Small Regulatory RNA-Induced Growth Rate Heterogeneity of Bacillus subtilis

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Mars, Ruben A T ^a   Nicolas, Pierre ^b   Ciccolini, Mariano ^a   Reilman, Ewoud ^a   Reder, Alexander ^c   Schaffer, Marc ^c   Mäder, Ulrike ^c   Völker, Uwe ^c   van Dijl, Jan Maarten ^a   Denham, Emma L ^a,d  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b INRA Institut National de la Recherche Agronomique   (France)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABRB PROTEIN; BACTERIAL PROTEIN; RNA; SMALL REGULATORY RNA; UNCLASSIFIED DRUG; ABRB PROTEIN, BACILLUS SUBTILIS; DNA BINDING PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR;

ABRB GENE; ARTICLE; AUTOREGULATION; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GROWTH; CELL INTERACTION; CONTROLLED STUDY; GENE DELETION; GROWTH RATE; GROWTH REGULATION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN RNA BINDING; RNA PROCESSING; TRANSCRIPTION REGULATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC HETEROGENEITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC HETEROGENEITY; PROMOTER REGIONS, GENETIC; RNA; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84926359782     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005046     Document Type: Article

References (66)

1. Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, et al. (2012) Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science335(6072): 1099–1103. doi: 10.1126/science.120687122383848
2. Beisel CL, Storz G, . (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev34(5): 866–882. doi: 10.1111/j.1574-6976.2010.00241.x20662934
3. Storz G, Vogel J, Wassarman KM, . (2011) Regulation by small RNAs in bacteria: Expanding frontiers. Mol Cell43(6): 880–891. doi: 10.1016/j.molcel.2011.08.02221925377
4. Aiba H, . (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol10(2): 134–139. 17383928
5. 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 A105(33): 11927–11932. doi: 10.1073/pnas.071175210518697947
6. 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 Microbiol62(2): 520–536. 17020585
7. 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 Bacteriol194(10): 2594–2605. doi: 10.1128/JB.05990-1122389480
8. Irnov I, Sharma CM, Vogel J, Winkler WC, . (2010) Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res38(19): 6637–6651. doi: 10.1093/nar/gkq45420525796
9. Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, et al. (2012) Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science335(6072): 1103–1106. doi: 10.1126/science.120684822383849
10. Raj A, van Oudenaarden A, . (2008) Nature, nurture, or chance: Stochastic gene expression and its consequences. Cell135(2): 216–226. doi: 10.1016/j.cell.2008.09.05018957198
11. Losick R, Desplan C, . (2008) Stochasticity and cell fate. Science320(5872): 65–68. doi: 10.1126/science.114788818388284
12. Maamar H, Raj A, Dubnau D, . (2007) Noise in gene expression determines cell fate in Bacillus subtilis. Science317(5837): 526–529. 17569828
13. Chastanet A, Vitkup D, Yuan GC, Norman TM, Liu JS, et al. (2010) Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis. Proc Natl Acad Sci U S A107(18): 8486–8491. doi: 10.1073/pnas.100249910720404177
14. Veening JW, Smits WK, Kuipers OP, . (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol62: 193–210. doi: 10.1146/annurev.micro.62.081307.16300218537474
15. Elowitz MB, Levine AJ, Siggia ED, Swain PS, . (2002) Stochastic gene expression in a single cell. Science297(5584): 1183–1186. 12183631
16. Paulsson J, . (2004) Summing up the noise in gene networks. Nature427(6973): 415–418. 14749823
17. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S, . (2004) Bacterial persistence as a phenotypic switch. Science305(5690): 1622–1625. 15308767
18. Eldar A, Elowitz MB, . (2010) Functional roles for noise in genetic circuits. Nature467(7312): 167–173. doi: 10.1038/nature0932620829787
19. Madar D, Dekel E, Bren A, Alon U, . (2011) Negative auto-regulation increases the input dynamic-range of the arabinose system of Escherichia coli. BMC Syst Biol5. doi: 10.1186/1752-0509-5-111.Negative21749723
20. Saile E, Koehler TM, . (2002) Control of anthrax toxin gene expression by the transition state regulator abrB. J Bacteriol184(2): 370–380. 11751813
21. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science294(5543): 849–852. 11679669
22. Fisher SH, Strauch MA, Atkinson MR, Wray LV, Jr. (1994) Modulation of Bacillus subtilis catabolite repression by transition state regulatory protein AbrB. J Bacteriol176(7): 1903–1912. 8144456
23. Mader U, Schmeisky AG, Florez LA, Stulke J, . (2012) SubtiWiki—a comprehensive community resource for the model organism Bacillus subtilis. Nucleic Acids Res40(Database issue): D1278–87. doi: 10.1093/nar/gkr92322096228
24. Chumsakul O, Takahashi H, Oshima T, Hishimoto T, Kanaya S, et al. (2011) Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation. Nucleic Acids Res39(2): 414–428. doi: 10.1093/nar/gkq78020817675
25. Bobay BG, Benson L, Naylor S, Feeney B, Clark AC, et al. (2004) Evaluation of the DNA binding tendencies of the transition state regulator AbrB. Biochemistry43(51): 16106–16118. 15610005
26. Banse AV, Chastanet A, Rahn-Lee L, Hobbs EC, Losick R, . (2008) Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis. Proc Natl Acad Sci U S A105(40): 15547–15552. doi: 10.1073/pnas.080520310518840696
27. 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 A106(50): 21027–21034. doi: 10.1073/pnas.091218510619995980
28. Schmalisch M, Maiques E, Nikolov L, Camp AH, Chevreux B, et al. (2010) Small genes under sporulation control in the Bacillus subtilis genome. J Bacteriol192(20): 5402–5412. doi: 10.1128/JB.00534-1020709900
29. Will S, Joshi T, Hofacker IL, Stadler PF, Backofen R, . (2012) LocARNA-P: Accurate boundary prediction and improved detection of structural RNAs. RNA18(5): 900–914. doi: 10.1261/rna.029041.11122450757
30. Hofacker IL, Stadler PF, . (2006) Memory efficient folding algorithms for circular RNA secondary structures. Bioinformatics22(10): 1172–1176. 16452114
31. Nicholson WL, . (2012) Increased competitive fitness of Bacillus subtilis under nonsporulating conditions via inactivation of pleiotropic regulators AlsR, SigD, and SigW. Appl Environ Microbiol78(9): 3500–3503. doi: 10.1128/AEM.07742-1122344650
32. Tjaden B, . (2008) TargetRNA: A tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res36(Web Server issue): W109–13. doi: 10.1093/nar/gkn26418477632
33. Horsburgh MJ, Moir A, . (1999) Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol32(1): 41–50. 10216858
34. Xu K, Clark D, Strauch MA, . (1996) Analysis of abrB mutations, mutant proteins, and why abrB does not utilize a perfect consensus in the-35 region of its sigma A promoter. J Biol Chem271(5): 2621–2626. 8576231
35. Hahn J, Roggiani M, Dubnau D, . (1995) The major role of Spo0A in genetic competence is to downregulate abrB, an essential competence gene. J Bacteriol177(12): 3601–3605. 7768874
36. Deana A, Belasco JG, . (2005) Lost in translation: The influence of ribosomes on bacterial mRNA decay. Genes Dev19(21): 2526–2533. 16264189
37. Peer A, Margalit H, . (2011) Accessibility and evolutionary conservation mark bacterial small-RNA target-binding regions. J Bacteriol193(7): 1690–1701. doi: 10.1128/JB.01419-1021278294
38. Botella E, Fogg M, Jules M, Piersma S, Doherty G, et al. (2010) pBaSysBioII: An integrative plasmid generating gfp transcriptional fusions for high-throughput analysis of gene expression in Bacillus subtilis. Microbiology156(Pt 6): 1600–1608. doi: 10.1099/mic.0.035758-020150235
39. Doherty GP, Fogg MJ, Wilkinson AJ, Lewis PJ, . (2010) Small subunits of RNA polymerase: Localization, levels and implications for core enzyme composition. Microbiology156(Pt 12): 3532–3543. doi: 10.1099/mic.0.041566-020724389
40. Smits WK, Kuipers OP, Veening JW, . (2006) Phenotypic variation in bacteria: The role of feedback regulation. Nat Rev Microbiol4(4): 259–271. 16541134
41. Greene EA, Spiegelman GB, . (1996) The Spo0A protein of Bacillus subtilis inhibits transcription of the abrB gene without preventing binding of the polymerase to the promoter. J Biol Chem271(19): 11455–11461. 8626703
42. Becskei A, Serrano L, . (2000) Engineering stability in gene networks by autoregulation. Nature405(6786): 590–593. 10850721
43. Dublanche Y, Michalodimitrakis K, Kummerer N, Foglierini M, Serrano L, . (2006) Noise in transcription negative feedback loops: Simulation and experimental analysis. Mol Syst Biol2: 41. 16883354
