Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae

Jyoti Verma, Satyabrata Bag, Bipasa Saha, Pawan Kumar, Tarini Shankar Ghosh, Mayanka Dayal, Tarosi Senapati, Seema Mehra, Prasanta Dey, Anbumani Desigamani, Dhirendra Kumar, Preety Rana, Bhoj Kumar, Tushar K. Maiti, Naresh C. Sharma, Rupak K. Bhadra, Ankur Mutreja, G. Balakrish Nair, Thandavarayan Ramamurthy, Bhabatosh Das

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

The Bay of Bengal is known as the epicenter for seeding several devastating cholera outbreaks across the globe. Vibrio cholerae, the etiological agent of cholera, has extraordinary competency to acquire exogenous DNA by horizontal gene transfer (HGT) and adapt them into its genome for structuring metabolic processes, developing drug resistance, and colonizing the human intestine. Antimicrobial resistance (AMR) in V. cholerae has become a global concern. However, little is known about the identity of the resistance traits, source of AMR genes, acquisition process, and stability of the genetic elements linked with resistance genes in V. cholerae. Here we present details of AMR profiles of 443 V. cholerae strains isolated from the stool samples of diarrheal patients from two regions of India. We sequenced the whole genome of multidrug-resistant (MDR) and extensively drug-resistant (XDR) V. cholerae to identify AMR genes and genomic elements that harbor the resistance traits. Our genomic findings were further confirmed by proteome analysis. We also engineered the genome of V. cholerae to monitor the importance of the autonomously replicating plasmid and core genome in the resistance profile. Our findings provided insights into the genomes of recent cholera isolates and identified several acquired traits including plasmids, transposons, integrative conjugative elements (ICEs), pathogenicity islands (PIs), prophages, and gene cassettes that confer fitness to the pathogen. The knowledge generated from this study would help in better understanding of V. cholerae evolution and management of cholera disease by providing clinical guidance on preferred treatment regimens.

Original languageEnglish
Pages (from-to)6226-6231
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number13
DOIs
Publication statusPublished - 01-01-2019
Externally publishedYes

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Vibrio cholerae
Cholera
Genome
Genes
Plasmids
Genetic Phenomena
Prophages
Genomic Islands
Horizontal Gene Transfer
Proteome
Disease Management
Drug Resistance
Intestines
Disease Outbreaks
India
DNA
Pharmaceutical Preparations

All Science Journal Classification (ASJC) codes

  • General

Cite this

Verma, Jyoti ; Bag, Satyabrata ; Saha, Bipasa ; Kumar, Pawan ; Ghosh, Tarini Shankar ; Dayal, Mayanka ; Senapati, Tarosi ; Mehra, Seema ; Dey, Prasanta ; Desigamani, Anbumani ; Kumar, Dhirendra ; Rana, Preety ; Kumar, Bhoj ; Maiti, Tushar K. ; Sharma, Naresh C. ; Bhadra, Rupak K. ; Mutreja, Ankur ; Nair, G. Balakrish ; Ramamurthy, Thandavarayan ; Das, Bhabatosh. / Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 13. pp. 6226-6231.
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abstract = "The Bay of Bengal is known as the epicenter for seeding several devastating cholera outbreaks across the globe. Vibrio cholerae, the etiological agent of cholera, has extraordinary competency to acquire exogenous DNA by horizontal gene transfer (HGT) and adapt them into its genome for structuring metabolic processes, developing drug resistance, and colonizing the human intestine. Antimicrobial resistance (AMR) in V. cholerae has become a global concern. However, little is known about the identity of the resistance traits, source of AMR genes, acquisition process, and stability of the genetic elements linked with resistance genes in V. cholerae. Here we present details of AMR profiles of 443 V. cholerae strains isolated from the stool samples of diarrheal patients from two regions of India. We sequenced the whole genome of multidrug-resistant (MDR) and extensively drug-resistant (XDR) V. cholerae to identify AMR genes and genomic elements that harbor the resistance traits. Our genomic findings were further confirmed by proteome analysis. We also engineered the genome of V. cholerae to monitor the importance of the autonomously replicating plasmid and core genome in the resistance profile. Our findings provided insights into the genomes of recent cholera isolates and identified several acquired traits including plasmids, transposons, integrative conjugative elements (ICEs), pathogenicity islands (PIs), prophages, and gene cassettes that confer fitness to the pathogen. The knowledge generated from this study would help in better understanding of V. cholerae evolution and management of cholera disease by providing clinical guidance on preferred treatment regimens.",
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Verma, J, Bag, S, Saha, B, Kumar, P, Ghosh, TS, Dayal, M, Senapati, T, Mehra, S, Dey, P, Desigamani, A, Kumar, D, Rana, P, Kumar, B, Maiti, TK, Sharma, NC, Bhadra, RK, Mutreja, A, Nair, GB, Ramamurthy, T & Das, B 2019, 'Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 13, pp. 6226-6231. https://doi.org/10.1073/pnas.1900141116

Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. / Verma, Jyoti; Bag, Satyabrata; Saha, Bipasa; Kumar, Pawan; Ghosh, Tarini Shankar; Dayal, Mayanka; Senapati, Tarosi; Mehra, Seema; Dey, Prasanta; Desigamani, Anbumani; Kumar, Dhirendra; Rana, Preety; Kumar, Bhoj; Maiti, Tushar K.; Sharma, Naresh C.; Bhadra, Rupak K.; Mutreja, Ankur; Nair, G. Balakrish; Ramamurthy, Thandavarayan; Das, Bhabatosh.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 13, 01.01.2019, p. 6226-6231.

Research output: Contribution to journalArticle

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T1 - Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae

AU - Verma, Jyoti

AU - Bag, Satyabrata

AU - Saha, Bipasa

AU - Kumar, Pawan

AU - Ghosh, Tarini Shankar

AU - Dayal, Mayanka

AU - Senapati, Tarosi

AU - Mehra, Seema

AU - Dey, Prasanta

AU - Desigamani, Anbumani

AU - Kumar, Dhirendra

AU - Rana, Preety

AU - Kumar, Bhoj

AU - Maiti, Tushar K.

AU - Sharma, Naresh C.

AU - Bhadra, Rupak K.

AU - Mutreja, Ankur

AU - Nair, G. Balakrish

AU - Ramamurthy, Thandavarayan

AU - Das, Bhabatosh

PY - 2019/1/1

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N2 - The Bay of Bengal is known as the epicenter for seeding several devastating cholera outbreaks across the globe. Vibrio cholerae, the etiological agent of cholera, has extraordinary competency to acquire exogenous DNA by horizontal gene transfer (HGT) and adapt them into its genome for structuring metabolic processes, developing drug resistance, and colonizing the human intestine. Antimicrobial resistance (AMR) in V. cholerae has become a global concern. However, little is known about the identity of the resistance traits, source of AMR genes, acquisition process, and stability of the genetic elements linked with resistance genes in V. cholerae. Here we present details of AMR profiles of 443 V. cholerae strains isolated from the stool samples of diarrheal patients from two regions of India. We sequenced the whole genome of multidrug-resistant (MDR) and extensively drug-resistant (XDR) V. cholerae to identify AMR genes and genomic elements that harbor the resistance traits. Our genomic findings were further confirmed by proteome analysis. We also engineered the genome of V. cholerae to monitor the importance of the autonomously replicating plasmid and core genome in the resistance profile. Our findings provided insights into the genomes of recent cholera isolates and identified several acquired traits including plasmids, transposons, integrative conjugative elements (ICEs), pathogenicity islands (PIs), prophages, and gene cassettes that confer fitness to the pathogen. The knowledge generated from this study would help in better understanding of V. cholerae evolution and management of cholera disease by providing clinical guidance on preferred treatment regimens.

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DO - 10.1073/pnas.1900141116

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