Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions

Bas E. Dutilh; Cristiane C. Thompson; Ana C.P. Vicente; Michel A. Marin; Clarence Lee; Genivaldo G.Z. Silva; Robert Schmieder; Bruno G.N. Andrade; Luciane Chimetto; Daniel Cuevas; Daniel R. Garza; Iruka N. Okeke; Aaron O. Aboderin; Jessica Spangler; Tristen Ross; Elizabeth A. Dinsdale; Fabiano L. Thompson; Timothy T. Harkins; Robert A. Edwards

doi:10.1186/1471-2164-15-654

Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions

Bas E. Dutilh, Cristiane C. Thompson, Ana C.P. Vicente, Michel A. Marin, Clarence Lee, Genivaldo G.Z. Silva, Robert Schmieder, Bruno G.N. Andrade, Luciane Chimetto, Daniel Cuevas, Daniel R. Garza, Iruka N. Okeke, Aaron O. Aboderin, Jessica Spangler, Tristen Ross, Elizabeth A. Dinsdale, Fabiano L. Thompson, Timothy T. Harkins, Robert A. Edwards

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

Abstract

Background: Vibrio cholerae is a globally dispersed pathogen that has evolved with humans for centuries, but also includes non-pathogenic environmental strains. Here, we identify the genomic variability underlying this remarkable persistence across the three major niche dimensions space, time, and habitat.Results: Taking an innovative approach of genome-wide association applicable to microbial genomes (GWAS-M), we classify 274 complete V. cholerae genomes by niche, including 39 newly sequenced for this study with the Ion Torrent DNA-sequencing platform. Niche metadata were collected for each strain and analyzed together with comprehensive annotations of genetic and genomic attributes, including point mutations (single-nucleotide polymorphisms, SNPs), protein families, functions and prophages.Conclusions: Our analysis revealed that genomic variations, in particular mobile functions including phages, prophages, transposable elements, and plasmids underlie the metadata structuring in each of the three niche dimensions. This underscores the role of phages and mobile elements as the most rapidly evolving elements in bacterial genomes, creating local endemicity (space), leading to temporal divergence (time), and allowing the invasion of new habitats. Together, we take a data-driven approach for comparative functional genomics that exploits high-volume genome sequencing and annotation, in conjunction with novel statistical and machine learning analyses to identify connections between genotype and phenotype on a genome-wide scale.

Original language	English
Article number	654
Number of pages	11
Journal	BMC Genomics
Volume	15
DOIs	https://doi.org/10.1186/1471-2164-15-654
Publication status	Published - 5 Aug 2014
Externally published	Yes

Bibliographical note

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated

Keywords

Functional genomics
Genome evolution
Genotype-phenotype association
Mobile elements
Niche adaptation
Phages
Random forest
Vibrio

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Dutilh, B. E., Thompson, C. C., Vicente, A. C. P., Marin, M. A., Lee, C., Silva, G. G. Z., Schmieder, R., Andrade, B. G. N., Chimetto, L., Cuevas, D., Garza, D. R., Okeke, I. N., Aboderin, A. O., Spangler, J., Ross, T., Dinsdale, E. A., Thompson, F. L., Harkins, T. T., & Edwards, R. A. (2014). Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions. BMC Genomics, 15, [654]. https://doi.org/10.1186/1471-2164-15-654

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title = "Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions",

abstract = "Background: Vibrio cholerae is a globally dispersed pathogen that has evolved with humans for centuries, but also includes non-pathogenic environmental strains. Here, we identify the genomic variability underlying this remarkable persistence across the three major niche dimensions space, time, and habitat.Results: Taking an innovative approach of genome-wide association applicable to microbial genomes (GWAS-M), we classify 274 complete V. cholerae genomes by niche, including 39 newly sequenced for this study with the Ion Torrent DNA-sequencing platform. Niche metadata were collected for each strain and analyzed together with comprehensive annotations of genetic and genomic attributes, including point mutations (single-nucleotide polymorphisms, SNPs), protein families, functions and prophages.Conclusions: Our analysis revealed that genomic variations, in particular mobile functions including phages, prophages, transposable elements, and plasmids underlie the metadata structuring in each of the three niche dimensions. This underscores the role of phages and mobile elements as the most rapidly evolving elements in bacterial genomes, creating local endemicity (space), leading to temporal divergence (time), and allowing the invasion of new habitats. Together, we take a data-driven approach for comparative functional genomics that exploits high-volume genome sequencing and annotation, in conjunction with novel statistical and machine learning analyses to identify connections between genotype and phenotype on a genome-wide scale.",

keywords = "Functional genomics, Genome evolution, Genotype-phenotype association, Mobile elements, Niche adaptation, Phages, Random forest, Vibrio",

author = "Dutilh, {Bas E.} and Thompson, {Cristiane C.} and Vicente, {Ana C.P.} and Marin, {Michel A.} and Clarence Lee and Silva, {Genivaldo G.Z.} and Robert Schmieder and Andrade, {Bruno G.N.} and Luciane Chimetto and Daniel Cuevas and Garza, {Daniel R.} and Okeke, {Iruka N.} and Aboderin, {Aaron O.} and Jessica Spangler and Tristen Ross and Dinsdale, {Elizabeth A.} and Thompson, {Fabiano L.} and Harkins, {Timothy T.} and Edwards, {Robert A.}",

note = "This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated",

year = "2014",

month = aug,

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doi = "10.1186/1471-2164-15-654",

