Skip to content
1887

Microbiology Society logo Microbiology

Volume 170, Issue 7

OxyR is required for oxidative stress resistance of the entomopathogenic bacterium and has a minor role during the bacterial interaction with its hosts Open Access

Abstract

is a Gram-negative bacterium, mutualistically associated with the soil nematode , and this nemato-bacterial complex is parasitic for a broad spectrum of insects. The transcriptional regulator OxyR is widely conserved in bacteria and activates the transcription of a set of genes that influence cellular defence against oxidative stress. It is also involved in the virulence of several bacterial pathogens. The aim of this study was to identify the OxyR regulon and investigate its role in the bacterial life cycle. An mutant was constructed in and phenotypically characterized and after reassociation with its nematode partner. OxyR plays a major role during the resistance to oxidative stress . Transcriptome analysis allowed the identification of 59 genes differentially regulated in the mutant compared to the parental strain. , the mutant was able to reassociate with the nematode as efficiently as the control strain. These nemato-bacterial complexes harbouring the mutant symbiont were able to rapidly kill the insect larvae in less than 48 h after infestation, suggesting that factors other than OxyR could also allow to cope with oxidative stress encountered during this phase of infection in insect. The significantly increased number of offspring of the nemato-bacterial complex when reassociated with the mutant compared to the control strain revealed a potential role of OxyR during this symbiotic stage of the bacterial life cycle.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): insect , nematode , oxidative stress , OxyR regulon and symbiosis
Funding
This study was supported by the:
  • Université de Montpellier (Award 2020-UM)
    • Principle Award Recipient: BientzVictoria
  • Agence Nationale de la Recherche (Award ANR-17-CE20-0005)
    • Principle Award Recipient: BrillardJulien
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001481
2024-07-26
2025-05-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/7/mic001481.html?itemId=/content/journal/micro/10.1099/mic.0.001481&mimeType=html&fmt=ahah

References

  1. Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 2008; 77:755–776 [View Article] [PubMed]
     [Google Scholar]
  2. Imlay JA. Transcription factors that defend bacteria against reactive oxygen species. Annu Rev Microbiol 2015; 69:93–108 [View Article] [PubMed]
     [Google Scholar]
  3. Korshunov S, Imlay JA. Two sources of endogenous hydrogen peroxide in Escherichia coli. Mol Microbiol 2010; 75:1389–1401 [View Article] [PubMed]
     [Google Scholar]
  4. Imlay JA, Linn S. Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide. J Bacteriol 1987; 169:2967–2976 [View Article] [PubMed]
     [Google Scholar]
  5. Gupta A, Imlay JA. Escherichia coli induces DNA repair enzymes to protect itself from low-grade hydrogen peroxide stress. Mol Microbiol 2022; 117:754–769 [View Article] [PubMed]
     [Google Scholar]
  6. Sevilla E, Bes MT, González A, Peleato ML, Fillat MF. Redox-based transcriptional regulation in prokaryotes: revisiting model mechanisms. Antioxid Redox Signal 2019; 30:1651–1696 [View Article] [PubMed]
     [Google Scholar]
  7. Chiang SM, Schellhorn HE. Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys 2012; 525:161–169 [View Article] [PubMed]
     [Google Scholar]
  8. Méndez V, Rodríguez-Castro L, Durán RE, Padrón G, Seeger M. The OxyR and SoxR transcriptional regulators are involved in a broad oxidative stress response in Paraburkholderia xenovorans LB400. Biol Res 2022; 55:7 [View Article] [PubMed]
     [Google Scholar]
  9. Toledano MB, Kullik I, Trinh F, Baird PT, Schneider TD et al. Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 1994; 78:897–909 [View Article] [PubMed]
