1887

Abstract

Comparison of the publicly available genomes of the virulent serovar Typhimurium ( Typhimurium) strains SL1344, 14028s and D23580 to that of the virulence-attenuated isolate LT2 revealed the absence of a full sequence of bacteriophage ST64B in the latter. Four selected ST64B regions of unknown function (, , and ) were mapped by PCR in two strain collections: (i) 310 isolates of Typhimurium from human blood or stool samples, and from food, animal and environmental reservoirs; and (ii) 90 isolates belonging to other serovars. The region was found to be unique to Typhimurium and was strongly associated with strains isolated from blood samples (100  and 28.4 % of the blood and non-blood isolates, respectively). The region was cloned into LT2 and knocked out in SL1344, and these strains were compared to wild-type isogenic strains in assays used to predict virulence association. No difference in invasion of the Int407 human cell line was observed between the wild-type and mutated strains, but the isolate carrying the whole ST64B prophage was found to have a slightly better survival in blood. The study showed a high prevalence and a strong association between the prophage ST64B and isolates of Typhimurium collected from blood, and may indicate that such strains constitute a selected subpopulation within this serovar. Further studies are indicated to determine whether the slight increase in blood survival observed in the strain carrying ST64B genes is of paramount importance for systemic infections.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.068221-0
2014-03-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/3/331.html?itemId=/content/journal/jmm/10.1099/jmm.0.068221-0&mimeType=html&fmt=ahah

References

  1. Aguiló A. , Castaño E. , Tauler P. , Guix M. P. , Serra N. , Pons A. . ( 2000; ). Participation of blood cells in the changes of blood amino acid concentrations during maximal exercise. . J Nutr Biochem 11:, 81–86. [CrossRef] [PubMed]
    [Google Scholar]
  2. Alonso A. , Pucciarelli M. G. , Figueroa-Bossi N. , García-del Portillo F. . ( 2005; ). Increased excision of the Salmonella prophage ST64B caused by a deficiency in Dam methylase. . J Bacteriol 187:, 7901–7911. [CrossRef] [PubMed]
    [Google Scholar]
  3. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990; ). Basic local alignment search tool. . J Mol Biol 215:, 403–410.[PubMed] [CrossRef]
    [Google Scholar]
  4. Andreatta M. , Nielsen M. , Møller Aarestrup F. , Lund O. . ( 2010; ). In silico prediction of human pathogenicity in the γ-proteobacteria. . PLoS ONE 5:, e13680. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bhatta D. R. , Bangtrakulnonth A. , Tishyadhigama P. , Saroj S. D. , Bandekar J. R. , Hendriksen R. S. , Kapadnis B. P. . ( 2007; ). Serotyping, PCR, phage-typing and antibiotic sensitivity testing of Salmonella serovars isolated from urban drinking water supply systems of Nepal. . Lett Appl Microbiol 44:, 588–594. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bolton A. J. , Osborne M. P. , Wallis T. S. , Stephen J. . ( 1999; ). Interaction of Salmonella choleraesuis, Salmonella dublin and Salmonella typhimurium with porcine and bovine terminal ileum in vivo . . Microbiology 145:, 2431–2441.[PubMed]
    [Google Scholar]
