1887

Abstract

Extracytoplasmic function (ECF) sigma factors (σ) are known to bring about changes in gene expression to enable bacteria to adapt to different stresses. The Sp245 genome harbours nine genes encoding σ, of which two are adjacent to the genes encoding ChrR-type zinc-binding anti-sigma (ZAS) factors. We describe here the role and regulation of a new pair of , which was found in the genome of Sp7 in addition to the previously described pair (designated ). The pair is also cotranscribed, and their products show protein–protein interaction. The −10 and −35 promoter elements of and were similar but not identical. Unlike the promoter of , the promoter was neither autoregulated nor induced by oxidative stress. Inactivation of or overexpression of in Sp7 resulted in an overproduction of carotenoids. It also conferred resistance to oxidative stresses and antibiotics. By controlling the synthesis of carotenoids, initiation and elongation of translation, protein folding and purine biosynthesis, RpoE2 seems to play a crucial role in preventing and repairing the cellular damage caused by oxidative stress. Lack of autoregulation and constitutive expression of suggest that RpoE2–ChrR2 may provide a rapid mechanism to cope with oxidative stress, wherein singlet oxygen (O)-mediated dissociation of the RpoE2–ChrR2 complex might release RpoE2 to drive the expression of its target genes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.061937-0
2013-02-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/2/205.html?itemId=/content/journal/micro/10.1099/mic.0.061937-0&mimeType=html&fmt=ahah

References

  1. Alexandre G., Bally R., Taylor B. L., Zhulin I. B.. ( 1999;). Loss of cytochrome c oxidase activity and acquisition of resistance to quinone analogs in a laccase-positive variant of Azospirillum lipoferum. . J Bacteriol 181:, 6730–6738.[PubMed]
    [Google Scholar]
  2. Alvarez-Martinez C. E., Lourenço R. F., Baldini R. L., Laub M. T., Gomes S. L.. ( 2007;). The ECF sigma factor σT is involved in osmotic and oxidative stress responses in Caulobacter crescentus. . Mol Microbiol 66:, 1240–1255. [CrossRef][PubMed]
    [Google Scholar]
  3. Anthony J. R., Newman J. D., Donohue T. J.. ( 2004;). Interactions between the Rhodobacter sphaeroides ECF sigma factor, σE, and its anti-sigma factor, ChrR. . J Mol Biol 341:, 345–360. [CrossRef][PubMed]
    [Google Scholar]
  4. Anthony J. R., Warczak K. L., Donohue T. J.. ( 2005;). A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. . Proc Natl Acad Sci U S A 102:, 6502–6507. [CrossRef][PubMed]
    [Google Scholar]
  5. Baldani J. I., Krieg N. R., Baldani V. L. D., Hartmann A., Dobereiner J.. ( 1979;). Genus II. Azospirillum Tarrand, Krieg and Dobereiner, 79AL. . In Bergey’s Manual of Systematic Bacteriology, vol. 2. Edited by Garrity G. M., Brenner D. J., Krieg N. R., Staley J. T... New York:: Springer;.
    [Google Scholar]
  6. Bang I.-S., Frye J. G., McClelland M., Velayudhan J., Fang F. C.. ( 2005;). Alternative sigma factor interactions in Salmonella: σE and σH promote antioxidant defences by enhancing σS levels. . Mol Microbiol 56:, 811–823. [CrossRef][PubMed]
    [Google Scholar]
  7. 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]
  8. Brown K. L., Hughes K. T.. ( 1995;). The role of anti-sigma factors in gene regulation. . Mol Microbiol 16:, 397–404. [CrossRef][PubMed]
    [Google Scholar]
  9. 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]
  10. Cao M., Wang T., Ye R., Helmann J. D.. ( 2002;). Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis σW and σM regulons. . Mol Microbiol 45:, 1267–1276. [CrossRef][PubMed]
    [Google Scholar]
  11. Cogdell R. J., Howard T. D., Bittl R., Schlodder E., Geisenheimer I., Lubitz W.. ( 2000;). How carotenoids protect bacterial photosynthesis. . Philos Trans R Soc Lond B Biol Sci 355:, 1345–1349. [CrossRef][PubMed]
