Impact of Hfq on the Bacillus subtilis transcriptome

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Hämmerle, Hermann ^a   Amman, Fabian ^a,c   Večerek, Branislav ^a,d   Stülke, Jörg ^b   Hofacker, Ivo ^a   Bläsi, Udo ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MESSENGER RNA; PROTEIN HFQ; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL RNA; DNA BINDING PROTEIN; HOST FACTOR 1; RESD PROTEIN, BACILLUS SUBTILIS; SMALL NUCLEAR RNA; TRANSCRIPTION FACTOR;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ARTICLE; BACILLUS SUBTILIS; BACTERIAL SURVIVAL; COMK GENE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC CODE; GERE GENE; NONHUMAN; PROTEIN FUNCTION; REGULON; RESD GENE; RNA TRANSCRIPTION; TRANSCRIPTOMICS; UPREGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PROCEDURES;

AEROBIOSIS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; REGULON; RNA, BACTERIAL; RNA, MESSENGER; RNA, SMALL NUCLEAR; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84903291745     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098661     Document Type: Article

References (71)

1. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, et al. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71: 1-11.
2. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22. (Pubitemid 34127767)
3. Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589.
4. Afonyushkin T, Večerek B, Moll I, Bläsi 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. (Pubitemid 41418396)
5. Massé E, Escorcia FE, Gottesman S (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383. (Pubitemid 37214786)
6. Moll I, Afonyushkin T, Vytvytska O, Kaberdin VR, Bläsi U (2003) Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9: 1308-1314. (Pubitemid 37310861)
7. Sledjeski DD, Whitman C, Zhang A (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183: 1997-2005. (Pubitemid 32225995)
8. Møller T, Franch T, Højrup P, Keene DR, Bächinger HP, et al. (2002) Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9: 23- 30.
9. Sun X, Zhulin I, Wartell RM (2002) Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res 30: 3662-3671. (Pubitemid 35021229)
10. Večerek B, Rajkowitsch L, Sonnleitner E, Schroeder R, Bläsi U (2008) The Cterminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res 36: 133-143.
11. Beich-Frandsen M, Većerek B, Konarev PV, Sjöblom B, Kloiber K, et al. (2011) Structural insights into the dynamics and function of the C-terminus of the E. coli RNA chaperone Hfq. Nucleic Acids Res 39: 4900-4915.
12. Olsen AS, Møller-Jensen J, Brennan RG, Valentin-Hansen P (2010) Cterminally truncated derivatives of E. coli Hfq are proficient in riboregulation. J Mol Biol 404:173-182.
13. Someya T, Baba S, Fujimoto M, Kawai G, Kumasaka T, et al. (2012) Crystal structure of Hfq from Bacillus subtilis in complex with SELEX-derived RNA aptamer: insight into RNA-binding properties of bacterial Hfq. Nucleic Acids Res 40: 1856-1867.
14. Rochat T, Bouloc P, Yang Q, Bossi L, Figueroa-Bossi N (2012) Lack of interchangeability of Hfq-like proteins. Biochimie 94: 1554-1559.
15. 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. (Pubitemid 44477239)
16. Heidrich N, Moll I, Brantl S (2007) In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res 35: 4331-4346. (Pubitemid 47244587)
17. 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.
18. Jahn N, Preis H, Wiedemann C, Brantl S (2012) BsrG/SR4 from Bacillus subtilis-the first temperature-dependent type I toxin-antitoxin system. Mol Microbiol 83: 579-598.
19. Silvaggi JM, Perkins JB, Losick R (2006) Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J Bacteriol 188: 532-541. (Pubitemid 43100542)
20. 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.
21. Dambach M, Irnov I, Winkler WC (2013) Association of RNAs with Bacillus subtilis Hfq. PLoS One 8: e55156.
22. Liu Y, Wu N, Dong J, Gao Y, Zhang X, et al. (2010) Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus. PLoS One 5: e13069.
23. 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. (Pubitemid 40396111)
24. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366. (Pubitemid 46871039)
25. Chevalier C, Boisset S, Romilly C, Masquida B, Fechter P, et al. (2010) Staphylococcus aureus RNAIII binds to two distant regions of coa mRNA to arrest translation and promote mRNA degradation. PLoS Pathog 6: e1000809.
