1887

Abstract

Copper (Cu)-based biocides are currently used as control measures for both fungal and bacterial diseases in agricultural fields. In this communication, we show that exposure of the bacterial plant pathogen to nonlethal concentrations of Cu ions (75 µM) enhanced expression of genes in OxyR, OhrR and IscR regulons. High levels of catalase, Ohr peroxidase and superoxide dismutase diminished Cu-induced gene expression, suggesting that the production of hydrogen peroxide (HO) and organic hydroperoxides is responsible for Cu-induced gene expression. Despite high expression of antioxidant genes, the CuCl-treated cells were more susceptible to HO killing treatment than the uninduced cells. This phenotype arose from lowered catalase activity in the CuCl-pretreated cells. Thus, exposure to a nonlethal dose of Cu renders vulnerable to HO, even when various genes for peroxide-metabolizing enzymes are highly expressed. Moreover, CuCl-pretreated cells are sensitive to treatment with the redox cycling drug, menadione. No physiological cross-protection response was observed in CuCl-treated cells in a subsequent challenge with killing concentrations of an organic hydroperoxide. As HO production is an important initial plant immune response, defects in HO protection are likely to reduce bacterial survival in plant hosts and enhance the usefulness of copper biocides in controlling bacterial pathogens.

Funding
This study was supported by the:
  • Chulabhorn Research Institute
  • the Center of Excellence on Environmental Health and Toxicology, Science & Technology Postgraduate Education and Research Development Office (PERDO), Ministry of Education, Thailand
  • Chulabhorn Graduate Institute
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2014-02-01
2021-10-26
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References

  1. Ayala-Castro C., Saini A., Outten F. W. ( 2008). Fe-S cluster assembly pathways in bacteria. Microbiol Mol Biol Rev 72:110–125 [View Article][PubMed]
    [Google Scholar]
  2. Banjerdkij P., Vattanaviboon P., Mongkolsuk S. ( 2005). Exposure to cadmium elevates expression of genes in the OxyR and OhrR regulons and induces cross-resistance to peroxide killing treatment in Xanthomonas campestris.. Appl Environ Microbiol 71:1843–1849 [View Article][PubMed]
    [Google Scholar]
  3. Bargabus R. L., Zidack N. K., Sherwood J. E., Jacobsen B. J. ( 2003). Oxidative burst elicited by Bacillus mycoides isolate Bac J, a biological control agent, occurs independently of hypersensitive cell death in sugar beet. Mol Plant Microbe Interact 16:1145–1153 [View Article][PubMed]
    [Google Scholar]
  4. Basim H., Minsavage G. V., Stall R. E., Wang J. F., Shanker S., Jones J. B. ( 2005). Characterization of a unique chromosomal copper resistance gene cluster from Xanthomonas campestris pv. vesicatoria. Appl Environ Microbiol 71:8284–8291 [View Article][PubMed]
    [Google Scholar]
  5. Bolwell G. P., Daudi A. ( 2009). Reactive oxygen species in plant-pathogen interactions. Reactive Oxygen Species in Plant Signalling113–133 del Rio L. A., Puppo A. Berlin, Germany: Springer; [View Article]
    [Google Scholar]
  6. Buranajitpakorn S., Piwkam A., Charoenlap N., Vattanaviboon P., Mongkolsuk S. ( 2011). Genes for hydrogen peroxide detoxification and adaptation contribute to protection against heat shock in Xanthomonas campestris pv. campestris. FEMS Microbiol Lett 317:60–66 [View Article][PubMed]
    [Google Scholar]
  7. Charoenlap N., Eiamphungporn W., Chauvatcharin N., Utamapongchai S., Vattanaviboon P., Mongkolsuk S. ( 2005). OxyR mediated compensatory expression between ahpC and katA and the significance of ahpC in protection from hydrogen peroxide in Xanthomonas campestris.. FEMS Microbiol Lett 249:73–78 [View Article][PubMed]
    [Google Scholar]
  8. Charoenlap N., Buranajitpakorn S., Duang-Nkern J., Namchaiw P., Vattanaviboon P., Mongkolsuk S. ( 2011). Evaluation of the virulence of Xanthomonas campestris pv. campestris mutant strains lacking functional genes in the OxyR regulon. Curr Microbiol 63:232–237 [View Article][PubMed]
    [Google Scholar]
  9. Chauvatcharin N., Atichartpongkul S., Utamapongchai S., Whangsuk W., Vattanaviboon P., Mongkolsuk S. ( 2005). Genetic and physiological analysis of the major OxyR-regulated katA from Xanthomonas campestris pv. phaseoli. Microbiology 151:597–605 [View Article][PubMed]