     [Google Scholar]
  10. Jo I, Chung IY, Bae HW, Kim JS, Song S et al. Structural details of the OxyR peroxide-sensing mechanism. Proc Natl Acad Sci U S A 2015; 112:6443–6448 [View Article] [PubMed]
     [Google Scholar]
  11. Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC et al. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 2004; 11:1179–1185 [View Article] [PubMed]
     [Google Scholar]
  12. Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T et al. OxyR: a molecular code for redox-related signaling. Cell 2002; 109:383–396 [View Article] [PubMed]
     [Google Scholar]
  13. Haagmans W, van der Woude M. Phase variation of Ag43 in Escherichia coli: dam-dependent methylation abrogates OxyR binding and OxyR-mediated repression of transcription. Mol Microbiol 2000; 35:877–887 [View Article] [PubMed]
     [Google Scholar]
  14. Payelleville A, Brillard J. Novel identification of bacterial epigenetic regulations would benefit from a better exploitation of methylomic data. Front Microbiol 2021; 12:685670 [View Article] [PubMed]
     [Google Scholar]
  15. Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML et al. Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol 2007; 63:54–68 [View Article] [PubMed]
     [Google Scholar]
  16. Wan F, Kong L, Gao H. Defining the binding determinants of Shewanella oneidensis OxyR: implications for the link between the contracted OxyR regulon and adaptation. J Biol Chem 2018; 293:4085–4096 [View Article] [PubMed]
     [Google Scholar]
  17. Wei Q, Minh PNL, Dötsch A, Hildebrand F, Panmanee W et al. Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res 2012; 40:4320–4333 [View Article] [PubMed]
     [Google Scholar]
  18. Flores-Cruz Z, Allen C. Necessity of OxyR for the hydrogen peroxide stress response and full virulence in Ralstonia solanacearum. Appl Environ Microbiol 2011; 77:6426–6432 [View Article] [PubMed]
     [Google Scholar]
  19. Johnson JR, Russo TA, Drawz SM, Clabots C, Olson R et al. OxyR contributes to the virulence of a Clonal Group A Escherichia coli strain (O17:K+:H18) in animal models of urinary tract infection, subcutaneous infection, and systemic sepsis. Microb Pathog 2013; 64:1–5 [View Article]
     [Google Scholar]
  20. Erickson DL, Russell CW, Johnson KL, Hileman T, Stewart RM. PhoP and OxyR transcriptional regulators contribute to Yersinia pestis virulence and survival within Galleria mellonella. Microb Pathog 2011; 51:389–395 [View Article] [PubMed]
     [Google Scholar]
  21. Lau GW, Britigan BE, Hassett DJ. Pseudomonas aeruginosa OxyR is required for full virulence in rodent and insect models of infection and for resistance to human neutrophils. Infect Immun 2005; 73:2550–2553 [View Article] [PubMed]
     [Google Scholar]
  22. Pagán-Ramos E, Master SS, Pritchett CL, Reimschuessel R, Trucksis M et al. Molecular and physiological effects of mycobacterial oxyR inactivation. J Bacteriol 2006; 188:2674–2680 [View Article] [PubMed]
     [Google Scholar]
  23. Nielsen-LeRoux C, Gaudriault S, Ramarao N, Lereclus D, Givaudan A. How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Curr Opin Microbiol 2012; 15:220–231 [View Article] [PubMed]
     [Google Scholar]
  24. Dreyer J, Malan AP, Dicks LMT. Bacteria of the genus Xenorhabdus, a novel source of bioactive compounds. Front Microbiol 2018; 9:3177 [View Article] [PubMed]
     [Google Scholar]
  25. Herbert EE, Goodrich-Blair H. Friend and foe: the two faces of Xenorhabdus nematophila. . Nat Rev Microbiol 2007; 5:634–646 [View Article] [PubMed]
     [Google Scholar]
  26. Cambon MC, Parthuisot N, Pagès S, Lanois A, Givaudan A et al. Selection of bacterial mutants in late infections: when vector transmission trades off against growth advantage in stationary phase. mBio 2019; 10:e01437-19 [View Article] [PubMed]
     [Google Scholar]