    [Google Scholar]
  12. Crooks G. E., Hon G., Chandonia J. M., Brenner S. E.. ( 2004;). WebLogo: a sequence logo generator. . Genome Res 14:, 1188–1190. [CrossRef][PubMed]
    [Google Scholar]
  13. 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]
  14. Demidova T. N., Hamblin M. R.. ( 2004;). Photodynamic therapy targeted to pathogens. . Int J Immunopathol Pharmacol 17:, 245–254.[PubMed]
    [Google Scholar]
  15. Dufour Y. S., Landick R., Donohue T. J.. ( 2008;). Organization and evolution of the biological response to singlet oxygen stress. . J Mol Biol 383:, 713–730. [CrossRef][PubMed]
    [Google Scholar]
  16. Firoved A. M., Boucher J. C., Deretic V.. ( 2002;). Global genomic analysis of AlgU (σE)-dependent promoters (sigmulon) in Pseudomonas aeruginosa and implications for inflammatory processes in cystic fibrosis. . J Bacteriol 184:, 1057–1064. [CrossRef][PubMed]
    [Google Scholar]
  17. Glaeser J., Klug G.. ( 2005;). Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. . Microbiology 151:, 1927–1938. [CrossRef][PubMed]
    [Google Scholar]
  18. Glaeser J., Nuss A. M., Berghoff B. A., Klug G.. ( 2011;). Singlet oxygen stress in microorganisms. . Adv Microb Physiol 58:, 141–173. [CrossRef][PubMed]
    [Google Scholar]
  19. Graumann P., Schröder K., Schmid R., Marahiel M. A.. ( 1996;). Cold shock stress-induced proteins in Bacillus subtilis. . J Bacteriol 178:, 4611–4619.[PubMed]
    [Google Scholar]
  20. Greenwell R., Nam T. W., Donohue T. J.. ( 2011;). Features of Rhodobacter sphaeroides ChrR required for stimuli to promote the dissociation of σE/ChrR complexes. . J Mol Biol 407:, 477–491. [CrossRef][PubMed]
    [Google Scholar]
  21. Grünenfelder B., Rummel G., Vohradsky J., Röder D., Langen H., Jenal U.. ( 2001;). Proteomic analysis of the bacterial cell cycle. . Proc Natl Acad Sci U S A 98:, 4681–4686. [CrossRef][PubMed]
    [Google Scholar]
  22. Haine V., Dozot M., Dornand J., Letesson J. J., De Bolle X.. ( 2006;). NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. . J Bacteriol 188:, 1615–1619. [CrossRef][PubMed]
    [Google Scholar]
  23. 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]
  24. Helmann J. D.. ( 2002;). The extracytoplasmic function (ECF) sigma factors. . Adv Microb Physiol 46:, 47–110. [CrossRef][PubMed]
    [Google Scholar]
  25. Ho T. D., Ellermeier C. D.. ( 2012;). Extra cytoplasmic function σ factor activation. . Curr Opin Microbiol 15:, 182–188. [CrossRef][PubMed]
    [Google Scholar]
  26. Hondorp E. R., Matthews R. G.. ( 2004;). Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. . PLoS Biol 2:, e336. [CrossRef][PubMed]
    [Google Scholar]
  27. Kumar K., Tharad M., Ganapathy S., Ram G., Narayan A., Khan J. A., Pratap R., Ghosh A., Samuchiwal S. K.. & other authors ( 2009;). Phenylalanine-rich peptides potently bind ESAT6, a virulence determinant of Mycobacterium tuberculosis, and concurrently affect the pathogen’s growth. . PLoS ONE 4:, e7615. [CrossRef][PubMed]
    [Google Scholar]
  28. 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]
  29. Lourenço R. F., Gomes S. L.. ( 2009;). The transcriptional response to cadmium, organic hydroperoxide, singlet oxygen and UV-A mediated by the σE-ChrR system in Caulobacter crescentus. . Mol Microbiol 72:, 1159–1170. [CrossRef][PubMed]
    [Google Scholar]
  30. Lourenço R. F., Kohler C., Gomes S. L.. ( 2011;). A two-component system, an anti-sigma factor and two paralogous ECF sigma factors are involved in the control of general stress response in Caulobacter crescentus. . Mol Microbiol 80:, 1598–1612. [CrossRef][PubMed]
    [Google Scholar]
  31. Luo Y., Helmann J. D.. ( 2012;). Analysis of the role of Bacillus subtilis σM in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. . Mol Microbiol 83:, 623–639. [CrossRef][PubMed]
