1887

Abstract

subspecies serovar Typhimurium (. Typhimurium) definitive phage type 104 (DT104), subspecies serovar Worthington (. Worthington) and produce ArtA and ArtB (ArtAB) toxin homologues, which catalyse ADP-ribosylation of pertussis toxin-sensitive G protein. ArtAB gene () is encoded on prophage in DT104 and its expression is induced by mitomycin C (MTC) and hydrogen peroxide (HO) that trigger the bacterial SOS response. Although the genetic regulatory mechanism associated with expression is not characterized, it is thought to be associated with prophage induction, which occurs when the RecA-mediated SOS response is triggered. Here we show that subinhibitory concentration of quinolone antibiotics that are SOS-inducing agents, also induce ArtAB production in these strains. Both MTC and fluoroquinolone antibiotics such as enrofloxacin-induced and transcription and -encoding prophage (ArtAB-prophage) in DT104 and . Worthington. However, in , which harbours genes on incomplete prophage, transcription was induced by MTC and enrofloxacin, but prophage induction was not observed. Taken together, these results suggest that SOS response followed by induction of transcription is essential for ArtAB production. HO-mediated induction of ArtAB prophage and efficient production of ArtAB was observed in DT104 but not in . Worthington and . Therefore, induction of expression with HO is strain-specific, and the mode of action of HO as an SOS-inducing agent might be different from those of MTC and quinolone antibiotics.

Funding
This study was supported by the:
  • A grant from the Japan Society for the Promotion of Science KAKENHI (Award 16K18797)
    • Principle Award Recipient: Yukino Tamamura
  • A grant from the Japan Society for the Promotion of Science KAKENHI (Award 18K06001)
    • Principle Award Recipient: Ikuo Uchida
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000939
2020-06-24
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/166/8/785.html?itemId=/content/journal/micro/10.1099/mic.0.000939&mimeType=html&fmt=ahah

