High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi

Isolates of Salmonella enterica serovar Typhi (Typhi), a human-restricted bacterial pathogen that causes typhoid, show limited genetic variation. We generated whole-genome sequences for 19 Typhi isolates using 454 (Roche) and Solexa (Illumina) technologies. Isolates, including the previously sequenced CT18 and Ty2 isolates, were selected to represent major nodes in the phylogenetic tree. Comparative analysis showed little evidence of purifying selection, antigenic variation or recombination between isolates. Rather, evolution in the Typhi population seems to be characterized by ongoing loss of gene function, consistent with a small effective population size. The lack of evidence for antigenic variation driven by immune selection is in contrast to strong adaptive selection for mutations conferring antibiotic resistance in Typhi. The observed patterns of genetic isolation and drift are consistent with the proposed key role of asymptomatic carriers of Typhi as the main reservoir of this pathogen, highlighting the need for identification and treatment of carriers.

[1]  A. B. CiusnE,et al.  Typhoid fever. , 1967, The Journal of the Arkansas Medical Society.

[2]  M. Levine,et al.  Precise estimation of the numbers of chronic carriers of Salmonella typhi in Santiago, Chile, an endemic area. , 1982, The Journal of infectious diseases.

[3]  M. Levine,et al.  The use of Moore swabs for isolation of Salmonella typhi from irrigation water in Santiago, Chile. , 1984, The Journal of infectious diseases.

[4]  J. Hörandel,et al.  COSMIC RAYS FROM THE KNEE TO THE SECOND , 2007 .

[5]  J. M. Smith,et al.  Free recombination within Helicobacter pylori. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[6]  William Saurin,et al.  Getting In or Out: Early Segregation Between Importers and Exporters in the Evolution of ATP-Binding Cassette (ABC) Transporters , 1999, Journal of Molecular Evolution.

[7]  J. Andersson,et al.  Genome degradation is an ongoing process in Rickettsia. , 1999, Molecular biology and evolution.

[8]  S. J. Kim,et al.  Viable, but non-culturable, state of a green fluorescence protein-tagged environmental isolate of Salmonella typhi in groundwater and pond water. , 1999, FEMS microbiology letters.

[9]  Kim Rutherford,et al.  Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18 , 2001, Nature.

[10]  I. Stansfield,et al.  Endless possibilities: translation termination and stop codon recognition. , 2001, Microbiology.

[11]  B. Barrell,et al.  Massive gene decay in the leprosy bacillus , 2001, Nature.

[12]  Guy Plunkett,et al.  Comparative Genomics of Salmonellaenterica Serovar Typhi Strains Ty2 and CT18 , 2003, Journal of bacteriology.

[13]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[14]  L. Piddock,et al.  The importance of efflux pumps in bacterial antibiotic resistance. , 2003, The Journal of antimicrobial chemotherapy.

[15]  E. Boyd,et al.  Differences in Gene Content among Salmonella enterica Serovar Typhi Isolates , 2003, Journal of Clinical Microbiology.

[16]  J. Wain,et al.  Composition, Acquisition, and Distribution of the Vi Exopolysaccharide-Encoding Salmonella enterica Pathogenicity Island SPI-7 , 2003, Journal of bacteriology.

[17]  B. Barrell,et al.  Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica , 2003, Nature Genetics.

[18]  P. Youderian,et al.  Precise Excision of the Large Pathogenicity Island, SPI7, in Salmonella enterica Serovar Typhi , 2004, Journal of bacteriology.

[19]  S. Nair,et al.  Salmonella enterica Serovar Typhi Strains from Which SPI7, a 134-Kilobase Island with Genes for Vi Exopolysaccharide and Other Functions, Has Been Deleted , 2004, Journal of bacteriology.

[20]  J. Wain,et al.  The role of prophage-like elements in the diversity of Salmonella enterica serovars. , 2004, Journal of molecular biology.

[21]  Paul Keim,et al.  Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  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.

[23]  Satnam Singh,et al.  Epidemiology of Typhoid Carriers among Blood Donors and Patients with Biliary, Gastrointestinal and Other Related Diseases , 2005, Microbiology and immunology.

[24]  M. Lewis,et al.  Typhoid fever: a massive, single-point source, multidrug-resistant outbreak in Nepal. , 2005, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[25]  Georgios S. Vernikos,et al.  Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands , 2006, Bioinform..

[26]  Paul D van Helden,et al.  Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions , 2006, BMC Evolutionary Biology.

[27]  Daniel Falush,et al.  Genome-wide association mapping in bacteria? , 2006, Trends in microbiology.

[28]  S. Nair,et al.  The acquisition of full fluoroquinolone resistance in Salmonella Typhi by accumulation of point mutations in the topoisomerase targets. , 2006, The Journal of antimicrobial chemotherapy.

[29]  R. Gomulkiewicz,et al.  Source–sink dynamics of virulence evolution , 2006, Nature Reviews Microbiology.

[30]  Eduardo P C Rocha,et al.  Comparisons of dN/dS are time dependent for closely related bacterial genomes. , 2006, Journal of theoretical biology.

[31]  Lisa C. Crossman,et al.  The Complete Genome Sequence and Comparative Genome Analysis of the High Pathogenicity Yersinia enterocolitica Strain 8081 , 2006, PLoS genetics.

[32]  Mark Achtman,et al.  Evolutionary History of Salmonella Typhi , 2006, Science.

[33]  Evan Powell,et al.  Comparative Genomic Analyses of Seventeen Streptococcus pneumoniae Strains: Insights into the Pneumococcal Supragenome , 2007, Journal of bacteriology.

[34]  J. Wain,et al.  Antimicrobial Drug Resistance of Salmonella enterica Serovar Typhi in Asia and Molecular Mechanism of Reduced Susceptibility to the Fluoroquinolones , 2007, Antimicrobial Agents and Chemotherapy.

[35]  Neil Hall,et al.  Advanced sequencing technologies and their wider impact in microbiology , 2007, Journal of Experimental Biology.

[36]  Daniel Falush,et al.  A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination? , 2006, Genome research.

[37]  P. Roumagnac,et al.  Clonal Expansion and Microevolution of Quinolone-Resistant Salmonella enterica Serotype Typhi in Vietnam from 1996 to 2004 , 2007, Journal of Clinical Microbiology.

[38]  B. Coburn,et al.  Salmonella, the host and disease: a brief review , 2007, Immunology and cell biology.

[39]  W. Bruno,et al.  Evolution of Chlamydia trachomatis diversity occurs by widespread interstrain recombination involving hotspots. , 2006, Genome research.

[40]  S. Octavia,et al.  Single-Nucleotide-Polymorphism Typing and Genetic Relationships of Salmonella enterica Serovar Typhi Isolates , 2007, Journal of Clinical Microbiology.

[41]  Samuel I. Miller,et al.  Salmonellae interplay with host cells , 2008, Nature Reviews Microbiology.

[42]  Panagiotis Deloukas,et al.  High-Throughput Genotyping of Salmonella enterica Serovar Typhi Allowing Geographical Assignment of Haplotypes and Pathotypes within an Urban District of Jakarta, Indonesia , 2008, Journal of Clinical Microbiology.