A Nitric Oxide Regulated Small RNA Controls Expression of Genes Involved in Redox Homeostasis in

English version České info

Bacteria have evolved various strategies to continually monitor the redox state of the internal and external environments to prevent cell damage and/or to protect them from host defense mechanisms. These signals modify the expression of genes, allowing bacteria to adapt to altered redox environments and to maintain homeostasis. Studies in Enterobacteriaceae have shown that sRNAs play central roles in adaptation to oxidative stress. We show here that the conserved sRNA, RoxS is induced by the presence of nitric oxide (NO) in the medium, through the ResDE and SrrAB two-component systems of Bacillus subtilis and Staphylococcus aureus, respectively. B. subtilis RoxS regulates functions related to oxidation-reduction reactions and acts as an antisense RNA to control translation initiation and the degradation of ppnKB mRNA, encoding an NAD+/NADH kinase. Interestingly, RNase Y processes the 5′ end of the RoxS sRNA leading to a truncated sRNA that in turn interacts more efficiently with a second target, the sucCD mRNA, encoding succinyl-CoA synthase. Taken together this work shows that RoxS is part of a complex regulatory network that allows the cell to sense and respond to redox perturbations, and revealed a novel process that allows an expansion of the repertoire of sRNA targets.

Vyšlo v časopise: A Nitric Oxide Regulated Small RNA Controls Expression of Genes Involved in Redox Homeostasis in. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004957
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004957

Souhrn

Zdroje

1. Storz G, Vogel J, Wassarman KM (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: 880–891. doi: 10.1016/j.molcel.2011.08.022 21925377

2. Caldelari I, Chao Y, Romby P, Vogel J (2013) RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb Perspect Med 3: a010298. doi: 10.1101/cshperspect.a010298 24003243

3. Ramirez-Pena E, Trevino J, Liu Z, Perez N, Sumby P (2010) The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript. Mol Microbiol 78: 1332–1347. doi: 10.1111/j.1365-2958.2010.07427.x 21143309

4. Obana N, Shirahama Y, Abe K, Nakamura K (2010) Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5′ leader sequence. Mol Microbiol 77: 1416–1428. doi: 10.1111/j.1365-2958.2010.07258.x 20572941

5. Opdyke JA, Fozo EM, Hemm MR, Storz G (2011) RNase III participates in GadY-dependent cleavage of the gadX-gadW mRNA. J Mol Biol 406: 29–43. doi: 10.1016/j.jmb.2010.12.009 21147125

6. Pfeiffer V, Papenfort K, Lucchini S, Hinton JC, Vogel J (2009) Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16: 840–846. doi: 10.1038/nsmb.1631 19620966

7. Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB, et al. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105: 11927–11932. doi: 10.1073/pnas.0711752105 18697947

8. Heidrich N, Chinali A, Gerth U, Brantl S (2006) The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. Mol Microbiol 62: 520–536. 17020585

9. Gimpel M, Preis H, Barth E, Gramzow L, Brantl S (2012) SR1- a small RNA with two remarkably conserved functions. Nucleic Acids Res 40: 11659–11672. doi: 10.1093/nar/gks895 23034808

10. Smaldone GT, Antelmann H, Gaballa A, Helmann JD (2012) The FsrA sRNA and FbpB protein mediate the iron-dependent induction of the Bacillus subtilis lutABC iron-sulfur-containing oxidases. J Bacteriol 194: 2586–2593. doi: 10.1128/JB.05567-11 22427629

11. Smaldone GT, Revelles O, Gaballa A, Sauer U, Antelmann H, et al. (2012) A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism. J Bacteriol 194: 2594–2605. doi: 10.1128/JB.05990-11 22389480

12. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24: 824–835. doi: 10.1038/sj.emboj.7600572 15678100

13. Hammerle H, Amman F, Vecerek B, Stulke J, Hofacker I, et al. (2014) Impact of Hfq on the Bacillus subtilis transcriptome. PLoS One 9: e98661. doi: 10.1371/journal.pone.0098661 24932523

