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A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes

In this study, draft-genome sequencing was conducted for 60 Chinese Morganella isolates, and furthermore, 12 of them were fully sequenced. Then, a total of 166 global sequenced Morganella isolates, including the above 60, were collected to perform average nucleotide identity-based genomic classifica...

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Autores principales: Jing, Ying, Yin, Zhe, Wang, Peng, Guan, Jiayao, Chen, Fangzhou, Wang, Lingling, Li, Xinyue, Mu, Xiaofei, Zhou, Dongsheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865565/
https://www.ncbi.nlm.nih.gov/pubmed/35196820
http://dx.doi.org/10.1128/spectrum.02650-21
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author Jing, Ying
Yin, Zhe
Wang, Peng
Guan, Jiayao
Chen, Fangzhou
Wang, Lingling
Li, Xinyue
Mu, Xiaofei
Zhou, Dongsheng
author_facet Jing, Ying
Yin, Zhe
Wang, Peng
Guan, Jiayao
Chen, Fangzhou
Wang, Lingling
Li, Xinyue
Mu, Xiaofei
Zhou, Dongsheng
author_sort Jing, Ying
collection PubMed
description In this study, draft-genome sequencing was conducted for 60 Chinese Morganella isolates, and furthermore, 12 of them were fully sequenced. Then, a total of 166 global sequenced Morganella isolates, including the above 60, were collected to perform average nucleotide identity-based genomic classification and core single nucleotide polymorphism-based phylogenomic analysis. A genome sequence-based species classification scheme for Morganella was established, and accordingly, the two conventional Morganella species were redefined as two complexes and further divided into four and two genospecies, respectively. At least 88 acquired antimicrobial resistance genes (ARGs) were disseminated in these 166 isolates and were prevalent mostly in the isolates from hospital settings. IS26/IS15DI, IS10 and IS1R, and Tn3-, Tn21-, and Tn7-subfamily unit transposons were frequently presented in these 166 isolates. Furthermore, a detailed sequence comparison was applied to 18 Morganella chromosomal accessory genetic elements (AGEs) from the fully sequenced 12 isolates, together with 5 prototype AGEs from GenBank. These 23 AGEs were divided into eight different groups belonging to composite/unit transposons, transposable prophages, integrative and mobilizable elements, and integrative and conjugative elements, and they harbored at least 52 ARGs involved in resistance to 15 categories of antimicrobials. Eleven of these 23 AGEs acquired large accessory modules, which exhibited complex mosaic structures and contained many antimicrobial resistance loci and associated ARGs. Integration of ARG-containing AGEs into Morganella chromosomes would contribute to the accumulation and dissemination of ARGs in Morganella and enhance the adaption and survival of Morganella under complex and diverse antimicrobial selection pressures. IMPORTANCE This study presents a comprehensive genomic epidemiology analysis on global sequenced Morganella isolates. First, a genome sequence-based species classification scheme for Morganella is established with a higher resolution and accuracy than those of the conventional scheme. Second, the prevalence of accessory genetic elements (AGEs) and associated antimicrobial resistance genes (ARGs) among Morganella isolates is disclosed based on genome sequences. Finally, a detailed sequence comparison of eight groups of 23 AGEs (including 19 Morganella chromosomal AGEs) reveals that Morganella chromosomes have evolved to acquire diverse AGEs harboring different profiles of ARGs and that some of these AGEs harbor large accessory modules that exhibit complex mosaic structures and contain a large number of ARGs. Data presented here provide a deeper understanding of the classification and evolution of Morganella species and also those of ARG-containing AGEs in Morganella at the genomic scale.
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spelling pubmed-88655652022-03-03 A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes Jing, Ying Yin, Zhe Wang, Peng Guan, Jiayao Chen, Fangzhou Wang, Lingling Li, Xinyue Mu, Xiaofei Zhou, Dongsheng Microbiol Spectr Research Article In this study, draft-genome sequencing was conducted for 60 Chinese Morganella isolates, and furthermore, 12 of them were fully sequenced. Then, a total of 166 global sequenced Morganella isolates, including the above 60, were collected to perform average nucleotide identity-based genomic classification and core single nucleotide polymorphism-based phylogenomic analysis. A genome sequence-based species classification scheme for Morganella was established, and accordingly, the two conventional Morganella species were redefined as two complexes and further divided into four and two genospecies, respectively. At least 88 acquired antimicrobial resistance genes (ARGs) were disseminated in these 166 isolates and were prevalent mostly in the isolates from hospital settings. IS26/IS15DI, IS10 and IS1R, and Tn3-, Tn21-, and Tn7-subfamily unit transposons were frequently presented in these 166 isolates. Furthermore, a detailed sequence comparison was applied to 18 Morganella chromosomal accessory genetic elements (AGEs) from the fully sequenced 12 isolates, together with 5 prototype AGEs from GenBank. These 23 AGEs were divided into eight different groups belonging to composite/unit transposons, transposable prophages, integrative and mobilizable elements, and integrative and conjugative elements, and they harbored at least 52 ARGs involved in resistance to 15 categories of antimicrobials. Eleven of these 23 AGEs acquired large accessory modules, which exhibited complex mosaic structures and contained many antimicrobial resistance loci and associated ARGs. Integration of ARG-containing AGEs into Morganella chromosomes would contribute to the accumulation and dissemination of ARGs in Morganella and enhance the adaption and survival of Morganella under complex and diverse antimicrobial selection pressures. IMPORTANCE This study presents a comprehensive genomic epidemiology analysis on global sequenced Morganella isolates. First, a genome sequence-based species classification scheme for Morganella is established with a higher resolution and accuracy than those of the conventional scheme. Second, the prevalence of accessory genetic elements (AGEs) and associated antimicrobial resistance genes (ARGs) among Morganella isolates is disclosed based on genome sequences. Finally, a detailed sequence comparison of eight groups of 23 AGEs (including 19 Morganella chromosomal AGEs) reveals that Morganella chromosomes have evolved to acquire diverse AGEs harboring different profiles of ARGs and that some of these AGEs harbor large accessory modules that exhibit complex mosaic structures and contain a large number of ARGs. Data presented here provide a deeper understanding of the classification and evolution of Morganella species and also those of ARG-containing AGEs in Morganella at the genomic scale. American Society for Microbiology 2022-02-23 /pmc/articles/PMC8865565/ /pubmed/35196820 http://dx.doi.org/10.1128/spectrum.02650-21 Text en Copyright © 2022 Jing et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Jing, Ying
Yin, Zhe
Wang, Peng
Guan, Jiayao
Chen, Fangzhou
Wang, Lingling
Li, Xinyue
Mu, Xiaofei
Zhou, Dongsheng
A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title_full A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title_fullStr A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title_full_unstemmed A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title_short A Genomic and Bioinformatics View of the Classification and Evolution of Morganella Species and Their Chromosomal Accessory Genetic Elements Harboring Antimicrobial Resistance Genes
title_sort genomic and bioinformatics view of the classification and evolution of morganella species and their chromosomal accessory genetic elements harboring antimicrobial resistance genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865565/
https://www.ncbi.nlm.nih.gov/pubmed/35196820
http://dx.doi.org/10.1128/spectrum.02650-21
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