44. Kearns DB, Losick R, . (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev19(24): 3083–3094. 16357223
45. Levine E, Zhang Z, Kuhlman T, Hwa T, . (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol5(9): e229. 17713988
46. Arbel-Goren R, Tal A, Friedlander T, Meshner S, Costantino N, et al. (2013) Effects of post-transcriptional regulation on phenotypic noise in Escherichia coli. Nucleic Acids Res41(9): 4825–4834. doi: 10.1093/nar/gkt18423519613
47. Jia Y, Liu W, Li A, Yang L, Zhan X, . (2009) Intrinsic noise in post-transcriptional gene regulation by small non-coding RNA. Biophys Chem143(1–2): 60–69. doi: 10.1016/j.bpc.2009.05.00319487068
48. Hambraeus G, von Wachenfeldt C, Hederstedt L, . (2003) Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs. Mol Genet Genomics269(5): 706–714. 12884008
49. Jost D, Nowojewski A, Levine E, . (2013) Regulating the many to benefit the few: Role of weak small RNA targets. Biophys J104(8): 1773–1782. doi: 10.1016/j.bpj.2013.02.02023601324
50. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, et al. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol184(17): 4881–4890. 12169614
51. Reilman E, Mars RA, van Dijl JM, Denham EL, . (2015) The multidrug ABC transporter BmrC/BmrD of Bacillus subtilis is regulated via a ribosome-mediated transcriptional attenuation mechanism. Nucleic Acids Res42(18): 11393–11407.
52. Piersma S, Denham EL, Drulhe S, Tonk RH, Schwikowski B, et al. (2013) TLM-quant: An open-source pipeline for visualization and quantification of gene expression heterogeneity in growing microbial cells. PLoS One8(7): e68696. doi: 10.1371/journal.pone.006869623874729
53. Gefen O, Balaban NQ, . (2009) The importance of being persistent: Heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol Rev33(4): 704–717. doi: 10.1111/j.1574-6976.2008.00156.x19207742
54. Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A, . (1986) The rate of killing of Escherichia coli by ß-lactam antibiotics is strictly proportional to the rate of bacterial growth. Journal of General Microbiology132(5): 1297–1304. 3534137
55. Hecker M, Pane-Farre J, Volker U, . (2007) SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria. Annu Rev Microbiol61: 215–236. 18035607
56. Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, et al. (2010) Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc Natl Acad Sci U S A107(28): 12541–12546. doi: 10.1073/pnas.100433310720616060
57. Kunst F, Rapoport G, . (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol177(9): 2403–2407. 7730271
58. Tanaka K, Henry CS, Zinner JF, Jolivet E, Cohoon MP, et al. (2013) Building the repertoire of dispensable chromosome regions in Bacillus subtilis entails major refinement of cognate large-scale metabolic model. Nucleic Acids Res41(1): 687–699. doi: 10.1093/nar/gks96323109554
59. Darmon E, Dorenbos R, Meens J, Freudl R, Antelmann H, et al. (2006) A disulfide bond-containing alkaline phosphatase triggers a BdbC-dependent secretion stress response in Bacillus subtilis. Appl Environ Microbiol72(11): 6876–6885. 17088376
60. Quan J, Tian J, . (2009) Circular polymerase extension cloning of complex gene libraries and pathways. PLoS One4(7): e6441. doi: 10.1371/journal.pone.000644119649325
61. Haun RS, Serventi IM, Moss J, . (1992) Rapid, reliable ligation-independent cloning of PCR products using modified plasmid vectors. BioTechniques13(4): 515–518. 1362067
62. Ki JS, Zhang W, Qian PY, . (2009) Discovery of marine bacillus species by 16S rRNA and rpoB comparisons and their usefulness for species identification. J Microbiol Methods77(1): 48–57. doi: 10.1016/j.mimet.2009.01.00319166882
63. Homuth G, Masuda S, Mogk A, Kobayashi Y, Schumann W, . (1997) The dnaK operon of Bacillus subtilis is heptacistronic. J Bacteriol179(4): 1153–1164. 9023197
64. Zweers JC, Wiegert T, van Dijl JM, . (2009) Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl Environ Microbiol75(23): 7356–7364. doi: 10.1128/AEM.01560-0919820159
65. Shock JL, Fischer KF, DeRisi JL, . (2007) Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol8(7): R134. 17612404
66. Gillespie DT, . (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem81(25): 2340–2361.