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Volume 159, Issue Pt_6

Inactivation of the LysR regulator Cj1000 of affects host colonization and respiration Free

Abstract

Transcriptional regulation mediates adaptation of pathogens to environmental stimuli and is important for host colonization. The genome sequence reveals a surprisingly small set of regulators, mostly of unknown function, suggesting an intricate regulatory network. Interestingly, lacks the homologues of ubiquitous regulators involved in stress response found in many other Gram-negative bacteria. Nonetheless, is predicted to encode the sole LysR-type regulator in the genome, and thus may be involved in major adaptation pathways. A mutant strain was constructed and found to be attenuated in its ability to colonize 1-day-old chicks. Complementation of the mutation restored the colonization ability to wild-type levels. The mutant strain was also outcompeted in a competitive colonization assay of the piglet intestine. Oxygraphy was carried out for what is believed to be the first time with the Oroboros Oxygraph-2k on and revealed a role for Cj1000 in controlling O consumption. Furthermore, microarray analysis of the mutant revealed both direct and indirect regulatory targets, including genes involved in energy metabolism and oxidative stress defences. These results highlight the importance of Cj1000 regulation in host colonization and in major physiological pathways.

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2013-06-01
2024-04-24
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References

  1. Atack J. M., Kelly D. J. ( 2009). Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol 4:677–690 [View Article][PubMed]
     [Google Scholar]
  2. Avrain L., Vernozy-Rozand C., Kempf I. ( 2004). Evidence for natural horizontal transfer of tetO gene between Campylobacter jejuni strains in chickens. J Appl Microbiol 97:134–140 [View Article][PubMed]
     [Google Scholar]
  3. Bernstein J. A., Khodursky A. B., Lin P. H., Lin-Chao S., Cohen S. N. ( 2002). Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci U S A 99:9697–9702 [View Article][PubMed]
     [Google Scholar]
  4. Berrang M. E., Buhr R. J., Cason J. A., Dickens J. A. ( 2001). Broiler carcass contamination with Campylobacter from feces during defeathering. J Food Prot 64:2063–2066[PubMed]
     [Google Scholar]
  5. Butcher J., Flint A., Stahl M., Stintzi A. ( 2010). Campylobacter Fur and PerR regulons. Iron uptake and homeostasis in microorganisms167–202 Cornelis P., Andrews S. Wymondham, UK: Caister Academic Press;
     [Google Scholar]
  6. Butcher J., Sarvan S., Brunzelle J. S., Couture J. F., Stintzi A. ( 2012). Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation. Proc Natl Acad Sci U S A 109:10047–10052 [View Article][PubMed]
     [Google Scholar]
  7. EFSA ( 2011). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal 9:2090
     [Google Scholar]
  8. Fields J. A., Thompson S. A. ( 2008). Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol 190:3411–3416 [View Article][PubMed]
     [Google Scholar]
  9. Fields J. A., Thompson S. A. ( 2012). Campylobacter jejuni CsrA complements an Escherichia coli csrA mutation for the regulation of biofilm formation, motility and cellular morphology but not glycogen accumulation. BMC Microbiol 12:233 [View Article][PubMed]
     [Google Scholar]
  10. Flint A., Butcher J., Clarke C., Marlow D., Stintzi A. ( 2010). Use of a rabbit soft tissue chamber model to investigate campylobacter jejuni-host interactions. Front Microbiol 1:126 [View Article][PubMed]
     [Google Scholar]
  11. Flint A., Sun Y. Q., Stintzi A. ( 2012). Cj1386 is an ankyrin-containing protein involved in heme trafficking to catalase in Campylobacter jejuni. . J Bacteriol 194:334–345 [View Article][PubMed]
     [Google Scholar]
  12. Gillis D., Cronquist A., Cartter M., Tobin-D'Angelo M., Blythe D., Smith K., Lathrop S., Birkhead G., Cieslak P. & other authors ( 2011). Vital signs: incidence and trends of infection with pathogens transmitted commonly through food–foodborne diseases active surveillance network, 10 U.S. sites, 1996–2010. MMWR Morb Mortal Wkly Rep 60:749–755[PubMed]
     [Google Scholar]
  13. Gnaiger E. ( 2001). Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 128:277–297 [View Article][PubMed]
     [Google Scholar]
  14. Gnaiger E. ( 2008). Polarographic oxygen sensors, the oxygraph, and high-resolution respirometry to assess mitochondrial function. Drug-Induced Mitochondrial Dysfunction325–352 Dykens J. A., Will Y. Hoboken, NJ: Wiley; [View Article]
     [Google Scholar]