    [Google Scholar]
  10. Chi B. K., Gronau K., Mäder U., Hessling B., Becher D., Antelmann H. ( 2011). S-bacillithiolation protects against hypochlorite stress in Bacillus subtilis as revealed by transcriptomics and redox proteomics. Mol Cell Proteomics 10:M111.009506 [View Article][PubMed]
    [Google Scholar]
  11. Chillappagari S., Seubert A., Trip H., Kuipers O. P., Marahiel M. A., Miethke M. ( 2010). Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis.. J Bacteriol 192:2512–2524 [View Article][PubMed]
    [Google Scholar]
  12. Chuchue T., Tanboon W., Prapagdee B., Dubbs J. M., Vattanaviboon P., Mongkolsuk S. ( 2006). ohrR and ohr are the primary sensor/regulator and protective genes against organic hydroperoxide stress in Agrobacterium tumefaciens.. J Bacteriol 188:842–851 [View Article][PubMed]
    [Google Scholar]
  13. da Silva A. C., Ferro J. A., Reinach F. C., Farah C. S., Furlan L. R., Quaggio R. B., Monteiro-Vitorello C. B., Van Sluys M. A., Almeida N. F. & other authors ( 2002). Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–463 [View Article][PubMed]
    [Google Scholar]
  14. Feldberg R. S., Carew J. A., Paradise R. ( 1985). Probing Cu(II)/H2O2 damage in DNA with a damage-specific DNA binding protein. J Free Radic Biol Med 1:459–466 [View Article][PubMed]
    [Google Scholar]
  15. Freedman J. H., Ciriolo M. R., Peisach J. ( 1989). The role of glutathione in copper metabolism and toxicity. J Biol Chem 264:5598–5605[PubMed]
    [Google Scholar]
  16. Gu M., Imlay J. A. ( 2011). The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol Microbiol 79:1136–1150 [View Article][PubMed]
    [Google Scholar]
  17. Hopkins D. L. ( 2004). Management of Bacterial Diseases: Chemical Methods London, UK: Taylor & Francis;
    [Google Scholar]
  18. Hsiao Y. M., Liu Y. F., Lee P. Y., Hsu P. C., Tseng S. Y., Pan Y. C. ( 2011). Functional characterization of copA gene encoding multicopper oxidase in Xanthomonas campestris pv. campestris. J Agric Food Chem 59:9290–9302 [View Article][PubMed]
    [Google Scholar]
  19. Jittawuttipoka T., Buranajitpakorn S., Vattanaviboon P., Mongkolsuk S. ( 2009). The catalase-peroxidase KatG is required for virulence of Xanthomonas campestris pv. campestris in a host plant by providing protection against low levels of H2O2.. J Bacteriol 191:7372–7377 [View Article][PubMed]
    [Google Scholar]
  20. Kehrer J. P. ( 2000). The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149:43–50 [View Article][PubMed]
    [Google Scholar]
  21. Kershaw C. J., Brown N. L., Constantinidou C., Patel M. D., Hobman J. L. ( 2005). The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187–1198 [View Article][PubMed]
    [Google Scholar]
  22. Kim S. O., Merchant K., Nudelman R., Beyer W. F. Jr, Keng T., DeAngelo J., Hausladen A., Stamler J. S. ( 2002). OxyR: a molecular code for redox-related signaling. Cell 109:383–396 [View Article][PubMed]
    [Google Scholar]
  23. Kimura T., Nishioka H. ( 1997). Intracellular generation of superoxide by copper sulphate in Escherichia coli.. Mutat Res 389:237–242 [View Article][PubMed]
    [Google Scholar]
  24. Lamb C., Dixon R. A. ( 1997). The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275 [View Article][PubMed]
    [Google Scholar]
  25. Lee Y. A., Hendson M., Panopoulos N. J., Schroth M. N. ( 1994). Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas campestris pv. juglandis: homology with small blue copper proteins and multicopper oxidase. J Bacteriol 176:173–188[PubMed]
    [Google Scholar]
  26. Letelier M. E., Sánchez-Jofré S., Peredo-Silva L., Cortés-Troncoso J., Aracena-Parks P. ( 2010). Mechanisms underlying iron and copper ions toxicity in biological systems: Pro-oxidant activity and protein-binding effects. Chem Biol Interact 188:220–227 [View Article][PubMed]
    [Google Scholar]
  27. Levine A., Tenhaken R., Dixon R., Lamb C. ( 1994). H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593 [View Article][PubMed]
    [Google Scholar]
  28. Macomber L., Imlay J. A. ( 2009). The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci U S A 106:8344–8349 [View Article][PubMed]
    [Google Scholar]
  29. Macomber L., Rensing C., Imlay J. A. ( 2007). Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli.. J Bacteriol 189:1616–1626 [View Article][PubMed]
