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 andmore »
- Authors:
-
- San Diego State Univ., CA (United States). Dept. of Biology; San Diego State Univ., CA (United States). Dept. of Computer Science; Radboud Univ., Nijmegen (Netherlands). Centre for Molecular and Biomolecular Informatics; Federal Univ. of Rio de Janeiro (Brazil). Inst. of Biology. Dept. of Marine Biology
- Oswaldo Cruz Inst., FIOCRUZ, Rio de Janeiro (Brazil). Lab. of Molecular Genetics of Microorganisms
- Life Technologies, Inc, Beverly, MA (United States). Advanced Applications Group
- San Diego State Univ., CA (United States). Dept. of Computer Science; San Diego State Univ., CA (United States). Computational Science Research Center
- Federal Univ. of Rio de Janeiro (Brazil). Inst. of Biology. Dept. of Marine Biology
- San Diego State Univ., CA (United States). Dept. of Computer Science; Life Technologies, Inc, Beverly, MA (United States). Advanced Applications Group
- San Diego State Univ., CA (United States). Dept. of Computer Science
- Haverford College, Haverford, PA (United States). Dept. of Biology
- Obafemi Awolowo University, Ile-Ife (Nigeria). College of Health Sciences. Dept. of Medical Microbiology & Parasitology
- San Diego State Univ., CA (United States). Dept. of Biology
- San Diego State Univ., CA (United States). Dept. of Biology; San Diego State Univ., CA (United States). Dept. of Computer Science; Federal Univ. of Rio de Janeiro (Brazil). Inst. of Biology. Dept. of Marine Biology; San Diego State Univ., CA (United States). Computational Science Research Center; Argonne National Lab. (ANL), Argonne, IL (United States). Mathematics and Computer Science Division
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1626436
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- BMC Genomics
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2164
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity; Functional genomics; Mobile elements; Phages; Niche adaptation; Vibrio; Genome evolution; Genotype-phenotype association; Random forest
Citation Formats
Dutilh, Bas E., Thompson, Cristiane C., Vicente, Ana CP, Marin, Michel A., Lee, Clarence, Silva, Genivaldo GZ, Schmieder, Robert, Andrade, Bruno GN, Chimetto, Luciane, Cuevas, Daniel, Garza, Daniel R., Okeke, Iruka N., Aboderin, Aaron, Spangler, Jessica, Ross, Tristen, Dinsdale, Elizabeth A., Thompson, Fabiano L., Harkins, Timothy T., and Edwards, Robert A. Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions. United States: N. p., 2014.
Web. doi:10.1186/1471-2164-15-654.
Dutilh, Bas E., Thompson, Cristiane C., Vicente, Ana CP, Marin, Michel A., Lee, Clarence, Silva, Genivaldo GZ, Schmieder, Robert, Andrade, Bruno GN, Chimetto, Luciane, Cuevas, Daniel, Garza, Daniel R., Okeke, Iruka N., Aboderin, Aaron, Spangler, Jessica, Ross, Tristen, Dinsdale, Elizabeth A., Thompson, Fabiano L., Harkins, Timothy T., & Edwards, Robert A. Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions. United States. https://doi.org/10.1186/1471-2164-15-654
Dutilh, Bas E., Thompson, Cristiane C., Vicente, Ana CP, Marin, Michel A., Lee, Clarence, Silva, Genivaldo GZ, Schmieder, Robert, Andrade, Bruno GN, Chimetto, Luciane, Cuevas, Daniel, Garza, Daniel R., Okeke, Iruka N., Aboderin, Aaron, Spangler, Jessica, Ross, Tristen, Dinsdale, Elizabeth A., Thompson, Fabiano L., Harkins, Timothy T., and Edwards, Robert A. Tue .
"Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions". United States. https://doi.org/10.1186/1471-2164-15-654. https://www.osti.gov/servlets/purl/1626436.
@article{osti_1626436,
title = {Comparative genomics of 274 Vibrio cholerae genomes reveals mobile functions structuring three niche dimensions},
author = {Dutilh, Bas E. and Thompson, Cristiane C. and Vicente, Ana CP and Marin, Michel A. and Lee, Clarence and Silva, Genivaldo GZ and Schmieder, Robert and Andrade, Bruno GN and Chimetto, Luciane and Cuevas, Daniel and Garza, Daniel R. and Okeke, Iruka N. and Aboderin, Aaron and Spangler, Jessica and Ross, Tristen and Dinsdale, Elizabeth A. and Thompson, Fabiano L. and Harkins, Timothy T. and Edwards, Robert A.},
abstractNote = {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.},
doi = {10.1186/1471-2164-15-654},
journal = {BMC Genomics},
number = 1,
volume = 15,
place = {United States},
year = {Tue Aug 05 00:00:00 EDT 2014},
month = {Tue Aug 05 00:00:00 EDT 2014}
}
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