  15. Guccione E., Del Rocio Leon-Kempis M., Pearson B. M., Hitchin E., Mulholland F., van Diemen P. M., Stevens M. P., Kelly D. J. ( 2008). Amino acid-dependent growth of Campylobacter jejuni: key roles for aspartase (AspA) under microaerobic and oxygen-limited conditions and identification of AspB (Cj0762), essential for growth on glutamate. Mol Microbiol 69:77–93 [View Article][PubMed]
     [Google Scholar]
  16. Guccione E., Hitchcock A., Hall S. J., Mulholland F., Shearer N., van Vliet A. H., Kelly D. J. ( 2010). Reduction of fumarate, mesaconate and crotonate by Mfr, a novel oxygen-regulated periplasmic reductase in Campylobacter jejuni. . Environ Microbiol 12:576–591 [View Article][PubMed]
     [Google Scholar]
  17. Gundogdu O., Mills D. C., Elmi A., Martin M. J., Wren B. W., Dorrell N. ( 2011). The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J Bacteriol 193:4238–4249 [View Article][PubMed]
     [Google Scholar]
  18. Hoang V. ( 2010). Mechanisms of antimicrobial peptide resistance in Campylobacter.. University of Tennessee, Knoxville, USA:
     [Google Scholar]
  19. Hoang K. V., Stern N. J., Lin J. ( 2011). Development and stability of bacteriocin resistance in Campylobacter spp. J Appl Microbiol 111:1544–1550 [View Article][PubMed]
     [Google Scholar]
  20. Hoffman P. S., Goodman T. G. ( 1982). Respiratory physiology and energy conservation efficiency of Campylobacter jejuni. . J Bacteriol 150:319–326[PubMed]
     [Google Scholar]
  21. Hütter E., Unterluggauer H., Garedew A., Jansen-Dürr P., Gnaiger E. ( 2006). High-resolution respirometry–a modern tool in aging research. Exp Gerontol 41:103–109 [View Article][PubMed]
     [Google Scholar]
  22. Hwang S., Kim M., Ryu S., Jeon B. ( 2011). Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. . PLoS ONE 6:e22300 [View Article][PubMed]
     [Google Scholar]
  23. Hwang S., Zhang Q., Ryu S., Jeon B. ( 2012). Transcriptional regulation of the CmeABC multidrug efflux pump and the KatA catalase by CosR in Campylobacter jejuni. . J Bacteriol 194:6883–6891 [View Article][PubMed]
     [Google Scholar]
  24. Jackson R. J., Elvers K. T., Lee L. J., Gidley M. D., Wainwright L. M., Lightfoot J., Park S. F., Poole R. K. ( 2007). Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J Bacteriol 189:1604–1615 [View Article][PubMed]
     [Google Scholar]
  25. Kaakoush N. O., Sterzenbach T., Miller W. G., Suerbaum S., Mendz G. L. ( 2007). Identification of disulfide reductases in Campylobacterales: a bioinformatics investigation. Antonie van Leeuwenhoek 92:429–441 [View Article][PubMed]
     [Google Scholar]
  26. Lertsethtakarn P., Ottemann K. M., Hendrixson D. R. ( 2011). Motility and chemotaxis in Campylobacter and Helicobacter. . Annu Rev Microbiol 65:389–410 [View Article][PubMed]
     [Google Scholar]
  27. Maddocks S. E., Oyston P. C. ( 2008). Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154:3609–3623 [View Article][PubMed]
     [Google Scholar]
  28. Miller J. F., Dower W. J., Tompkins L. S. ( 1988). High-voltage electroporation of bacteria: genetic transformation of Campylobacter jejuni with plasmid DNA. Proc Natl Acad Sci U S A 85:856–860 [View Article][PubMed]
     [Google Scholar]
  29. Miller W. G., Bates A. H., Horn S. T., Brandl M. T., Wachtel M. R., Mandrell R. E. ( 2000). Detection on surfaces and in Caco-2 cells of Campylobacter jejuni cells transformed with new gfp, yfp, and cfp marker plasmids. Appl Environ Microbiol 66:5426–5436 [View Article][PubMed]
     [Google Scholar]
  30. Myers J. D., Kelly D. J. ( 2005). A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. . Microbiology 151:233–242 [View Article][PubMed]
     [Google Scholar]
  31. Naikare H., Palyada K., Panciera R., Marlow D., Stintzi A. ( 2006). Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74:5433–5444 [View Article][PubMed]
     [Google Scholar]
  32. Palyada K., Threadgill D., Stintzi A. ( 2004). Iron acquisition and regulation in Campylobacter jejuni. . J Bacteriol 186:4714–4729 [View Article][PubMed]
     [Google Scholar]
  33. Palyada K., Sun Y. Q., Flint A., Butcher J., Naikare H., Stintzi A. ( 2009). Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. . BMC Genomics 10:481 [View Article][PubMed]
     [Google Scholar]
  34. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T. & other authors ( 2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [View Article][PubMed]
     [Google Scholar]
  35. Parsek M. R., Ye R. W., Pun P., Chakrabarty A. M. ( 1994). Critical nucleotides in the interaction of a LysR-type regulator with its target promoter region. catBC promoter activation by CatR. J Biol Chem 269:11279–11284[PubMed]