14. Dambach M, Irnov I, Winkler WC (2013) Association of RNAs with Bacillus subtilis Hfq. PLoS One 8: e55156. doi: 10.1371/journal.pone.0055156 23457461

15. Even S, Pellegrini O, Zig L, Labas V, Vinh J, et al. (2005) Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33: 2141–2152. doi: 10.1093/nar/gki505 15831787

16. Mathy N, Benard L, Pellegrini O, Daou R, Wen T, et al. (2007) 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129: 681–692. 17512403

17. Geissmann T, Chevalier C, Cros MJ, Boisset S, Fechter P, et al. (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37: 7239–7257. doi: 10.1093/nar/gkp668 19786493

18. Bohn C, Rigoulay C, Chabelskaya S, Sharma CM, Marchais A, et al. (2010) Experimental discovery of small RNAs in Staphylococcus aureus reveals a riboregulator of central metabolism. Nucleic Acids Res 38: 6620–6636. doi: 10.1093/nar/gkq462 20511587

19. Song J, Lays C, Vandenesch F, Benito Y, Bes M, et al. (2012) The expression of small regulatory RNAs in clinical samples reflects the different life styles of Staphylococcus aureus in colonization vs. infection. PLoS One 7: e37294. doi: 10.1371/journal.pone.0037294 22629378

20. Demple B (1999) Genetic responses against nitric oxide toxicity. Braz J Med Biol Res 32: 1417–1427. 10559844

21. Crane BR, Sudhamsu J, Patel BA (2010) Bacterial nitric oxide synthases. Annu Rev Biochem 79: 445–470. doi: 10.1146/annurev-biochem-062608-103436 20370423

22. Gusarov I, Nudler E (2005) NO-mediated cytoprotection: instant adaptation to oxidative stress in bacteria. Proc Natl Acad Sci U S A 102: 13855–13860. doi: 10.1073/pnas.0504307102 16172391

23. Shatalin K, Gusarov I, Avetissova E, Shatalina Y, McQuade LE, et al. (2008) Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc Natl Acad Sci U S A 105: 1009–1013. doi: 10.1073/pnas.0710950105 18215992

24. Hochgrafe F, Wolf C, Fuchs S, Liebeke M, Lalk M, et al. (2008) Nitric oxide stress induces different responses but mediates comparable protein thiol protection in Bacillus subtilis and Staphylococcus aureus. J Bacteriol 190: 4997–5008. doi: 10.1128/JB.01846-07 18487332

25. Gusarov I, Shatalin K, Starodubtseva M, Nudler E (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325: 1380–1384. doi: 10.1126/science.1175439 19745150

26. van Sorge NM, Beasley FC, Gusarov I, Gonzalez DJ, von Kockritz-Blickwede M, et al. (2013) Methicillin-resistant Staphylococcus aureus bacterial nitric-oxide synthase affects antibiotic sensitivity and skin abscess development. J Biol Chem 288: 6417–6426. doi: 10.1074/jbc.M112.448738 23322784

27. Gusarov I, Gautier L, Smolentseva O, Shamovsky I, Eremina S, et al. (2013) Bacterial nitric oxide extends the lifespan of C. elegans. Cell 152: 818–830. doi: 10.1016/j.cell.2012.12.043 23415229

28. Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, et al. (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 335: 1103–1106. doi: 10.1126/science.1206848 22383849

29. Baruah A, Lindsey B, Zhu Y, Nakano MM (2004) Mutational analysis of the signal-sensing domain of ResE histidine kinase from Bacillus subtilis. J Bacteriol 186: 1694–1704. doi: 10.1128/JB.186.6.1694-1704.2004 14996800

30. Kinkel TL, Roux CM, Dunman PM, Fang FC (2013) The Staphylococcus aureus SrrAB two-component system promotes resistance to nitrosative stress and hypoxia. MBio 4: e00696–00613. doi: 10.1128/mBio.00696-13 24222487