  27. Richards GR, Goodrich-Blair H. Masters of conquest and pillage: Xenorhabdus nematophila global regulators control transitions from virulence to nutrient acquisition. Cell Microbiol 2009; 11:1025–1033 [View Article] [PubMed]
     [Google Scholar]
  28. Givaudan A, Lanois A. FlhDC, the flagellar master operon of Xenorhabdus nematophilus: requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. J Bacteriol 2000; 182:107–115 [View Article] [PubMed]
     [Google Scholar]
  29. Lanois A, Jubelin G, Givaudan A. FliZ, a flagellar regulator, is at the crossroads between motility, haemolysin expression and virulence in the insect pathogenic bacterium Xenorhabdus. Mol Microbiol 2008; 68:516–533 [View Article] [PubMed]
     [Google Scholar]
  30. Reimer D, Cowles KN, Proschak A, Nollmann FI, Dowling AJ et al. Rhabdopeptides as insect-specific virulence factors from entomopathogenic bacteria. Chembiochem 2013; 14:1991–1997 [View Article] [PubMed]
     [Google Scholar]
  31. Snyder H, He H, Owen H, Hanna C, Forst S. Role of Mrx fimbriae of Xenorhabdus nematophila in competitive colonization of the nematode host. Appl Environ Microbiol 2011; 77:7247–7254 [View Article]
     [Google Scholar]
  32. Pothula R, Lee MW, Patricia Stock S. Type 6 secretion system components hcp and vgrG support mutualistic partnership between Xenorhabdus bovienii symbiont and Steinernema jollieti host. J Invertebr Pathol 2023; 198:107925 [View Article] [PubMed]
     [Google Scholar]
  33. Richards GR, Goodrich-Blair H. Examination of Xenorhabdus nematophila lipases in pathogenic and mutualistic host interactions reveals a role for xlpA in nematode progeny production. Appl Environ Microbiol 2010; 76:221–229 [View Article]
     [Google Scholar]
  34. Cowles CE, Goodrich-Blair H. The Xenorhabdus nematophila nilABC genes confer the ability of Xenorhabdus spp. to colonize Steinernema carpocapsae nematodes. J Bacteriol 2008; 190:4121–4128 [View Article] [PubMed]
     [Google Scholar]
  35. Herbert EE, Cowles KN, Goodrich-Blair H. CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila. Appl Environ Microbiol 2007; 73:7826–7836 [View Article] [PubMed]
     [Google Scholar]
  36. Cowles KN, Cowles CE, Richards GR, Martens EC, Goodrich-Blair H. The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol 2007; 9:1311–1323 [View Article] [PubMed]
     [Google Scholar]
  37. Bismuth HD, Brasseur G, Ezraty B, Aussel L. Bacterial genetic approach to the study of reactive oxygen species production in Galleria mellonella during Salmonella infection. Front Cell Infect Microbiol 2021; 11:640112 [View Article] [PubMed]
     [Google Scholar]
  38. Wan F, Feng X, Yin J, Gao H. Distinct H2O2-scavenging system in Yersinia pseudotuberculosis: KatG and AhpC Act together to scavenge endogenous hydrogen peroxide. Front Microbiol 2021; 12:626874 [View Article]
     [Google Scholar]
  39. Akhurst RJ, Boemare NE. Bergey’s Manual of Systematics of Archaea and Bacteria pp 1–14 [View Article]
     [Google Scholar]
  40. Kullik I, Toledano MB, Tartaglia LA, Storz G. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 1995; 177:1275–1284 [View Article] [PubMed]
     [Google Scholar]
  41. Pomposiello PJ, Demple B. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 2001; 19:109–114 [View Article] [PubMed]
     [Google Scholar]
  42. Sund CJ, Rocha ER, Tzianabos AO, Wells WG, Gee JM et al. The Bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence. Mol Microbiol 2008; 67:129–142 [View Article] [PubMed]
     [Google Scholar]
  43. Wen Y, Wen Y, Wen X, Cao S, Huang X et al. OxyR of Haemophilus parasuis is a global transcriptional regulator important in oxidative stress resistance and growth. Gene 2018; 643:107–116 [View Article] [PubMed]
     [Google Scholar]
  44. Imlay JA. Where in the world do bacteria experience oxidative stress?. Environ Microbiol 2019; 21:521–530 [View Article] [PubMed]
     [Google Scholar]