  7. Bossi L. , Fuentes J. A. , Mora G. , Figueroa-Bossi N. . ( 2003; ). Prophage contribution to bacterial population dynamics. . J Bacteriol 185:, 6467–6471. [CrossRef] [PubMed]
    [Google Scholar]
  8. Brown N. F. , Coombes B. K. , Bishop J. L. , Wickham M. E. , Lowden M. J. , Gal-Mor O. , Goode D. L. , Boyle E. C. , Sanderson K. L. , Finlay B. B. . ( 2011; ). Salmonella phage ST64B encodes a member of the SseK/NleB effector family. . PLoS ONE 6:, e17824. [CrossRef] [PubMed]
    [Google Scholar]
  9. Brüssow H. , Canchaya C. , Hardt W. D. . ( 2004; ). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. . Microbiol Mol Biol Rev 68:, 560–602. [CrossRef] [PubMed]
    [Google Scholar]
  10. Datsenko K. A. , Wanner B. L. . ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. . Proc Natl Acad Sci U S A 97:, 6640–6645. [CrossRef] [PubMed]
    [Google Scholar]
  11. Deng W. , Liou S. R. , Plunkett G. III , Mayhew G. F. , Rose D. J. , Burland V. , Kodoyianni V. , Schwartz D. C. , Blattner F. R. . ( 2003; ). Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. . J Bacteriol 185:, 2330–2337. [CrossRef] [PubMed]
    [Google Scholar]
  12. Fashae K. , Ogunsola F. , Aarestrup F. M. , Hendriksen R. S. . ( 2010; ). Antimicrobial susceptibility and serovars of Salmonella from chickens and humans in Ibadan, Nigeria. . J Infect Dev Ctries 4:, 484–494.[PubMed]
    [Google Scholar]
  13. Feasey N. A. , Dougan G. , Kingsley R. A. , Heyderman R. S. , Gordon M. A. . ( 2012; ). Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. . Lancet 379:, 2489–2499. [CrossRef] [PubMed]
    [Google Scholar]
  14. Figueroa-Bossi N. , Bossi L. . ( 2004; ). Resuscitation of a defective prophage in Salmonella cocultures. . J Bacteriol 186:, 4038–4041. [CrossRef] [PubMed]
    [Google Scholar]
  15. Figueroa-Bossi N. , Uzzau S. , Maloriol D. , Bossi L. . ( 2001; ). Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. . Mol Microbiol 39:, 260–272. [CrossRef] [PubMed]
    [Google Scholar]
  16. Galán J. E. , Wolf-Watz H. . ( 2006; ). Protein delivery into eukaryotic cells by type III secretion machines. . Nature 444:, 567–573. [CrossRef] [PubMed]
    [Google Scholar]
  17. Goh Y. S. , MacLennan C. A. . ( 2013; ). Invasive African nontyphoidal Salmonella requires high levels of complement for cell-free antibody-dependent killing. . J Immunol Methods 387:, 121–129. [CrossRef] [PubMed]
    [Google Scholar]
  18. Haraga A. , Ohlson M. B. , Miller S. I. . ( 2008; ). Salmonellae interplay with host cells. . Nat Rev Microbiol 6:, 53–66. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hasman H. , Mevius D. , Veldman K. , Olesen I. , Aarestrup F. M. . ( 2005; ). β-Lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. . J Antimicrob Chemother 56:, 115–121. [CrossRef] [PubMed]
    [Google Scholar]
  20. Herrero A. , Mendoza M. C. , Rodicio R. , Rodicio M. R. . ( 2008; ). Characterization of pUO-StVR2, a virulence-resistance plasmid evolved from the pSLT virulence plasmid of Salmonella enterica serovar Typhimurium. . Antimicrob Agents Chemother 52:, 4514–4517. [CrossRef] [PubMed]
    [Google Scholar]
  21. Issack M. I. , Hendriksen R. S. , Lun P. L. , Lutchun R. K. , Aarestrup F. M. . ( 2009; ). Salmonella enterica serovar Typhimurium in Mauritius linked to consumption of marlin mousse. . Foodborne Pathog Dis 6:, 739–741. [CrossRef] [PubMed]
    [Google Scholar]