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Dutilh, BE, Thompson, CC, Vicente, ACP, Marin, MA, Lee, C, Silva, GGZ, Schmieder, R, Andrade, BGN, Chimetto, L, Cuevas, D, Garza, DR, Okeke, IN, Aboderin, AO, Spangler, J, Ross, T, Dinsdale, EA, Thompson, FL, Harkins, TT & Edwards, RA 2014, 'Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions', BMC Genomics, vol. 15, 654. https://doi.org/10.1186/1471-2164-15-654

TY - JOUR

T1 - Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions

AU - Dutilh, Bas E.

AU - Thompson, Cristiane C.

AU - Vicente, Ana C.P.

AU - Marin, Michel A.

AU - Lee, Clarence

AU - Silva, Genivaldo G.Z.

AU - Schmieder, Robert

AU - Andrade, Bruno G.N.

AU - Chimetto, Luciane

AU - Cuevas, Daniel

AU - Garza, Daniel R.

AU - Okeke, Iruka N.

AU - Aboderin, Aaron O.

AU - Spangler, Jessica

AU - Ross, Tristen

AU - Dinsdale, Elizabeth A.

AU - Thompson, Fabiano L.

AU - Harkins, Timothy T.

AU - Edwards, Robert A.

N1 - This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,unless otherwise stated

PY - 2014/8/5

Y1 - 2014/8/5

N2 - Background: Vibrio cholerae is a globally dispersed pathogen that has evolved with humans for centuries, but also includes non-pathogenic environmental strains. Here, we identify the genomic variability underlying this remarkable persistence across the three major niche dimensions space, time, and habitat.Results: Taking an innovative approach of genome-wide association applicable to microbial genomes (GWAS-M), we classify 274 complete V. cholerae genomes by niche, including 39 newly sequenced for this study with the Ion Torrent DNA-sequencing platform. Niche metadata were collected for each strain and analyzed together with comprehensive annotations of genetic and genomic attributes, including point mutations (single-nucleotide polymorphisms, SNPs), protein families, functions and prophages.Conclusions: Our analysis revealed that genomic variations, in particular mobile functions including phages, prophages, transposable elements, and plasmids underlie the metadata structuring in each of the three niche dimensions. This underscores the role of phages and mobile elements as the most rapidly evolving elements in bacterial genomes, creating local endemicity (space), leading to temporal divergence (time), and allowing the invasion of new habitats. Together, we take a data-driven approach for comparative functional genomics that exploits high-volume genome sequencing and annotation, in conjunction with novel statistical and machine learning analyses to identify connections between genotype and phenotype on a genome-wide scale.

AB - Background: Vibrio cholerae is a globally dispersed pathogen that has evolved with humans for centuries, but also includes non-pathogenic environmental strains. Here, we identify the genomic variability underlying this remarkable persistence across the three major niche dimensions space, time, and habitat.Results: Taking an innovative approach of genome-wide association applicable to microbial genomes (GWAS-M), we classify 274 complete V. cholerae genomes by niche, including 39 newly sequenced for this study with the Ion Torrent DNA-sequencing platform. Niche metadata were collected for each strain and analyzed together with comprehensive annotations of genetic and genomic attributes, including point mutations (single-nucleotide polymorphisms, SNPs), protein families, functions and prophages.Conclusions: Our analysis revealed that genomic variations, in particular mobile functions including phages, prophages, transposable elements, and plasmids underlie the metadata structuring in each of the three niche dimensions. This underscores the role of phages and mobile elements as the most rapidly evolving elements in bacterial genomes, creating local endemicity (space), leading to temporal divergence (time), and allowing the invasion of new habitats. Together, we take a data-driven approach for comparative functional genomics that exploits high-volume genome sequencing and annotation, in conjunction with novel statistical and machine learning analyses to identify connections between genotype and phenotype on a genome-wide scale.

KW - Functional genomics

KW - Genome evolution

KW - Genotype-phenotype association

KW - Mobile elements

KW - Niche adaptation

KW - Phages

KW - Random forest

KW - Vibrio

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DO - 10.1186/1471-2164-15-654

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AN - SCOPUS:84906732045

VL - 15

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

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ER -

Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions

Abstract

Bibliographical note

Keywords

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