31. Hartig E, Geng H, Hartmann A, Hubacek A, Munch R, et al. (2004) Bacillus subtilis ResD induces expression of the potential regulatory genes yclJK upon oxygen limitation. J Bacteriol 186: 6477–6484. doi: 10.1128/JB.186.19.6477-6484.2004 15375128

32. Henares B, Kommineni S, Chumsakul O, Ogasawara N, Ishikawa S, et al. (2014) The ResD Response Regulator, through Functional Interaction with NsrR and Fur, Plays Three Distinct Roles in Bacillus subtilis Transcriptional Control. J Bacteriol 196: 493–503. doi: 10.1128/JB.01166-13 24214949

33. Rochat T, Nicolas P, Delumeau O, Rabatinova A, Korelusova J, et al. (2012) Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis. Nucleic Acids Res 40: 9571–9583. doi: 10.1093/nar/gks755 22904090

34. Nakano MM (2002) Induction of ResDE-dependent gene expression in Bacillus subtilis in response to nitric oxide and nitrosative stress. J Bacteriol 184: 1783–1787. doi: 10.1128/JB.184.6.1783-1787.2002 11872732

35. Antelmann H, Engelmann S, Schmid R, Sorokin A, Lapidus A, et al. (1997) Expression of a stress- and starvation-induced dps/pexB-homologous gene is controlled by the alternative sigma factor sigmaB in Bacillus subtilis. J Bacteriol 179: 7251–7256. 9393687

36. You C, Sekowska A, Francetic O, Martin-Verstraete I, Wang Y, et al. (2008) Spx mediates oxidative stress regulation of the methionine sulfoxide reductases operon in Bacillus subtilis. BMC Microbiol 8: 128. doi: 10.1186/1471-2180-8-128 18662407

37. Kiran MD, Bala S, Hirshberg M, Balaban N (2010) YhgC protects Bacillus anthracis from oxidative stress. Int J Artif Organs.

38. Wang ZQ, Lawson RJ, Buddha MR, Wei CC, Crane BR, et al. (2007) Bacterial flavodoxins support nitric oxide production by Bacillus subtilis nitric-oxide synthase. J Biol Chem 282: 2196–2202. 17127770

39. Durand S, Gilet L, Bessieres P, Nicolas P, Condon C (2012) Three essential ribonucleases-RNase Y, J1, and III-control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8: e1002520. doi: 10.1371/journal.pgen.1002520 22412379

40. Tjaden B (2012) Computational identification of sRNA targets. Methods Mol Biol 905: 227–234. doi: 10.1007/978-1-61779-949-5_14 22736007

41. Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, et al. (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci U S A 110: E3487–3496. doi: 10.1073/pnas.1303248110 23980183

42. Eggenhofer F, Tafer H, Stadler PF, Hofacker IL (2011) RNApredator: fast accessibility-based prediction of sRNA targets. Nucleic Acids Res 39: W149–154. doi: 10.1093/nar/gkr467 21672960

43. Geng H, Nakano S, Nakano MM (2004) Transcriptional activation by Bacillus subtilis ResD: tandem binding to target elements and phosphorylation-dependent and -independent transcriptional activation. J Bacteriol 186: 2028–2037. doi: 10.1128/JB.186.7.2028-2037.2004 15028686

44. Georgellis D, Kwon O, Lin EC (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science 292: 2314–2316. 11423658

45. Ye RW, Tao W, Bedzyk L, Young T, Chen M, et al. (2000) Global gene expression profiles of Bacillus subtilis grown under anaerobic conditions. J Bacteriol 182: 4458–4465. 10913079

46. Fan J, Ye J, Kamphorst JJ, Shlomi T, Thompson CB, et al. (2014) Quantitative flux analysis reveals folate-dependent NADPH production. Nature 510: 298–302. doi: 10.1038/nature13236 24805240

47. Shahbabian K, Jamalli A, Zig L, Putzer H (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523–3533. doi: 10.1038/emboj.2009.283 19779461

48. Lehnik-Habrink M, Rempeters L, Kovacs AT, Wrede C, Baierlein C, et al. (2013) DEAD-Box RNA helicases in Bacillus subtilis have multiple functions and act independently from each other. J Bacteriol 195: 534–544. doi: 10.1128/JB.01475-12 23175651