    [Google Scholar]
  32. Luo Y., Asai K., Sadaie Y., Helmann J. D.. ( 2010;). Transcriptomic and phenotypic characterization of a Bacillus subtilis strain without extracytoplasmic function σ factors. . J Bacteriol 192:, 5736–5745. [CrossRef][PubMed]
    [Google Scholar]
  33. Marchal K., Sun J., Keijers V., Haaker H., Vanderleyden J.. ( 1998;). A cytochrome cbb3 (cytochrome c) terminal oxidase in Azospirillum brasilense Sp7 supports microaerobic growth. . J Bacteriol 180:, 5689–5696.[PubMed]
    [Google Scholar]
  34. Martínez-Salazar J. M., Salazar E., Encarnación S., Ramírez-Romero M. A., Rivera J.. ( 2009;). Role of the extracytoplasmic function sigma factor RpoE4 in oxidative and osmotic stress responses in Rhizobium etli. . J Bacteriol 191:, 4122–4132. [CrossRef][PubMed]
    [Google Scholar]
  35. 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]
  36. Matallana-Surget S., Joux F., Raftery M. J., Cavicchioli R.. ( 2009;). The response of the marine bacterium Sphingopyxis alaskensis to solar radiation assessed by quantitative proteomics. . Environ Microbiol 11:, 2660–2675. [CrossRef][PubMed]
    [Google Scholar]
  37. Miller J. H.. ( 1972;). Experiments in Molecular Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  38. Mishra M. N., Thirunavukkarasu N., Sharma I. M., Jagnnadham M. V., Tripathi A. K.. ( 2008;). Mutation in a gene encoding anti-σ factor in A. brasilense confers tolerance to elevated temperature, antibacterial peptide and PEG-200 via carotenoid synthesis. . FEMS Microbiol Lett 287:, 221–229. [CrossRef][PubMed]
    [Google Scholar]
  39. Mishra M. N., Kumar S., Gupta N., Kaur S., Gupta A., Tripathi A. K.. ( 2011;). An extracytoplasmic function sigma factor cotranscribed with its cognate anti-sigma factor confers tolerance to NaCl, ethanol and methylene blue in Azospirillum brasilense Sp7. . Microbiology 157:, 988–999. [CrossRef][PubMed]
    [Google Scholar]
  40. 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]
  41. Newman J. D., Anthony J. R., Donohue T. J.. ( 2001;). The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor. . J Mol Biol 313:, 485–499. [CrossRef][PubMed]
    [Google Scholar]
  42. Norman R. A., Poh C. L., Pearl L. H., O’Hara B. P., Drew R. E.. ( 2000;). Steric hindrance regulation of the Pseudomonas aeruginosa amidase operon. . J Biol Chem 275:, 30660–30667. [CrossRef][PubMed]
    [Google Scholar]
  43. 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]
  44. 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]
  45. Paget M. S. B., Bae J.-B., Hahn M.-Y., Li W., Kleanthous C., Roe J.-H., Buttner M. J.. ( 2001;). Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. . Mol Microbiol 39:, 1036–1047. [CrossRef][PubMed]
    [Google Scholar]
  46. Park S.-D., Youn J.-W., Kim Y.-J., Lee S.-M., Kim Y., Lee H.-S.. ( 2008;). Corynebacterium glutamicum σE is involved in responses to cell surface stresses and its activity is controlled by the anti-σ factor CseE. . Microbiology 154:, 915–923. [CrossRef][PubMed]
    [Google Scholar]
  47. Paulsrud P., Lindblad P.. ( 2002;). Fasciclin domain proteins are present in nostoc symbionts of lichens. . Appl Environ Microbiol 68:, 2036–2039. [CrossRef][PubMed]
    [Google Scholar]
  48. Poole K.. ( 2012;). Stress responses as determinants of antimicrobial resistance in Gram-negative bacteria. . Trends Microbiol 20:, 227–234. [CrossRef][PubMed]
    [Google Scholar]
  49. Proctor R. A., von Humboldt A.. ( 1998;). Bacterial energetics and antimicrobial resistance. . Drug Resist Updat 1:, 227–235. [CrossRef][PubMed]
    [Google Scholar]
  50. Ravanat J. L., Martinez G. R., Medeiros M. H., Di Mascio P., Cadet J.. ( 2004;). Mechanistic aspects of the oxidation of DNA constituents mediated by singlet molecular oxygen. . Arch Biochem Biophys 423:, 23–30. [CrossRef][PubMed]
    [Google Scholar]