26. 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.
27. Jousselin A, Metzinger L, Felden B (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17: 399-405.
28. Christiansen JK, Larsen MH, Ingmer H, Sogaard-Andersen L, Kallipolitis BH (2004) The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J Bacteriol 186: 3355-3362. (Pubitemid 38661530)
29. Christiansen JK, Nielsen JS, Ebersbach T, Valentin-Hansen P, Sogaard-Andersen L, et al. (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12: 1383-1396. (Pubitemid 43990562)
30. Nielsen JS, Lei LK, Ebersbach T, Olsen AS, Klitgaard JK, et al. (2010) Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes. Nucleic Acids Res 38: 907-919.
31. Nielsen JS, Larsen MH, Lillebaek EM, Bergholz TM, Christiansen MH, et al. (2011) A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS One 6: e19019.
32. Halfmann A, Kovacs M, Hakenbeck R, Brückner R (2007) Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol Microbiol 66: 110-126. (Pubitemid 47414793)
33. Kumar R, Shah P, Swiatlo E, Burgess SC, Lawrence ML, et al. (2010) Identification of novel non-coding small RNAs from Streptococcus pneumoniae TIGR4 using high-resolution genome tiling arrays. BMC Genomics 11: 350.
34. Tsui HC, Mukherjee D, Ray VA, Sham LT, Feig AL, et al. (2010) Identification and characterization of noncoding small RNAs in Streptococcus pneumoniae serotype 2 strain D39. J Bacteriol 192: 264-279.
35. Acebo P, Martin-Galiano AJ, Navarro S, Zaballos A, Amblar M (2012) Identification of 88 regulatory small RNAs in the TIGR4 strain of the human pathogen Streptococcus pneumoniae. RNA 18: 530-546.
36. Mann B, van Opijnen T, Wang J, Obert C, Wang YD, et al. (2012) Control of virulence by small RNAs in Streptococcus pneumoniae. PLoS Pathog 8: e1002788.
37. Schnorpfeil A, Kranz M, Kovacs M, Kirsch C, Gartmann J, et al. (2013) Target evaluation of the non-coding csRNAs reveals a link of the two-component regulatory system CiaRH to competence control in Streptococcus pneumoniae R6. Mol Microbiol 89: 334-349.
38. Sonnleitner E, Schuster M, Sorger-Domenigg T, Greenberg EP, Bläsi U (2006) Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol Microbiol 59: 1542-1558.
39. Cui M, Wang T, Xu J, Ke Y, Du X, et al. (2013) Impact of Hfq on Global Gene Expression and Intracellular Survival in Brucella melitensis. PLoS One 8: e71933.
40. Härtig E, Jahn D (2012) Regulation of the anaerobic metabolism in Bacillus subtilis. Adv Microb Physiol 61: 195-216.
41. Eichenberger P, Fujita M, Jensen ST, Conlon EM, Rudner DZ, et al. (2004) The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol 2: e328.
42. Lopez D, Vlamakis H, Kolter R (2009) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33: 152-163.
43. Robertson GT, Roop RM Jr (1999) The Brucella abortus host factor I (HF-I) protein contributes to stress resistance during stationary phase and is a major determinant of virulence in mice. Mol Microbiol 34: 690-700.
44. Nakano MM, Zuber P, Glaser P, Danchin A, Hulett FM (1996) Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J Bacteriol 178: 3796-3802. (Pubitemid 26227195)
45. Nakano MM, Hoffmann T, Zhu Y, Jahn D (1998) Nitrogen and oxygen regulation of Bacillus subtilis nasDEF encoding NADH-dependent nitrite reductase by TnrA and ResDE. J Bacteriol 180: 5344-5350. (Pubitemid 28471530)
46. Nakano MM, Zuber P (1998) Anaerobic growth of a "strict aerobe" (Bacillus subtilis). Annu Rev Microbiol 52: 165-190.
47. Geng H, Zhu Y, Mullen K, Zuber CS, Nakano MM (2007) Characterization of ResDE-dependent fnr transcription in Bacillus subtilis. J Bacteriol 189: 1745- 1755.