  45. Bjelland S, Seeberg E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 2003; 531:37–80 [View Article] [PubMed]
     [Google Scholar]
  46. Rodríguez-Rojas A, Kim JJ, Johnston PR, Makarova O, Eravci M et al. Non-lethal exposure to H2O2 boosts bacterial survival and evolvability against oxidative stress. PLoS Genet 2020; 16:e1008649 [View Article] [PubMed]
     [Google Scholar]
  47. Lagage V, Chen V, Uphoff S. Adaptation delay causes a burst of mutations in bacteria responding to oxidative stress. EMBO Rep 2023; 24:e55640 [View Article]
     [Google Scholar]
  48. González-Flecha B, Demple B. Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. . J Bacteriol 1997; 179:382–388 [View Article]
     [Google Scholar]
  49. Greenberg JT, Demple B. Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxyR-mutants. EMBO J 1988; 7:2611–2617 [View Article]
     [Google Scholar]
  50. Storz G, Christman MF, Sies H, Ames BN. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc Natl Acad Sci U S A 1987; 84:8917–8921 [View Article] [PubMed]
     [Google Scholar]
  51. Blanco M, Herrera G, Urios A. Increased mutability by oxidative stress in OxyR-deficient Escherichia coli and Salmonella typhimurium cells: clonal occurrence of the mutants during growth on nonselective media. Mutat Res Lett 1995; 346:215–220 [View Article]
     [Google Scholar]
  52. Yamamura E, Nunoshiba T, Kawata M, Yamamoto K. Characterization of spontaneous mutation in the oxyR strain of Escherichia coli. . Biochem Biophys Res Commun 2000; 279:427–432 [View Article] [PubMed]
     [Google Scholar]
  53. Wang J, Liu J, Zhao Y, Sun M, Yu G et al. OxyR contributes to virulence of Acidovorax citrulli by regulating anti-oxidative stress and expression of flagellin FliC and type IV pili PilA. Front Microbiol 2022; 13: [View Article]
     [Google Scholar]
  54. Hoopman TC, Liu W, Joslin SN, Pybus C, Brautigam CA et al. Identification of gene products involved in the oxidative stress response of Moraxella catarrhalis. Infect Immun 2011; 79:745–755 [View Article] [PubMed]
     [Google Scholar]
  55. Loprasert S, Sallabhan R, Whangsuk W, Mongkolsuk S. The Burkholderia pseudomallei oxyR gene: expression analysis and mutant characterization. Gene 2002; 296:161–169 [View Article] [PubMed]
     [Google Scholar]
  56. Lanois A, Ogier JC, Gouzy J, Laroui C, Rouy Z et al. Draft genome sequence and annotation of the entomopathogenic bacterium Xenorhabdus nematophila strain F1. Genome Announc 2013; 1:e00342-13 [View Article] [PubMed]
     [Google Scholar]
  57. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA et al. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 2001; 183:4562–4570 [View Article] [PubMed]
     [Google Scholar]
  58. Sen A, Imlay JA. How microbes defend themselves from incoming hydrogen peroxide. Front Immunol 2021; 12:667343 [View Article] [PubMed]
     [Google Scholar]
  59. Seo Sang W, Kim D, Szubin R, Palsson BO. Genome-wide reconstruction of OxyR and SoxRS transcriptional regulatory networks under oxidative stress in Escherichia coli K-12 MG1655. Cell Rep 2015; 12:1289–1299 [View Article]
     [Google Scholar]
  60. Honma K, Mishima E, Inagaki S, Sharma A. The OxyR homologue in Tannerella forsythia regulates expression of oxidative stress responses and biofilm formation. Microbiology 2009; 155:1912–1922 [View Article]
     [Google Scholar]
  61. Diaz PI, Slakeski N, Reynolds EC, Morona R, Rogers AH et al. Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J Bacteriol 2006; 188:2454–2462 [View Article] [PubMed]
     [Google Scholar]
  62. Zhang B, Gu H, Yang Y, Bai H, Zhao C et al. Molecular mechanisms of AhpC in resistance to oxidative stress in Burkholderia thailandensis. Front Microbiol 2019; 10:1483 [View Article] [PubMed]
     [Google Scholar]
  63. Chandra H, Khandelwal P, Khattri A, Banerjee N. Type 1 fimbriae of insecticidal bacterium Xenorhabdus nematophila is necessary for growth and colonization of its symbiotic host nematode Steinernema carpocapsiae. Environ Microbiol 2008; 10:1285–1295 [View Article] [PubMed]
