1887

Abstract

Bacteria belonging to the Alphaproteobacteria normally harbour multiple copies of the heat shock sigma factor (known as σ, σ or RpoH). , a non-photosynthetic rhizobacterium, harbours five copies of genes, one of which is an homologue. The genes around the locus in show synteny with that found in rhizobia. The of was able to complement the temperature-sensitive phenotype of the mutant. Inactivation of in results in increased sensitivity to methylene blue and to triphenyl tetrazolium chloride (TTC). Exposure of to TTC and the singlet oxygen-generating agent methylene blue induced several-fold higher expression of . Comparison of the proteome of with its deletion mutant and with an strain overexpressing revealed chaperone GroEL, elongation factors (Ef-Tu and EF-G), peptidyl prolyl isomerase, and peptide methionine sulfoxide reductase as the major proteins whose expression was controlled by RpoH2. Here, we show that the RpoH2 sigma factor-controlled photooxidative stress response in is similar to that in the photosynthetic bacterium , but that RpoH2 is not involved in the detoxification of methylglyoxal in .

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2012-12-01
2019-12-07
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References

  1. Arsène F. , Tomoyasu T. , Bukau B. . ( 2000; ). The heat shock response of Escherichia coli . . Int J Food Microbiol 55:, 3–9. [CrossRef] [PubMed]
    [Google Scholar]
  2. Beloti V. , Barros M. A. F. , De Freitas J. C. , Nero L. A. , De Souza J. A. , Santana E. H. W. , Franco B. D. G. M. . ( 1999; ). Frequency of 2,3,5-triphenyltetrazolium chloride (TTC) non-reducing bacteria in pasteurized milk. . Rev Microbiol 30:, 137–140. [CrossRef]
    [Google Scholar]
  3. Berghoff B. A. , Glaeser J. , Nuss A. M. , Zobawa M. , Lottspeich F. , Klug G. . ( 2011; ). Anoxygenic photosynthesis and photooxidative stress: a particular challenge for Roseobacter . . Environ Microbiol 13:, 775–791. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bittner A. N. , Oke V. . ( 2006; ). Multiple groESL operons are not key targets of RpoH1 and RpoH2 in Sinorhizobium meliloti . . J Bacteriol 188:, 3507–3515. [CrossRef] [PubMed]
    [Google Scholar]
  5. Brot N. , Weissbach H. . ( 2000; ). Peptide methionine sulfoxide reductase: biochemistry and physiological role. . Biopolymers 55:, 288–296. [CrossRef] [PubMed]
    [Google Scholar]
  6. Butcher R. G. . ( 1978; ). Oxygen and the production of formazan from neotetrazolium chloride. . Histochemistry 56:, 329–340. [CrossRef] [PubMed]
    [Google Scholar]
  7. Caldas T. , Demont-Caulet N. , Ghazi A. , Richarme G. . ( 1999; ). Thermoprotection by glycine betaine and choline. . Microbiology 145:, 2543–2548.[PubMed]
    [Google Scholar]
  8. Caldas T. , Laalami S. , Richarme G. . ( 2000; ). Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. . J Biol Chem 275:, 855–860. [CrossRef] [PubMed]
    [Google Scholar]
  9. Chattopadhyay M. K. , Kern R. , Mistou M. Y. , Dandekar A. M. , Uratsu S. L. , Richarme G. . ( 2004; ). The chemical chaperone proline relieves the thermosensitivity of a dnaK deletion mutant at 42°C. . J Bacteriol 186:, 8149–8152. [CrossRef] [PubMed]
    [Google Scholar]
  10. da Silva Neto J. F. , Koide T. , Gomes S. L. , Marques M. V. . ( 2007; ). The single extracytoplasmic-function sigma factor of Xylella fastidiosa is involved in the heat shock response and presents an unusual regulatory mechanism. . J Bacteriol 189:, 551–560. [CrossRef] [PubMed]
    [Google Scholar]
  11. Fibach-Paldi S. , Burdman S. , Okon Y. . ( 2012; ). Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense . . FEMS Microbiol Lett 326:, 99–108. [CrossRef] [PubMed]
    [Google Scholar]
  12. Green H. A. , Donohue T. J. . ( 2006; ). Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. . J Bacteriol 188:, 5712–5721. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gunz F. W. . ( 1948; ). Reduction of tetrazolium salts by some biological agents. . Nature 162:, 98.[PubMed]
    [Google Scholar]