  22. Jacobsen A. , Hendriksen R. S. , Aaresturp F. M. , Ussery D. W. , Friis C. . ( 2011; ). The Salmonella enterica pan-genome. . Microb Ecol 62:, 487–504. [CrossRef] [PubMed]
    [Google Scholar]
  23. Jarvik T. , Smillie C. , Groisman E. A. , Ochman H. . ( 2010; ). Short-term signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. . J Bacteriol 192:, 560–567. [CrossRef] [PubMed]
    [Google Scholar]
  24. Jepson M. A. , Clark M. A. . ( 2001; ). The role of M cells in Salmonella infection. . Microbes Infect 3:, 1183–1190. [CrossRef] [PubMed]
    [Google Scholar]
  25. Katara P. , Grover A. , Kuntal H. , Sharma V. . ( 2011; ). In silico prediction of drug targets in Vibrio cholerae. . Protoplasma 248:, 799–804. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kingsley R. A. , Msefula C. L. , Thomson N. R. , Kariuki S. , Holt K. E. , Gordon M. A. , Harris D. , Clarke L. , Whitehead S. . & other authors ( 2009; ). Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. . Genome Res 19:, 2279–2287. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kröger C. , Dillon S. C. , Cameron A. D. , Papenfort K. , Sivasankaran S. K. , Hokamp K. , Chao Y. , Sittka A. , Hébrard M. . & other authors ( 2012; ). The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. . Proc Natl Acad Sci U S A 109:, E1277–E1286. [CrossRef] [PubMed]
    [Google Scholar]
  28. Leekitcharoenphon P. , Friis C. , Zankari E. , Svendsen C. A. , Price L. B. , Rahmani M. , Herrero-Fresno A. , Fashae K. , Vandenberg O. . & other authors ( 2013; ). Genomics of an emerging clone of Salmonella serovar Typhimurium ST313 from Nigeria and the Democratic Republic of Congo. . J Infect Dev Ctries 7:, 696–706.[PubMed] [CrossRef]
    [Google Scholar]
  29. McClelland M. , Sanderson K. E. , Spieth J. , Clifton S. W. , Latreille P. , Courtney L. , Porwollik S. , Ali J. , Dante M. . & other authors ( 2001; ). Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. . Nature 413:, 852–856. [CrossRef] [PubMed]
    [Google Scholar]
  30. Miao E. A. , Miller S. I. . ( 1999; ). Bacteriophages in the evolution of pathogen-host interactions. . Proc Natl Acad Sci U S A 96:, 9452–9454. [CrossRef] [PubMed]
    [Google Scholar]
  31. Mmolawa P. T. , Schmieger H. , Heuzenroeder M. W. . ( 2003; ). Bacteriophage ST64B, a genetic mosaic of genes from diverse sources isolated from Salmonella enterica serovar typhimurium DT 64. . J Bacteriol 185:, 6481–6485. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mylotte J. M. , Tayara A. . ( 2000; ). Blood cultures: clinical aspects and controversies. . Eur J Clin Microbiol Infect Dis 19:, 157–163. [CrossRef] [PubMed]
    [Google Scholar]
  33. O'Callaghan D. , Charbit A. . ( 1990; ). High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. . Mol Gen Genet 223:, 156–158. [CrossRef] [PubMed]
    [Google Scholar]
  34. Parry C. M. , Hien T. T. , Dougan G. , White N. J. , Farrar J. J. . ( 2002; ). Typhoid fever. . N Engl J Med 347:, 1770–1782. [CrossRef] [PubMed]
    [Google Scholar]
  35. Pizza M. , Scarlato V. , Masignani V. , Giuliani M. M. , Aricò B. , Comanducci M. , Jennings G. T. , Baldi L. , Bartolini E. . & other authors ( 2000; ). Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. . Science 287:, 1816–1820. [CrossRef] [PubMed]
    [Google Scholar]
  36. Richter-Dahlfors A. , Buchan A. M. , Finlay B. B. . ( 1997; ). Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. . J Exp Med 186:, 569–580. [CrossRef] [PubMed]