     [Google Scholar]
  64. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell 1993; 72:165–168 [View Article] [PubMed]
     [Google Scholar]
  65. Siegele DA, Kolter R. Life after log. J Bacteriol 1992; 174:345–348 [View Article] [PubMed]
     [Google Scholar]
  66. Kim D, Hong J-J, Qiu Y, Nagarajan H, Seo J-H et al. Comparative analysis of regulatory elements between Escherichia coli and Klebsiella pneumoniae by genome-wide transcription start site profiling. PLoS Genet 2012; 8:e1002867 [View Article]
     [Google Scholar]
  67. Weerasinghe JP, Dong T, Schertzberg MR, Kirchhof MG, Sun Y et al. Stationary phase expression of the Arginine biosynthetic operon argCBH in Escherichia coli. BMC Microbiol 2006; 6:14 [View Article] [PubMed]
     [Google Scholar]
  68. Hennequin C, Forestier C. OxyR, a LysR-type regulator involved in Klebsiella pneumoniae mucosal and abiotic colonization. Infect Immun 2009; 77:5449–5457 [View Article] [PubMed]
     [Google Scholar]
  69. Ma Z, Russo VC, Rabadi SM, Jen Y, Catlett SV et al. Elucidation of a mechanism of oxidative stress regulation in Francisella tularensis live vaccine strain. Mol Microbiol 2016; 101:856–878 [View Article] [PubMed]
     [Google Scholar]
  70. Bae HW, Cho YH. Mutational analysis of Pseudomonas aeruginosa OxyR to define the regions required for peroxide resistance and acute virulence. Res Microbiol 2012; 163:55–63 [View Article] [PubMed]
     [Google Scholar]
  71. Nakjarung K, Mongkolsuk S, Vattanaviboon P. The oxyR from Agrobacterium tumefaciens: evaluation of its role in the regulation of catalase and peroxide responses. Biochem Biophys Res Commun 2003; 304:41–47 [View Article] [PubMed]
     [Google Scholar]
  72. Charoenlap N, Buranajitpakorn S, Duang-Nkern J, Namchaiw P, Vattanaviboon P et al. Evaluation of the virulence of Xanthomonas campestris pv. campestris mutant strains lacking functional genes in the OxyR regulon. Curr Microbiol 2011; 63:232–237 [View Article] [PubMed]
     [Google Scholar]
  73. Yu C, Wang N, Wu M, Tian F, Chen H et al. OxyR-regulated catalase CatB promotes the virulence in rice via detoxifying hydrogen peroxide in Xanthomonas oryzae pv. oryzae. . BMC Microbiol 2016; 16:269 [View Article]
     [Google Scholar]
  74. Wang H, Naseer N, Chen Y, Zhu AY, Kuai X et al. OxyR2 modulates OxyR1 activity and vibrio cholerae oxidative stress response. Infect Immun 2017; 85: [View Article]
     [Google Scholar]
  75. de Pedro-Jové R, Corral J, Rocafort M, Puigvert M, Azam FL et al. Gene expression changes throughout the life cycle allow a bacterial plant pathogen to persist in diverse environmental habitats. PLoS Pathog 2023; 19:e1011888 [View Article]
     [Google Scholar]
  76. Cappelli EA, do Espírito Santo Cucinelli A, Simpson-Louredo L, Canellas MEF, Antunes CA et al. Insights of OxyR role in mechanisms of host-pathogen interaction of Corynebacterium diphtheriae. Braz J Microbiol 2022; 53:583–594 [View Article] [PubMed]
     [Google Scholar]
  77. Brillard J, Ribeiro C, Boemare N, Brehélin M, Givaudan A. Two distinct hemolytic activities in Xenorhabdus nematophila are active against immunocompetent insect cells. Appl Environ Microbiol 2001; 67:2515–2525 [View Article] [PubMed]
     [Google Scholar]
  78. Song CJ, Seo S, Shrestha S, Kim Y. Bacterial metabolites of an entomopathogenic bacterium, Xenorhabdus nematophila, inhibit a catalytic activity of phenoloxidase of the diamondback moth, Plutella xylostella. J Microbiol Biotechnol 2011; 21:317–322 [PubMed]
     [Google Scholar]
  79. Parks SC, Nguyen S, Nasrolahi S, Bhat C, Juncaj D et al. Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways. PLoS Pathog 2021; 17:e1010027 [View Article] [PubMed]
     [Google Scholar]