  14. Hartl F. U. , Hayer-Hartl M. . ( 2002; ). Molecular chaperones in the cytosol: from nascent chain to folded protein. . Science 295:, 1852–1858. [CrossRef] [PubMed]
    [Google Scholar]
  15. Islam M. M. , Hoque M. A. , Okuma E. , Banu M. N. , Shimoishi Y. , Nakamura Y. , Murata Y. . ( 2009; ). Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. . J Plant Physiol 166:, 1587–1597. [CrossRef] [PubMed]
    [Google Scholar]
  16. Kerner M. J. , Naylor D. J. , Ishihama Y. , Maier T. , Chang H. C. , Stines A. P. , Georgopoulos C. , Frishman D. , Hayer-Hartl M. . & other authors ( 2005; ). Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli . . Cell 122:, 209–220. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kiley P. J. , Storz G. . ( 2004; ). Exploiting thiol modifications. . PLoS Biol 2:, e400. [CrossRef] [PubMed]
    [Google Scholar]
  18. Kourennaia O. V. , Tsujikawa L. , Dehaseth P. L. . ( 2005; ). Mutational analysis of Escherichia coli heat shock transcription factor sigma 32 reveals similarities with sigma 70 in recognition of the −35 promoter element and differences in promoter DNA melting and −10 recognition. . J Bacteriol 187:, 6762–6769. [CrossRef] [PubMed]
    [Google Scholar]
  19. Liu X. , Brutlag D. L. , Liu J. S. . ( 2001; ). BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. . Pac Symp Biocomput 6:, 127–138.[PubMed]
    [Google Scholar]
  20. MacLellan S. R. , MacLean A. M. , Finan T. M. . ( 2006; ). Promoter prediction in the rhizobia. . Microbiology 152:, 1751–1763. [CrossRef] [PubMed]
    [Google Scholar]
  21. Martínez-Salazar J. M. , Sandoval-Calderón M. , Guo X. , Castillo-Ramírez S. , Reyes A. , Loza M. G. , Rivera J. , Alvarado-Affantranger X. , Sánchez F. . & other authors ( 2009; ). The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses. . Microbiology 155:, 386–397. [CrossRef] [PubMed]
    [Google Scholar]
  22. Mascher T. , Hachmann A. B. , Helmann J. D. . ( 2007; ). Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function σ factors. . J Bacteriol 189:, 6919–6927. [CrossRef] [PubMed]
    [Google Scholar]
  23. Matsushita K. , Toyama H. , Yamada M. , Adachi O. . ( 2002; ). Quinoproteins: structure, function, and biotechnological applications. . Appl Microbiol Biotechnol 58:, 13–22. [CrossRef] [PubMed]
    [Google Scholar]
  24. Morales V. M. , Bäckman A. , Bagdasarian M. . ( 1991; ). A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. . Gene 97:, 39–47. [CrossRef] [PubMed]
    [Google Scholar]
  25. Morimoto R. I. . ( 1998; ). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. . Genes Dev 12:, 3788–3796. [CrossRef] [PubMed]
    [Google Scholar]
  26. Narberhaus F. , Krummenacher P. , Fischer H. M. , Hennecke H. . ( 1997; ). Three disparately regulated genes for σ32-like transcription factors in Bradyrhizobium japonicum . . Mol Microbiol 24:, 93–104. [CrossRef] [PubMed]
    [Google Scholar]
  27. Nur I. , Steinitz Y. L. , Okon Y. , Henis Y. . ( 1981; ). Carotenoid composition and function in nitrogen fixing bacteria of the genus Azospirillum . . J Gen Microbiol 122:, 27–32.
    [Google Scholar]
  28. Nuss A. M. , Glaeser J. , Klug G. . ( 2009; ). RpoHII activates oxidative-stress defense systems and is controlled by RpoE in the singlet oxygen-dependent response in Rhodobacter sphaeroides . . J Bacteriol 191:, 220–230. [CrossRef] [PubMed]
    [Google Scholar]
  29. Nuss A. M. , Glaeser J. , Berghoff B. A. , Klug G. . ( 2010; ). Overlapping alternative sigma factor regulons in the response to singlet oxygen in Rhodobacter sphaeroides . . J Bacteriol 192:, 2613–2623. [CrossRef] [PubMed]
    [Google Scholar]
  30. Oke V. , Rushing B. G. , Fisher E. J. , Moghadam-Tabrizi M. , Long S. R. . ( 2001; ). Identification of the heat-shock sigma factor RpoH and a second RpoH-like protein in Sinorhizobium meliloti . . Microbiology 147:, 2399–2408.[PubMed]
    [Google Scholar]
  31. Proctor R. A. , von Humboldt A. . ( 1998; ). Bacterial energetics and antimicrobial resistance. . Drug Resist Updat 1:, 227–235. [CrossRef] [PubMed]
    [Google Scholar]
  32. Richardson D. J. . ( 2000; ). Bacterial respiration: a flexible process for a changing environment. . Microbiology 146:, 551–571.[PubMed]