49. Faubladier M, Cam K, Bouche JP (1990) Escherichia coli cell division inhibitor DicF-RNA of the dicB operon. Evidence for its generation in vivo by transcription termination and by RNase III and RNase E-dependent processing. J Mol Biol 212: 461–471. 1691299

50. Guo MS, Updegrove TB, Gogol EB, Shabalina SA, Gross CA, et al. (2014) MicL, a new sigmaE-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev 28: 1620–1634. doi: 10.1101/gad.243485.114 25030700

51. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, et al. (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74: 139–158. doi: 10.1111/j.1365-2958.2009.06857.x 19732340

52. Mandin P, Gottesman S (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29: 3094–3107. doi: 10.1038/emboj.2010.179 20683441

53. Davis BM, Waldor MK (2007) RNase E-dependent processing stabilizes MicX, a Vibrio cholerae sRNA. Mol Microbiol 65: 373–385. doi: 10.1111/j.1365-2958.2007.05796.x 17590231

54. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci U S A 107: 9602–9607. doi: 10.1073/pnas.1004435107 20457943

55. Viegas SC, Silva IJ, Saramago M, Domingues S, Arraiano CM (2011) Regulation of the small regulatory RNA MicA by ribonuclease III: a target-dependent pathway. Nucleic Acids Res 39: 2918–2930. doi: 10.1093/nar/gkq1239 21138960

56. Afonyushkin T, Vecerek B, Moll I, Blasi U, Kaberdin VR (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res 33: 1678–1689. doi: 10.1093/nar/gki313 15781494

57. Marchais A, Duperrier S, Durand S, Gautheret D, Stragier P (2011) CsfG, a sporulation-specific, small non-coding RNA highly conserved in endospore formers. RNA Biol 8: 358–364. doi: 10.4161/rna.8.3.14998 21532344

58. Guerout-Fleury AM, Shazand K, Frandsen N, Stragier P (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167: 335–336. 8566804

59. Britton RA, Wen T, Schaefer L, Pellegrini O, Uicker WC, et al. (2007) Maturation of the 5′ end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol 63: 127–138. 17229210

60. Bechhofer DH, Oussenko IA, Deikus G, Yao S, Mathy N, et al. (2008) Analysis of mRNA decay in Bacillus subtilis. Methods Enzymol 447: 259–276. doi: 10.1016/S0076-6879(08)02214-3 19161848

61. Stead MB, Agrawal A, Bowden KE, Nasir R, Mohanty BK, et al. (2012) RNAsnap: a rapid, quantitative and inexpensive, method for isolating total RNA from bacteria. Nucleic Acids Res 40: e156. doi: 10.1093/nar/gks680 22821568

62. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3. 16646809

63. Strimmer K (2008) A unified approach to false discovery rate estimation. BMC Bioinformatics 9: 303. doi: 10.1186/1471-2105-9-303 18613966

64. Zybailov B, Coleman MK, Florens L, Washburn MP (2005) Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. Anal Chem 77: 6218–6224. 16194081

65. Bauer KM, Lambert PA, Hummon AB (2012) Comparative label-free LC-MS/MS analysis of colorectal adenocarcinoma and metastatic cells treated with 5-fluorouracil. Proteomics 12: 1928–1937. doi: 10.1002/pmic.201200041 22623418

66. Fechter P, Chevalier C, Yusupova G, Yusupov M, Romby P, et al. (2009) Ribosomal initiation complexes probed by toeprinting and effect of trans-acting translational regulators in bacteria. Methods Mol Biol 540: 247–263. doi: 10.1007/978-1-59745-558-9_18 19381565

67. Chevalier C, Geissmann T, Helfer AC, Romby P (2009) Probing mRNA structure and sRNA-mRNA interactions in bacteria using enzymes and lead(II). Methods Mol Biol 540: 215–232. doi: 10.1007/978-1-59745-558-9_16 19381563