  80. Ogier J-C, Pagès S, Frayssinet M, Gaudriault S. Entomopathogenic nematode-associated microbiota: from monoxenic paradigm to pathobiome. Microbiome 2020; 8:25 [View Article] [PubMed]
     [Google Scholar]
  81. Anes J, Dever K, Eshwar A, Nguyen S, Cao Y et al. Analysis of the oxidative stress regulon identifies soxS as a genetic target for resistance reversal in multidrug-resistant Klebsiella pneumoniae. mBio 2021; 12:e0086721 [View Article] [PubMed]
     [Google Scholar]
  82. Teixeira FL, Costa SB, Pauer H, de Almeida BJ, Oliveira ACSC et al. Characterization of the oxidative stress response regulatory network in Bacteroides fragilis: an interaction between BmoR and OxyR regulons promotes abscess formation in a model of intra-abdominal infection. Anaerobe 2022; 78:102668 [View Article] [PubMed]
     [Google Scholar]
  83. Wang B, Li K, Wu G, Xu Z, Hou R et al. Sulforaphane, a secondary metabolite in crucifers, inhibits the oxidative stress adaptation and virulence of Xanthomonasby directly targeting OxyR. Mol Plant Pathol 2022; 23:1508–1523 [View Article]
     [Google Scholar]
  84. Mucci NC, Jones KA, Cao M, Wyatt MR II, Foye S et al. Apex predator nematodes and meso-predator bacteria consume their basal insect prey through discrete stages of chemical transformations. mSystems 2022; 7:e0031222 [View Article]
     [Google Scholar]
  85. Bölker M, Kahmann R. The Escherichia coli regulatory protein OxyR discriminates between methylated and unmethylated states of the phage Mu mom promoter. EMBO J 1989; 8:2403–2410 [View Article]
     [Google Scholar]
  86. 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]
  87. Storz G, Tartaglia LA, Ames BN. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 1990; 248:189–194 [View Article]
     [Google Scholar]
  88. Ogier JC, Akhurst R, Boemare N, Gaudriault S. The endosymbiont and the second bacterial circle of entomopathogenic nematodes. Trends Microbiol 2023; 31:629–643 [View Article] [PubMed]
     [Google Scholar]
  89. Boemare NE, Akhurst RJ. Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacteriaceae). J Gen Microbiol 1988; 134:751–761 [View Article] [PubMed]
     [Google Scholar]
  90. Ginibre N, Legrand L, Bientz V, Ogier JC, Lanois A et al. Diverse roles for a conserved DNA-methyltransferase in the entomopathogenic bacterium Xenorhabdus. Int J Mol Sci 2022; 23:11981 [View Article]
     [Google Scholar]
  91. Givaudan A, Baghdiguian S, Lanois A, Boemare N. Swarming and swimming changes concomitant with phase variation in Xenorhabdus nematophilus. Appl Environ Microbiol 1995; 61:1408–1413 [View Article]
     [Google Scholar]
  92. Payelleville A, Lanois A, Gislard M, Dubois E, Roche D et al. DNA Adenine Methyltransferase (Dam) overexpression impairs Photorhabdus luminescens motility and virulence. Front Microbiol 2017; 8:1671 [View Article] [PubMed]
     [Google Scholar]
  93. Kim H, Xue X. Detection of total reactive oxygen species in adherent cells by 2’,7’-dichlorodihydrofluorescein diacetate staining. J Vis Exp 2020 [View Article] [PubMed]
     [Google Scholar]
  94. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC et al. Primer3--new capabilities and interfaces. Nucleic Acids Res 2012; 40:e115 [View Article] [PubMed]
     [Google Scholar]
  95. Brillard J, Lereclus D. Characterization of a small PlcR-regulated gene co-expressed with cereolysin O. BMC Microbiol 2007; 7:52 [View Article] [PubMed]
     [Google Scholar]
  96. Brillard J, Duchaud E, Boemare N, Kunst F, Givaudan A. The PhlA hemolysin from the entomopathogenic bacterium Photorhabdus luminescens belongs to the two-partner secretion family of hemolysins. J Bacteriol 2002; 184:3871–3878 [View Article] [PubMed]
     [Google Scholar]
  97. Brugirard-Ricaud K, Duchaud E, Givaudan A, Girard PA, Kunst F et al. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell Microbiol 2005; 7:363–371 [View Article] [PubMed]
     [Google Scholar]