  51. Ross C. L., Thomason K. S., Koehler T. M.. ( 2009;). An extracytoplasmic function sigma factor controls β-lactamase gene expression in Bacillus anthracis and other Bacillus cereus group species. . J Bacteriol 191:, 6683–6693. [CrossRef][PubMed]
    [Google Scholar]
  52. Rowen D. W., Deretic V.. ( 2000;). Membrane-to-cytosol redistribution of ECF sigma factor AlgU and conversion to mucoidy in Pseudomonas aeruginosa isolates from cystic fibrosis patients. . Mol Microbiol 36:, 314–327. [CrossRef][PubMed]
    [Google Scholar]
  53. Rowley G., Spector M., Kormanec J., Roberts M.. ( 2006;). Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. . Nat Rev Microbiol 4:, 383–394. [CrossRef][PubMed]
    [Google Scholar]
  54. Schurr M. J., Yu H., Martinez-Salazar J. M., Boucher J. C., Deretic V.. ( 1996;). Control of AlgU, a member of the σE-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. . J Bacteriol 178:, 4997–5004.[PubMed]
    [Google Scholar]
  55. 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]
  56. Staroń A., Sofia H. J., Dietrich S., Ulrich L. E., Liesegang H., Mascher T.. ( 2009;). The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family. . Mol Microbiol 74:, 557–581. [CrossRef][PubMed]
    [Google Scholar]
  57. Steenhoudt O., Vanderleyden J.. ( 2000;). Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. . FEMS Microbiol Rev 24:, 487–506. [CrossRef][PubMed]
    [Google Scholar]
  58. Thakur K. G., Jaiswal R. K., Shukla J. K., Praveena T., Gopal B.. ( 2010;). Over-expression and purification strategies for recombinant multi-protein oligomers: a case study of Mycobacterium tuberculosis σ/anti-σ factor protein complexes. . Protein Expr Purif 74:, 223–230. [CrossRef][PubMed]
    [Google Scholar]
  59. 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]
  60. Tran T. D., Kwon H. Y., Kim E. H., Kim K. W., Briles D. E., Pyo S., Rhee D. K.. ( 2011;). Decrease in penicillin susceptibility due to heat shock protein ClpL in Streptococcus pneumoniae. . Antimicrob Agents Chemother 55:, 2714–2728. [CrossRef][PubMed]
    [Google Scholar]
  61. Typas A., Banzhaf M., van den Berg van Saparoea B., Verheul J., Biboy J., Nichols R. J., Zietek M., Beilharz K., Kannenberg K.. & other authors ( 2010;). Regulation of peptidoglycan synthesis by outer-membrane proteins. . Cell 143:, 1097–1109. [CrossRef][PubMed]
    [Google Scholar]
  62. 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]
  63. 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]
  64. Wainwright M., Giddens R. M.. ( 2003;). Phenothiazinium photosensitisers: choices in synthesis and application. . Dyes Pigments 57:, 245–257. [CrossRef]
    [Google Scholar]
  65. 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]
  66. Yoshimura M., Asai K., Sadaie Y., Yoshikawa H.. ( 2004;). Interaction of Bacillus subtilis extracytoplasmic function (ECF) sigma factors with the N-terminal regions of their potential anti-sigma factors. . Microbiology 150:, 591–599. [CrossRef][PubMed]
    [Google Scholar]
  67. Zeller T., Klug G.. ( 2006;). Thioredoxins in bacteria: functions in oxidative stress response and regulation of thioredoxin genes. . Naturwissenschaften 93:, 259–266. [CrossRef][PubMed]
    [Google Scholar]
  68. 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. [CrossRef][PubMed]
    [Google Scholar]
  69. Zhu Y. S., Hearst J. E.. ( 1988;). Transcription of oxygen-regulated photosynthetic genes requires DNA gyrase in Rhodobacter capsulatus. . Proc Natl Acad Sci U S A 85:, 4209–4213. [CrossRef][PubMed]
    [Google Scholar]
  70. Ziegelhoffer E. C., Donohue T. J.. ( 2009;). Bacterial responses to photo-oxidative stress. . Nat Rev Microbiol 7:, 856–863.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.061937-0
Loading
/content/journal/micro/10.1099/mic.0.061937-0
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