References

  1. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J et al. Supplement 2003-2007 (NO. 47) to the White-Kauffmann-Le minor scheme. Res Microbiol 2010; 161:26–29 [View Article][PubMed]
    [Google Scholar]
  2. Threlfall EJ, Frost JA, Ward LR, Rowe B. Epidemic in cattle and humans of Salmonella typhimurium dT 104 with chromosomally integrated multiple drug resistance. Vet Rec 1994; 134:577 [View Article][PubMed]
    [Google Scholar]
  3. Glynn MK, Bopp C, Dewitt W, Dabney P, Mokhtar M et al. Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States. N Engl J Med 1998; 338:1333–1339 [View Article][PubMed]
    [Google Scholar]
  4. Villar RG, Macek MD, Simons S, Hayes PS, Goldoft MJ et al. Investigation of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Washington state. JAMA 1999; 281:1811–1816 [View Article][PubMed]
    [Google Scholar]
  5. Sameshima T, Akiba M, Izumiya H, Terajima J, Tamura K et al. Salmonella typhimurium DT104 from livestock in Japan. Jpn J Infect Dis 2000; 53:15–16[PubMed]
    [Google Scholar]
  6. Leekitcharoenphon P, Hendriksen RS, Le Hello S, Weill F-X, Baggesen DL et al. Global genomic epidemiology of Salmonella enterica serovar typhimurium DT104. Appl Environ Microbiol 2016; 82:2516–2526 [View Article][PubMed]
    [Google Scholar]
  7. Allen CA, Fedorka-Cray PJ, Vazquez-Torres A, Suyemoto M, Altier C et al. In vitro and in vivo assessment of Salmonella enterica serovar Typhimurium DT104 virulence. Infect Immun 2001; 69:4673–4677 [View Article][PubMed]
    [Google Scholar]
  8. Saitoh M, Tanaka K, Nishimori K, Makino S-I, Kanno T et al. The artAB genes encode a putative ADP-ribosyltransferase toxin homologue associated with Salmonella enterica serovar Typhimurium DT104. Microbiology 2005; 151:3089–3096 [View Article][PubMed]
    [Google Scholar]
  9. Uchida I, Ishihara R, Tanaka K, Hata E, Makino S-I et al. Salmonella enterica serotype Typhimurium DT104 ArtA-dependent modification of pertussis toxin-sensitive G proteins in the presence of [32P]NAD. Microbiology 2009; 155:3710–3718 [View Article][PubMed]
    [Google Scholar]
  10. Tamamura Y, Tanaka K, Uchida I. Characterization of pertussis-like toxin from Salmonella spp. that catalyzes ADP-ribosylation of G proteins. Sci Rep 2017; 7:2653 [View Article][PubMed]
    [Google Scholar]
  11. Bielaszewska M, Idelevich EA, Zhang W, Bauwens A, Schaumburg F et al. Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain. Antimicrob Agents Chemother 2012; 56:3277–3282 [View Article][PubMed]
    [Google Scholar]
  12. Fang Y, Mercer RG, McMullen LM, Gänzle MG. Induction of Shiga toxin-encoding prophage by abiotic environmental stress in food. Appl Environ Microbiol 2017; 83:e01378–17 [View Article][PubMed]
    [Google Scholar]
  13. Fogg PCM, Saunders JR, McCarthy AJ, Allison HE. Cumulative effect of prophage burden on Shiga toxin production in Escherichia coli . Microbiology 2012; 158:488–497 [View Article][PubMed]
    [Google Scholar]
  14. Kimmitt PT, Harwood CR, Barer MR. Toxin gene expression by Shiga toxin-producing Escherichia coli: the role of antibiotics and the bacterial SOS response. Emerg Infect Dis 2000; 6:458–465 [View Article][PubMed]
    [Google Scholar]
  15. Licznerska K, Nejman-Faleńczyk B, Bloch S, Dydecka A, Topka G et al. Oxidative stress in shiga toxin production by enterohemorrhagic Escherichia coli . Oxid Med Cell Longev 2016; 2016:1–8 [View Article][PubMed]
    [Google Scholar]
  16. Loś JM, Loś M, Wegrzyn A, Wegrzyn G. Hydrogen peroxide-mediated induction of the Shiga toxin-converting lambdoid prophage ST2-8624 in Escherichia coli O157:H7. FEMS Immunol Med Microbiol 2010; 58:322–329 [View Article][PubMed]
    [Google Scholar]
  17. Matsushiro A, Sato K, Miyamoto H, Yamamura T, Honda T. Induction of prophages of enterohemorrhagic Escherichia coli O157:H7 with norfloxacin. J Bacteriol 1999; 181:2257–2260 [View Article][PubMed]
    [Google Scholar]
  18. Toshima H, Yoshimura A, Arikawa K, Hidaka A, Ogasawara J et al. Enhancement of Shiga toxin production in enterohemorrhagic Escherichia coli serotype O157:H7 by DNase colicins. Appl Environ Microbiol 2007; 73:7582–7588 [View Article][PubMed]
    [Google Scholar]
  19. Chakraborty D, Clark E, Mauro SA, Koudelka GB. Molecular mechanisms governing “Hair-Trigger” induction of shiga toxin-encoding prophages. Viruses 2018; 10:228 [View Article][PubMed]
    [Google Scholar]
  20. Finkelstein RA, Atthasampunna P, Chulasamaya M, Charunmethee P. Pathogenesis of experimental cholera: biologic ativities of purified procholeragen a. J Immunol 1966; 96:440–449[PubMed]
    [Google Scholar]
  21. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial susceptibility Testing, 27th ed. 2017
    [Google Scholar]
  22. Fey A, Eichler S, Flavier S, Christen R, Höfle MG et al. Establishment of a real-time PCR-based approach for accurate quantification of bacterial RNA targets in water, using Salmonella as a model organism. Appl Environ Microbiol 2004; 70:3618–3623 [View Article][PubMed]
    [Google Scholar]
  23. Bonanno L, Petit M-A, Loukiadis E, Michel V, Auvray F. Heterogeneity in induction level, infection ability, and morphology of Shiga toxin-encoding phages (stx phages) from dairy and human shiga toxin-producing Escherichia coli O26:H11 Isolates. Appl Environ Microbiol 2016; 82:2177–2186 [View Article][PubMed]
    [Google Scholar]
  24. Arndt D, Grant JR, Marcu A, Sajed T, Pon A et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 2016; 44:W16–W21 [View Article][PubMed]
    [Google Scholar]
  25. Patel M, Jiang Q, Woodgate R, Cox MM, Goodman MF. A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase V. Crit Rev Biochem Mol Biol 2010; 45:171–184 [View Article][PubMed]
    [Google Scholar]
  26. Baharoglu Z, Mazel D. Sos, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 2014; 38:1126–1145 [View Article][PubMed]
    [Google Scholar]
  27. Mustard JA, Little JW. Analysis of Escherichia coli RecA interactions with LexA, lambda CI, and UmuD by site-directed mutagenesis of recA. J Bacteriol 2000; 182:1659–1670 [View Article][PubMed]
    [Google Scholar]
  28. Tyler JS, Mills MJ, Friedman DI. The operator and early promoter region of the Shiga toxin type 2-encoding bacteriophage 933W and control of toxin expression. J Bacteriol 2004; 186:7670–7679 [View Article][PubMed]
    [Google Scholar]
  29. Wagner PL, Neely MN, Zhang X, Acheson DW, Waldor MK et al. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 2001; 183:2081–2085 [View Article][PubMed]
    [Google Scholar]
  30. Lemire S, Figueroa-Bossi N, Bossi L. Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors. PLoS Genet 2011; 7:e1002149 [View Article][PubMed]
    [Google Scholar]
  31. Loś JM, Loś M, Węgrzyn A, Węgrzyn G. Altruism of Shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results. Front Cell Infect Microbiol 2012; 2:166 [View Article][PubMed]
    [Google Scholar]
  32. Loś JM, Loś M, Wegrzyn G, Wegrzyn A. Differential efficiency of induction of various lambdoid prophages responsible for production of Shiga toxins in response to different induction agents. Microb Pathog 2009; 47:289–298 [View Article][PubMed]
    [Google Scholar]
  33. Loś JM, Loś M, Węgrzyn G. Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria. Future Microbiol 2011; 6:909–924 [View Article][PubMed]
    [Google Scholar]
  34. Glinkowska M, Loś JM, Szambowska A, Czyz A, Całkiewicz J et al. Influence of the Escherichia coli oxyR gene function on lambda prophage maintenance. Arch Microbiol 2010; 192:673–683 [View Article][PubMed]
    [Google Scholar]
  35. Mei G-Y, Tang J, Carey C, Bach S, Kostrzynska M. The effect of oxidative stress on gene expression of Shiga toxin-producing Escherichia coli (STEC) O157:H7 and non-O157 serotypes. Int J Food Microbiol 2015; 215:7–15 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000939
Loading
/content/journal/micro/10.1099/mic.0.000939
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