  98. Derzelle S, Turlin E, Duchaud E, Pages S, Kunst F et al. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescensIs essential for virulence in insects. J Bacteriol 2004; 184:1270–1279 [View Article]
     [Google Scholar]
  99. Payelleville A, Legrand L, Ogier J-C, Roques C, Roulet A et al. The complete methylome of an entomopathogenic bacterium reveals the existence of loci with unmethylated adenines. Sci Rep 2018; 8:12091 [View Article]
     [Google Scholar]
  100. Li H, Durbin R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article]
     [Google Scholar]
  101. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article]
     [Google Scholar]
  102. Vallenet D, Calteau A, Dubois M, Amours P, Bazin A et al. MicroScope: an integrated platform for the annotation and exploration of microbial gene functions through genomic, pangenomic and metabolic comparative analysis. Nucleic Acids Res 2020; 48:D579–D589 [View Article] [PubMed]
     [Google Scholar]
  103. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5:R80 [View Article] [PubMed]
     [Google Scholar]
  104. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15:550 [View Article] [PubMed]
     [Google Scholar]
  105. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002; 30:e36 [View Article] [PubMed]
     [Google Scholar]
  106. Huot L, Bigourdan A, Pagès S, Ogier J-C, Girard P-A et al. Partner-specific induction of Spodoptera frugiperda immune genes in response to the entomopathogenic nematobacterial complex Steinernema carpocapsae-Xenorhabdus nematophila. Dev Comp Immunol 2020; 108:103676 [View Article] [PubMed]
     [Google Scholar]
  107. Cambon MC, Lafont P, Frayssinet M, Lanois A, Ogier J-C et al. Bacterial community profile after the lethal infection of Steinernema-Xenorhabdus pairs into soil-reared Tenebrio molitor larvae. FEMS Microbiol Ecol 2020; 96:fiaa009 [View Article] [PubMed]
     [Google Scholar]
  108. Payelleville A, Blackburn D, Lanois A, Pagès S, Cambon MC et al. Role of the Photorhabdus Dam methyltransferase during interactions with its invertebrate hosts. PLoS One 2019; 14:e0212655 [View Article] [PubMed]
     [Google Scholar]
  109. White GF. A method for obtaining infective nematodes larvae from cultures. Science 1927; 66:302–303 [View Article] [PubMed]
     [Google Scholar]
  110. Paulick A, Koerdt A, Lassak J, Huntley S, Wilms I et al. Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol Microbiol 2009; 71:836–850 [View Article] [PubMed]
     [Google Scholar]
  111. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA et al. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 1995; 166:175–176 [View Article] [PubMed]
     [Google Scholar]
  112. Jubelin G, Pagès S, Lanois A, Boyer M-H, Gaudriault S et al. Studies of the dynamic expression of the Xenorhabdus FliAZ regulon reveal atypical iron-dependent regulation of the flagellin and haemolysin genes during insect infection. Environ Microbiol 2011; 13:1271–1284 [View Article] [PubMed]
     [Google Scholar]
  113. Fellay R, Frey J, Krisch H. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 1987; 52:147–154 [View Article] [PubMed]
     [Google Scholar]
  114. Quandt J, Hynes MF. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 1993; 127:15–21 [View Article] [PubMed]
     [Google Scholar]
  115. Miller WG, Leveau JH, Lindow SE. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol Plant Microbe Interact 2000; 13:1243–1250 [View Article] [PubMed]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.001481
Loading
OxyR is required for oxidative stress resistance of the entomopathogenic bacterium Xenorhabdus nematophila and has a minor role during the bacterial interaction with its hosts
Microbiology 170, 001481 (2024); https://doi.org/10.1099/mic.0.001481
/content/journal/micro/10.1099/mic.0.001481
/content/journal/micro/10.1099/mic.0.001481
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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