    [Google Scholar]
  33. Rosen R. , Sacher A. , Shechter N. , Becher D. , Büttner K. , Biran D. , Hecker M. , Ron E. Z. . ( 2004; ). Two-dimensional reference map of Agrobacterium tumefaciens proteins. . Proteomics 4:, 1061–1073. [CrossRef] [PubMed]
    [Google Scholar]
  34. Schumann W. . ( 1996; ). Regulation of the heat shock response in Escherichia coli and Bacillus subtilis . . J Biosci 21:, 133–148. [CrossRef]
    [Google Scholar]
  35. Simon R. , Priefer U. , Pühler A. . ( 1983; ). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. . Biotechnology 1:, 784–791. [CrossRef]
    [Google Scholar]
  36. Singh R. , Lemire J. , Mailloux R. J. , Appanna V. D. . ( 2008; ). A novel strategy involved in anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. . PLoS ONE 3:, e2682. [CrossRef] [PubMed]
    [Google Scholar]
  37. Spaepen S. , Das F. , Luyten E. , Michiels J. , Vanderleyden J. . ( 2009; ). Indole-3-acetic acid-regulated genes in Rhizobium etli CNPAF512. . FEMS Microbiol Lett 291:, 195–200. [CrossRef] [PubMed]
    [Google Scholar]
  38. Tachon S. , Michelon D. , Chambellon E. , Cantonnet M. , Mezange C. , Henno L. , Cachon R. , Yvon M. . ( 2009; ). Experimental conditions affect the site of tetrazolium violet reduction in the electron transport chain of Lactococcus lactis . . Microbiology 155:, 2941–2948. [CrossRef] [PubMed]
    [Google Scholar]
  39. Thirunavukkarasu N. , Mishra M. N. , Spaepen S. , Vanderleyden J. , Gross C. A. , Tripathi A. K. . ( 2008; ). An extra-cytoplasmic function sigma factor and anti-sigma factor control carotenoid biosynthesis in Azospirillum brasilense . . Microbiology 154:, 2096–2105. [CrossRef] [PubMed]
    [Google Scholar]
  40. Thomas J. G. , Baneyx F. . ( 1998; ). Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. . J Bacteriol 180:, 5165–5172.[PubMed]
    [Google Scholar]
  41. Tittabutr P. , Payakapong W. , Teaumroong N. , Boonkerd N. , Singleton P. W. , Borthakur D. . ( 2006; ). The alternative sigma factor RpoH2 is required for salt tolerance in Sinorhizobium sp. strain BL3. . Res Microbiol 157:, 811–818. [CrossRef] [PubMed]
    [Google Scholar]
  42. Vanstockem M. , Michiels K. , Vanderleyden J. , Van Gool A. P. . ( 1987; ). Transposon mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: physical analysis of Tn5 and Tn5-mob insertion mutants. . Appl Environ Microbiol 53:, 410–415.[PubMed]
    [Google Scholar]
  43. Varghese S. , Tang Y. , Imlay J. A. . ( 2003; ). Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. . J Bacteriol 185:, 221–230. [CrossRef] [PubMed]
    [Google Scholar]
  44. Vorderwülbecke S. , Kramer G. , Merz F. , Kurz T. A. , Rauch T. , Zachmann-Brand B. , Bukau B. , Deuerling E. . ( 2004; ). Low temperature or GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. . FEBS Lett 559:, 181–187. [CrossRef] [PubMed]
    [Google Scholar]
  45. Whitworth D. E. , Bryan S. J. , Berry A. E. , McGowan S. J. , Hodgson D. A. . ( 2004; ). Genetic dissection of the light-inducible carQRS promoter region of Myxococcus xanthus . . J Bacteriol 186:, 7836–7846. [CrossRef] [PubMed]
    [Google Scholar]
  46. Wisniewski-Dyé F. , Borziak K. , Khalsa-Moyers G. , Alexandre G. , Sukharnikov L. O. , Wuichet K. , Hurst G. B. , McDonald W. H. , Robertson J. S. . & other authors ( 2011; ). Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. . PLoS Genet 7:, e1002430. [CrossRef] [PubMed]
    [Google Scholar]
  47. Zhang S. , Haldenwang W. G. . ( 2005; ). Contributions of ATP, GTP, and redox state to nutritional stress activation of the Bacillus subtilis σB transcription factor. . J Bacteriol 187:, 7554–7560. [PubMed] [CrossRef]
    [Google Scholar]
  48. Zhou Y. N. , Kusukawa N. , Erickson J. W. , Gross C. A. , Yura T. . ( 1988; ). Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. . J Bacteriol 170:, 3640–3649.[PubMed]
    [Google Scholar]
  49. Ziegelhoffer E. C. , Donohue T. J. . ( 2009; ). Bacterial responses to photo-oxidative stress. . Nat Rev Microbiol 7:, 856–863.[PubMed]
    [Google Scholar]
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