     [Google Scholar]
  36. Pinto A. F., Todorovic S., Hildebrandt P., Yamazaki M., Amano F., Igimi S., Romão C. V., Teixeira M. ( 2011). Desulforubrerythrin from Campylobacter jejuni, a novel multidomain protein. J Biol Inorg Chem 16:501–510 [View Article][PubMed]
     [Google Scholar]
  37. Pittman M. S., Elvers K. T., Lee L., Jones M. A., Poole R. K., Park S. F., Kelly D. J. ( 2007). Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol Microbiol 63:575–590 [View Article][PubMed]
     [Google Scholar]
  38. Pryjma M., Apel D., Huynh S., Parker C. T., Gaynor E. C. ( 2012). FdhTU-modulated formate dehydrogenase expression and electron donor availability enhance recovery of Campylobacter jejuni following host cell infection. J Bacteriol 194:3803–3813 [View Article][PubMed]
     [Google Scholar]
  39. Schell M. A. ( 1993). Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47:597–626 [View Article][PubMed]
     [Google Scholar]
  40. Sellars M. J., Hall S. J., Kelly D. J. ( 2002). Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J Bacteriol 184:4187–4196 [View Article][PubMed]
     [Google Scholar]
  41. Shaw F. L., Mulholland F., Le Gall G., Porcelli I., Hart D. J., Pearson B. M., van Vliet A. H. M. ( 2012). Selenium-dependent biogenesis of formate dehydrogenase in Campylobacter jejuni is controlled by the fdhTU accessory genes. J Bacteriol 194:3814–3823 [CrossRef]
     [Google Scholar]
  42. Shelton C. L., Raffel F. K., Beatty W. L., Johnson S. M., Mason K. M. ( 2011). Sap transporter mediated import and subsequent degradation of antimicrobial peptides in Haemophilus. . PLoS Pathog 7:e1002360 [View Article][PubMed]
     [Google Scholar]
  43. Silva J., Leite D., Fernandes M., Mena C., Gibbs P. A., Teixeira P. ( 2011). Campylobacter spp. as a foodborne pathogen: a review. Front Microbiol 2:200 [View Article][PubMed]
     [Google Scholar]
  44. Stintzi A. ( 2003). Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J Bacteriol 185:2009–2016 [View Article][PubMed]
     [Google Scholar]
  45. Svensson S. L., Davis L. M., MacKichan J. K., Allan B. J., Pajaniappan M., Thompson S. A., Gaynor E. C. ( 2009). The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 71:253–272 [View Article][PubMed]
     [Google Scholar]
  46. Tareen A. M., Dasti J. I., Zautner A. E., Gross U., Lugert R. ( 2011). Sulphite: cytochrome c oxidoreductase deficiency in Campylobacter jejuni reduces motility, host cell adherence and invasion. Microbiology 157:1776–1785 [View Article][PubMed]
     [Google Scholar]
  47. Tropel D., van der Meer J. R. ( 2004). Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68:474–500 [View Article][PubMed]
     [Google Scholar]
  48. Thomas M. T., Shepherd M., Poole R. K., van Vliet A. H. M., Kelly D. J., Pearson B. M. ( 2011). Two respiratory enzyme systems in Campylobacter jejuni NCTC 11168 contribute to growth on l-lactate. Environ Microbiol 13:48–61 [View Article][PubMed]
     [Google Scholar]
  49. Vemuri G. N., Altman E., Sangurdekar D. P., Khodursky A. B., Eiteman M. A. ( 2006). Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl Environ Microbiol 72:3653–3661 [View Article][PubMed]
     [Google Scholar]
  50. Wagner R. ( 2009). Translational components in prokaryotes: genetics and regulation of ribosomes. Enzyclopedia of Life Sciences (ELS) Chichester: Wiley;
     [Google Scholar]
  51. Wang Y., Taylor D. E. ( 1990a). Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94:23–28 [View Article][PubMed]
     [Google Scholar]
  52. Wang Y., Taylor D. E. ( 1990b). Natural transformation in Campylobacter species. J Bacteriol 172:949–955[PubMed]
     [Google Scholar]
  53. Weingarten R. A., Grimes J. L., Olson J. W. ( 2008). Role of Campylobacter jejuni respiratory oxidases and reductases in host colonization. Appl Environ Microbiol 74:1367–1375 [View Article][PubMed]
     [Google Scholar]
  54. Woodall C. A., Jones M. A., Barrow P. A., Hinds J., Marsden G. L., Kelly D. J., Dorrell N., Wren B. W., Maskell D. J. ( 2005). Campylobacter jejuni gene expression in the chick cecum: evidence for adaptation to a low-oxygen environment. Infect Immun 73:5278–5285 [View Article][PubMed]
     [Google Scholar]
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Inactivation of the LysR regulator Cj1000 of Campylobacter jejuni affects host colonization and respiration
Microbiology 159, 1165 (2013); https://doi.org/10.1099/mic.0.062992-0
/content/journal/micro/10.1099/mic.0.062992-0
/content/journal/micro/10.1099/mic.0.062992-0
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