    [Google Scholar]
  30. Mahavihakanont A., Charoenlap N., Namchaiw P., Eiamphungporn W., Chattrakarn S., Vattanaviboon P., Mongkolsuk S. ( 2012). Novel roles of SoxR, a transcriptional regulator from Xanthomonas campestris, in sensing redox-cycling drugs and regulating a protective gene that have overall implications for bacterial stress physiology and virulence on a host plant. J Bacteriol 194:209–217 [View Article][PubMed]
    [Google Scholar]
  31. McCord J. M., Fridovich I. ( 1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055[PubMed]
    [Google Scholar]
  32. McGuire R. G. ( 1988). Evaluation of bactericidal chemicals for control of Xanthomonas on citrus. Plant Dis 72:1016–1020 [View Article]
    [Google Scholar]
  33. Mongkolsuk S., Vattanaviboon P., Praitaun W. ( 1997). Induced adaptive and cross-protection responses against oxidative stress killing in a bacterial phytopathogen, Xanthomonas oryzae pv. oryzae. FEMS Microbiol Lett 146:217–222 [View Article]
    [Google Scholar]
  34. Panmanee W., Vattanaviboon P., Poole L. B., Mongkolsuk S. ( 2006). Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. J Bacteriol 188:1389–1395 [View Article][PubMed]
    [Google Scholar]
  35. Patikarnmonthon N., Nawapan S., Buranajitpakorn S., Charoenlap N., Mongkolsuk S., Vattanaviboon P. ( 2010). Copper ions potentiate organic hydroperoxide and hydrogen peroxide toxicity through different mechanisms in Xanthomonas campestris pv. campestris. FEMS Microbiol Lett 313:75–80 [View Article][PubMed]
    [Google Scholar]
  36. Qian W., Jia Y., Ren S. X., He Y. Q., Feng J. X., Lu L. F., Sun Q., Ying G., Tang D. J. & other authors ( 2005). Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 15:757–767 [View Article][PubMed]
    [Google Scholar]
  37. Rademacher C., Masepohl B. ( 2012). Copper-responsive gene regulation in bacteria. Microbiology 158:2451–2464 [View Article][PubMed]
    [Google Scholar]
  38. Rae T. D., Schmidt P. J., Pufahl R. A., Culotta V. C., O’Halloran T. V. ( 1999). Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284:805–808 [View Article][PubMed]
    [Google Scholar]
  39. Rensing C., Grass G. ( 2003). Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213 [View Article][PubMed]
    [Google Scholar]
  40. Saenkham P., Eiamphungporn W., Farrand S. K., Vattanaviboon P., Mongkolsuk S. ( 2007). Multiple superoxide dismutases in Agrobacterium tumefaciens: functional analysis, gene regulation, and influence on tumorigenesis. J Bacteriol 189:8807–8817 [View Article][PubMed]
    [Google Scholar]
  41. Somprasong N., Jittawuttipoka T., Duang-Nkern J., Romsang A., Chaiyen P., Schweizer H. P., Vattanaviboon P., Mongkolsuk S. ( 2012). Pseudomonas aeruginosa thiol peroxidase protects against hydrogen peroxide toxicity and displays atypical patterns of gene regulation. J Bacteriol 194:3904–3912 [View Article][PubMed]
    [Google Scholar]
  42. Teitzel G. M., Parsek M. R. ( 2003). Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa.. Appl Environ Microbiol 69:2313–2320 [View Article][PubMed]
    [Google Scholar]
  43. Vattanaviboon P., Mongkolsuk S. ( 2000). Expression analysis and characterization of the mutant of a growth-phase- and starvation-regulated monofunctional catalase gene from Xanthomonas campestris pv. phaseoli. Gene 241:259–265 [View Article][PubMed]
    [Google Scholar]
  44. Vattanaviboon P., Varaluksit T., Mongkolsuk S. ( 1999). Modulation of peroxide stress response by thiol reagents and the role of redox sensor - transcription regulator, OxyR, in mediating the response in Xanthomonas.. FEMS Microbiol Lett 176:471–476 [View Article]
    [Google Scholar]
  45. Vorhölter F. J., Schneiker S., Goesmann A., Krause L., Bekel T., Kaiser O., Linke B., Patschkowski T., Rückert C. & other authors ( 2008). The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J Biotechnol 134:33–45 [View Article][PubMed]
    [Google Scholar]
  46. Wengelnik K., Bonas U. ( 1996). HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol 178:3462–3469[PubMed]
    [Google Scholar]
  47. Yamashoji S., Manome I., Ikedo M. ( 2001). Menadione-catalyzed O2- production by Escherichia coli cells: application of rapid chemiluminescent assay to antimicrobial susceptibility testing. Microbiol Immunol 45:333–340 [View Article][PubMed]
    [Google Scholar]
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