Genomic and Phenotypic Diversity of Coastal Vibrio cholerae Strains Is Linked to Environmental Factors

ABSTRACT Studies of Vibrio cholerae diversity have focused primarily on pathogenic isolates of the O1 and O139 serotypes. However, autochthonous environmental isolates of this species routinely display more extensive genetic diversity than the primarily clonal pathogenic strains. In this study, genomic and metabolic profiles of 41 non-O1/O139 environmental isolates from central California coastal waters and four clinical strains are used to characterize the core genome and metabolome of V. cholerae. Comparative genome hybridization using microarrays constructed from the fully sequenced V. cholerae O1 El Tor N16961 genome identified 2,787 core genes that approximated the projected species core genome within 1.6%. Core genes are almost universally present in strains with widely different niches, suggesting that these genes are essential for persistence in diverse aquatic environments. In contrast, the dispensable genes and phenotypic traits identified in this study should provide increased fitness for certain niche environments. Environmental parameters, measured in situ during sample collection, are correlated to the presence of specific dispensable genes and metabolic capabilities, including utilization of mannose, sialic acid, citrate, and chitosan oligosaccharides. These results identify gene content and metabolic pathways that are likely selected for in certain coastal environments and may influence V. cholerae population structure in aquatic environments.

[1]  G. Schoolnik,et al.  Detection and Transformation of Genome Segments That Differ within a Coastal Population of Vibrio cholerae Strains , 2007, Applied and Environmental Microbiology.

[2]  A. Paytan,et al.  Human development is linked to multiple water body impairments along the California coast , 2006 .

[3]  P. Karp,et al.  Evidence supporting predicted metabolic pathways for Vibrio cholerae: gene expression data and clinical tests , 2006, Nucleic acids research.

[4]  T. Read,et al.  Shuffling bacterial metabolomes , 2006, Genome Biology.

[5]  M. Lesser.  Oxidative stress in marine environments: biochemistry and physiological ecology. , 2006, Annual review of physiology.

[6]  C. Pál,et al.  Adaptive evolution of bacterial metabolic networks by horizontal gene transfer , 2005, Nature Genetics.

[7]  Jaideep P. Sundaram,et al.  Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Edwards,et al.  A Glimpse into the Expanded Genome Content of Vibrio cholerae through Identification of Genes Present in Environmental Strains , 2005, Journal of bacteriology.

[9]  R. Kucherlapati,et al.  Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  E. Boyd,et al.  Genomic Comparisons of Salmonella enterica Serovar Dublin, Agona, and Typhimurium Strains Recently Isolated from Milk Filters and Bovine Samples from Ireland, Using a Salmonella Microarray , 2005, Applied and Environmental Microbiology.

[11]  Chanathip Pharino,et al.  Genotypic Diversity Within a Natural Coastal Bacterioplankton Population , 2005, Science.

[12]  Robert L Charlebois,et al.  Chlamydia: 780.57 (sd = 1.81), range 778–784, n =7 Cyanobacteria: 820.50 (sd = 23.53), range 776–844, n =8 , 2022 .

[13]  H. Matsuda,et al.  Biased biological functions of horizontally transferred genes in prokaryotic genomes , 2004, Nature Genetics.

[14]  David A Rasko,et al.  Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. , 2004, Nucleic acids research.

[15]  Sunny C. Jiang,et al.  Prevalence of Cholera Toxin Genes (ctxA and zot) among Non-O1/O139 Vibrio cholerae Strains from Newport Bay, California , 2003, Applied and Environmental Microbiology.

[16]  M. Riley,et al.  A molecular phylogeny of enteric bacteria and implications for a bacterial species concept , 2003, Journal of evolutionary biology.

[17]  R. Nichols,et al.  Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. , 2003, Genome research.

[18]  Charles C. Kim,et al.  Significance analysis of lexical bias in microarray data , 2003, BMC Bioinformatics.

[19]  J. Mekalanos,et al.  Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Colwell,et al.  Emergence and evolution of Vibrio cholerae O139 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Susan M. Butler,et al.  Host-induced epidemic spread of the cholera bacterium , 2002, Nature.

[22]  J. Lorén,et al.  Allelic Diversity and Population Structure in Vibrio cholerae O139 Bengal Based on Nucleotide Sequence Analysis , 2002, Journal of bacteriology.

[23]  John F. Heidelberg,et al.  Comparative genomic analysis of Vibrio cholerae: Genes that correlate with cholera endemic and pandemic disease , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  N. Moran,et al.  Deletional bias and the evolution of bacterial genomes. , 2001, Trends in genetics : TIG.

[25]  B. Barrell,et al.  Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. , 2001, Genome research.

[26]  P. Reeves,et al.  When does a clone deserve a name? A perspective on bacterial species based on population genetics. , 2001, Trends in microbiology.

[27]  James M. Musser,et al.  Evolutionary genomics of Staphylococcus aureus: Insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  G. Sherlock,et al.  A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  P. Reeves,et al.  Intraspecies variation in bacterial genomes: the need for a species genome concept. , 2000, Trends in microbiology.

[30]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[31]  Sunny C. Jiang,et al.  Genetic Diversity of Vibrio cholerae in Chesapeake Bay Determined by Amplified Fragment Length Polymorphism Fingerprinting , 2000, Applied and Environmental Microbiology.

[32]  G. Schoolnik,et al.  Comparative genomics of BCG vaccines by whole-genome DNA microarray. , 1999, Science.

[33]  J. Chun,et al.  Analysis of 16S-23S rRNA Intergenic Spacer Regions of Vibrio cholerae and Vibrio mimicus , 1999, Applied and Environmental Microbiology.

[34]  Ruiting Lan,et al.  Evolutionary Relationships of Pathogenic Clones of Vibrio cholerae by Sequence Analysis of Four Housekeeping Genes , 1999, Infection and Immunity.

[35]  S. Wai,et al.  Vibrio cholerae O1 Strain TSI-4 Produces the Exopolysaccharide Materials That Determine Colony Morphology, Stress Resistance, and Biofilm Formation , 1998, Applied and Environmental Microbiology.

[36]  R. Mackie,et al.  Biochemical identification and biological origin of key odor components in livestock waste. , 1998, Journal of animal science.

[37]  H. Drake,et al.  Anaerobic microflora of everglades sediments: effects of nutrients on population profiles and activities , 1996, Applied and environmental microbiology.

[38]  K. Amako,et al.  Effects of chitin and its soluble derivatives on survival of Vibrio cholerae O1 at low temperature , 1987, Applied and environmental microbiology.