    [Google Scholar]
  37. Saitoh M. , Tanaka K. , Nishimori K. , Makino S. , Kanno T. , Ishihara R. , Hatama S. , Kitano R. , Kishima M. . & other authors ( 2005; ). The artAB genes encode a putative ADP-ribosyltransferase toxin homologue associated with Salmonella enterica serovar Typhimurium DT104. . Microbiology 151:, 3089–3096. [CrossRef] [PubMed]
    [Google Scholar]
  38. Salcedo S. P. , Noursadeghi M. , Cohen J. , Holden D. W. . ( 2001; ). Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. . Cell Microbiol 3:, 587–597. [CrossRef] [PubMed]
    [Google Scholar]
  39. Schmidt H. , Hensel M. . ( 2004; ). Pathogenicity islands in bacterial pathogenesis. . Clin Microbiol Rev 17:, 14–56. [CrossRef] [PubMed]
    [Google Scholar]
  40. Simmonds R. J. , Harkness R. A. . ( 1981; ). High-performance liquid chromatographic methods for base and nucleoside analysis in extracellular fluids and in cells. . J Chromatogr A 226:, 369–381. [CrossRef] [PubMed]
    [Google Scholar]
  41. Sirichote P. , Hasman H. , Pulsrikarn C. , Schønheyder H. C. , Samulioniené J. , Pornruangmong S. , Bangtrakulnonth A. , Aarestrup F. M. , Hendriksen R. S. . ( 2010; ). Molecular characterization of extended-spectrum cephalosporinase-producing Salmonella enterica serovar Choleraesuis isolates from patients in Thailand and Denmark. . J Clin Microbiol 48:, 883–888. [CrossRef] [PubMed]
    [Google Scholar]
  42. Swords W. E. , Cannon B. M. , Benjamin W. H. Jr . ( 1997; ). Avirulence of LT2 strains of Salmonella typhimurium results from a defective rpoS gene. . Infect Immun 65:, 2451–2453.[PubMed]
    [Google Scholar]
  43. Tapalski D. , Hendriksen R. S. , Hasman H. , Ahrens P. , Aarestrup F. M. . ( 2007; ). Molecular characterisation of multidrug-resistant Salmonella enterica serovar Typhimurium isolates from Gomel region, Belarus. . Clin Microbiol Infect 13:, 1030–1033. [CrossRef] [PubMed]
    [Google Scholar]
  44. Vandenberg O. , Nyarukweba D. Z. , Ndeba P. M. , Hendriksen R. S. , Barzilay E. J. , Schirvel C. , Bisimwa B. B. , Collard J. M. , Aidara Kane A. , Aarestrup F. M. . ( 2010; ). Microbiologic and clinical features of Salmonella species isolated from bacteremic children in eastern Democratic Republic of Congo. . Pediatr Infect Dis J 29:, 504–510.[PubMed]
    [Google Scholar]
  45. Vejborg R. M. , Hancock V. , Schembri M. A. , Klemm P. . ( 2011; ). Comparative genomics of Escherichia coli strains causing urinary tract infections. . Appl Environ Microbiol 77:, 3268–3278. [CrossRef] [PubMed]
    [Google Scholar]
  46. Watson P. R. , Paulin S. M. , Bland A. P. , Jones P. W. , Wallis T. S. . ( 1995; ). Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. . Infect Immun 63:, 2743–2754.[PubMed]
    [Google Scholar]
  47. Wilmes-Riesenberg M. R. , Foster J. W. , Curtiss R. III . ( 1997; ). An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. . Infect Immun 65:, 203–210.[PubMed]
    [Google Scholar]
  48. Xia S. , Hendriksen R. S. , Xie Z. , Huang L. , Zhang J. , Guo W. , Xu B. , Ran L. , Aarestrup F. M. . ( 2009; ). Molecular characterization and antimicrobial susceptibility of Salmonella isolates from infections in humans in Henan Province, China. . J Clin Microbiol 47:, 401–409. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.068221-0
Loading
/content/journal/jmm/10.1099/jmm.0.068221-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error