detected in human/animal-associated bacteria, indicating a higher transfer potential. Increased accumulation of exogenous ARGs/VFs in human pathogens highlights the importance of gene acquisition in the evolution of human commensal bacteria. Overall, the findings provide insights into the genic features of combinations of ARG-VF and expand our understanding of ARG-VF coexistence in bacteria. IMPORTANCE Antibiotic resistance has become a serious global health concern. Despite numerous case studies, a comprehensive analysis of ARG and VF coexistence in bacteria is lacking. In this study, we explore the coexistence profiles of ARGs and VFs in diverse categories of bacteria by using a high-resolution bioinformatics approach. We also provide compelling evidence of unique ARG-VF gene pairs coexisting in specific bacterial genomes and reveal the potential risk associated with the coexistence of ARGs and VFs in organisms in both clinical settings and environments.Yu PanJiaxiong ZengLiguan LiJintao YangZiyun TangWenguang XiongYafei LiSheng ChenZhenling ZengAmerican Society for Microbiologyarticleantibiotic resistancevirulence factorsgene coexistencebacterial genomepathogensnatural environmentMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution DOAJ
collection DOAJ
language EN
topic antibiotic resistance
virulence factors
gene coexistence
bacterial genome
pathogens
natural environment
Microbiology
QR1-502
spellingShingle antibiotic resistance
virulence factors
gene coexistence
bacterial genome
pathogens
natural environment
Microbiology
QR1-502
Yu Pan
Jiaxiong Zeng
Liguan Li
Jintao Yang
Ziyun Tang
Wenguang Xiong
Yafei Li
Sheng Chen
Zhenling Zeng
Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
description ABSTRACT Widespread use of antibiotics has enhanced the evolution of highly resilient pathogens and poses a severe risk to human health via coselection of antibiotic resistance genes (ARGs) and virulence factors (VFs). In this study, we rigorously evaluate the abundance relationship and physical linkage between ARGs and VFs by performing a comprehensive analysis of 9,070 bacterial genomes isolated from multiple species and hosts. The coexistence of ARGs and VFs was observed in bacteria across distinct phyla, pathogenicities, and habitats, especially among human-associated pathogens. The coexistence patterns of gene elements in different habitats and pathogenicity groups were similar, presumably due to frequent gene transfer. A shorter intergenic distance between mobile genetic elements and ARGs/VFs was detected in human/animal-associated bacteria, indicating a higher transfer potential. Increased accumulation of exogenous ARGs/VFs in human pathogens highlights the importance of gene acquisition in the evolution of human commensal bacteria. Overall, the findings provide insights into the genic features of combinations of ARG-VF and expand our understanding of ARG-VF coexistence in bacteria. IMPORTANCE Antibiotic resistance has become a serious global health concern. Despite numerous case studies, a comprehensive analysis of ARG and VF coexistence in bacteria is lacking. In this study, we explore the coexistence profiles of ARGs and VFs in diverse categories of bacteria by using a high-resolution bioinformatics approach. We also provide compelling evidence of unique ARG-VF gene pairs coexisting in specific bacterial genomes and reveal the potential risk associated with the coexistence of ARGs and VFs in organisms in both clinical settings and environments.
format article
author Yu Pan
Jiaxiong Zeng
Liguan Li
Jintao Yang
Ziyun Tang
Wenguang Xiong
Yafei Li
Sheng Chen
Zhenling Zeng
author_facet Yu Pan
Jiaxiong Zeng
Liguan Li
Jintao Yang
Ziyun Tang
Wenguang Xiong
Yafei Li
Sheng Chen
Zhenling Zeng
author_sort Yu Pan
title Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
title_short Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
title_full Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
title_fullStr Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
title_full_unstemmed Coexistence of Antibiotic Resistance Genes and Virulence Factors Deciphered by Large-Scale Complete Genome Analysis
title_sort coexistence of antibiotic resistance genes and virulence factors deciphered by large-scale complete genome analysis
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/ced6f47d06294de49cf923b342701bdb
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