48. Larsson JT, Rogstam A, von Wachenfeldt C (2005) Coordinated patterns of cytochrome bd and lactate dehydrogenase expression in Bacillus subtilis. Microbiology 151: 3323-3335. (Pubitemid 41488915)
49. Gyan S, Shiohira Y, Sato I, Takeuchi M, Sato T (2006) Regulatory loop between redox sensing of the NADH/NAD(+) ratio by Rex (YdiH) and oxidation of NADH by NADH dehydrogenase Ndh in Bacillus subtilis. J Bacteriol 188: 7062-7071. (Pubitemid 44547611)
50. Wang E, Bauer MC, Rogstam A, Linse S, Logan DT, et al. (2008) Structure and functional properties of the Bacillus subtilis transcriptional repressor Rex. Mol Microbiol 69: 466-478. (Pubitemid 351988017)
51. Rasmussen S, Nielsen HB, Jarmer H (2009) The transcriptionally active regions in the genome of Bacillus subtilis. Mol Microbiol 73: 1043-1057.
52. Irnov I, Sharma CM, Vogel J, Winkler WC (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res 38: 6637-6651.
53. Silvaggi JM, Perkins JB, Losick R (2005) Small untranslated RNA antitoxin in Bacillus subtilis. J Bacteriol 187: 6641-6650. (Pubitemid 41356236)
54. Hamoen LW, Venema G, Kuipers OP (2003) Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149: 9-17. (Pubitemid 36175672)
55. Schultz D, Wolynes PG, Ben Jacob E, Onuchic JN (2009) Deciding fate in adverse times: sporulation and competence in Bacillus subtilis. Proc Natl Acad Sci U S A 106: 21027-21034.
56. Leisner M, Stingl K, Frey E, Maier B (2008) Stochastic switching to competence. Curr Opin Microbiol 11: 553-559.
57. Nielsen JS, Olsen AS, Bonde M, Valentin-Hansen P, Kallipolitis BH (2008) Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190: 6264-6270.
58. Oliver HF, Orsi RH, Ponnala L, Keich U, Wang W, et al. (2009) Deep RNA sequencing of L. monocytogenes reveals overlapping and extensive stationary phase and sigma B-dependent transcriptomes, including multiple highly transcribed noncoding RNAs. BMC Genomics 10: 641.
59. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
60. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, et al. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4: e1000163.
61. Durand S, Jahn N, Condon C, Brantl S (2012) Type I toxin-antitoxin systems in Bacillus subtilis. RNA Biol 9: 1491-1497.
62. Commichau FM, Herzberg C, Tripal P, Valerius O, Stülke J (2007) A regulatory protein-protein interaction governs glutamate biosynthesis in Bacillus subtilis: the glutamate dehydrogenase RocG moonlights in controlling the transcription factor GltC. Mol Microbiol 65: 642-654. (Pubitemid 47077227)
63. Kunst F, Rapoport G (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177: 2403-2407.
64. Dunn AK, Handelsman J (1999) A vector for promoter trapping in Bacillus cereus. Gene 226: 297-305. (Pubitemid 29087110)
65. Lehnik-Habrink M, Pfortner H, Rempeters L, Pietack N, Herzberg C, et al. (2010) The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 77: 958-971.
66. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
67. Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, et al. (2009) Fast mapping of short sequences with mismatches, insertions and deletions using index structures. PLoS Comput Biol 5: e1000502.
68. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
69. Bernhart SH, Hofacker IL, Stadler PF (2006) Local RNA base pairing probabilities in large sequences. Bioinformatics 22: 614-615. (Pubitemid 43372823)
70. Lorenz R, Bernhart SH, Höner Zu Siederdissen C, Tafer H, Flamm C, et al. (2011) ViennaRNA Package 2.0. Algorithms Mol Biol 6: 26.
71. Tafer H, Amman F, Eggenhofer F, Stadler PF, Hofacker IL (2011) Fast accessibility-based prediction of RNA-RNA interactions. Bioinformatics 27: 1934-1940.