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 .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.062380-0
2012-12-01
2021-02-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/12/2891.html?itemId=/content/journal/micro/10.1099/mic.0.062380-0&mimeType=html&fmt=ahah

References

  1. Arsène F., Tomoyasu T., Bukau B.. ( 2000;). The heat shock response of Escherichia coli . Int J Food Microbiol55:3–9 [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 Microbiol30:137–140 [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 Microbiol13:775–791 [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 Bacteriol188:3507–3515 [CrossRef][PubMed]
    [Google Scholar]
  5. Brot N., Weissbach H.. ( 2000;). Peptide methionine sulfoxide reductase: biochemistry and physiological role. Biopolymers55:288–296 [CrossRef][PubMed]
    [Google Scholar]
  6. Butcher R. G.. ( 1978;). Oxygen and the production of formazan from neotetrazolium chloride. Histochemistry56:329–340 [CrossRef][PubMed]
    [Google Scholar]
  7. Caldas T., Demont-Caulet N., Ghazi A., Richarme G.. ( 1999;). Thermoprotection by glycine betaine and choline. Microbiology145:2543–2548[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 Chem275:855–860 [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 Bacteriol186:8149–8152 [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 Bacteriol189:551–560 [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 Lett326:99–108 [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 Bacteriol188:5712–5721 [CrossRef][PubMed]
    [Google Scholar]
  13. Gunz F. W.. ( 1948;). Reduction of tetrazolium salts by some biological agents. Nature162:98[PubMed]
    [Google Scholar]
  14. Hartl F. U., Hayer-Hartl M.. ( 2002;). Molecular chaperones in the cytosol: from nascent chain to folded protein. Science295:1852–1858 [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 Physiol166:1587–1597 [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 . Cell122:209–220 [CrossRef][PubMed]
    [Google Scholar]
  17. Kiley P. J., Storz G.. ( 2004;). Exploiting thiol modifications. PLoS Biol2: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 Bacteriol187:6762–6769 [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 Biocomput6:127–138[PubMed]
    [Google Scholar]
  20. MacLellan S. R., MacLean A. M., Finan T. M.. ( 2006;). Promoter prediction in the rhizobia. Microbiology152:1751–1763 [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. Microbiology155:386–397 [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 Bacteriol189:6919–6927 [CrossRef][PubMed]
    [Google Scholar]
  23. Matsushita K., Toyama H., Yamada M., Adachi O.. ( 2002;). Quinoproteins: structure, function, and biotechnological applications. Appl Microbiol Biotechnol58:13–22 [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. Gene97:39–47 [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 Dev12:3788–3796 [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 Microbiol24:93–104 [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 Microbiol122:27–32
    [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 Bacteriol191:220–230 [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 Bacteriol192:2613–2623 [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 . Microbiology147:2399–2408[PubMed]
    [Google Scholar]
  31. Proctor R. A., von Humboldt A.. ( 1998;). Bacterial energetics and antimicrobial resistance. Drug Resist Updat1:227–235 [CrossRef][PubMed]
    [Google Scholar]
  32. Richardson D. J.. ( 2000;). Bacterial respiration: a flexible process for a changing environment. Microbiology146:551–571[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. Proteomics4:1061–1073 [CrossRef][PubMed]
    [Google Scholar]
  34. Schumann W.. ( 1996;). Regulation of the heat shock response in Escherichia coli and Bacillus subtilis . J Biosci21:133–148 [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. Biotechnology1:784–791 [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 ONE3: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 Lett291:195–200 [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 . Microbiology155:2941–2948 [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 . Microbiology154:2096–2105 [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 Bacteriol180:5165–5172[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 Microbiol157:811–818 [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 Microbiol53:410–415[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 Bacteriol185:221–230 [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 Lett559:181–187 [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 Bacteriol186:7836–7846 [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 Genet7: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 Bacteriol187:7554–7560[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 Bacteriol170:3640–3649[PubMed]
    [Google Scholar]
  49. Ziegelhoffer E. C., Donohue T. J.. ( 2009;). Bacterial responses to photo-oxidative stress. Nat Rev Microbiol7:856–863[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.062380-0
Loading
/content/journal/micro/10.1099/mic.0.062380-0
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