Dual RpoH sigma factors and transcriptional plasticity in a symbiotic bacterium

Journal of Bacteriology

Volumn 194, Issue 18, 2012, Pages 4983-4994

  Barnett, Melanie J ^a   Bittner, Alycia N ^b,c   Toman, Carol J ^a   Oke, Valerie ^b   Long, Sharon R ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; SIGMA FACTOR; SIGMA FACTOR RPOH; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; COMPUTER PROGRAM; CONSENSUS SEQUENCE; DATA MINING; DNA MICROARRAY; ESCHERICHIA COLI; EUBACTERIUM; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; NITROGEN FIXATION; NONHUMAN; NUCLEIC ACID AMPLIFICATION; PLANT ROOT; PRIORITY JOURNAL; PROMOTER REGION; REPLICON; SAPROTROPH; SINORHIZOBIUM MELILOTI; SOIL MICROFLORA; SYMBIOSIS; TRANSCRIPTIONAL PLASTICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SINORHIZOBIUM MELILOTI;

EID: 84866372439     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00449-12     Document Type: Article

References (69)

1. Bailey TL, Williams N, Misleh C, Li WW. 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34:W369-W373.
2. Barnett MJ, Fisher RF. 2006. Global gene expression in the rhizobiallegume symbiosis. Symbiosis 42:1-24.
3. Barnett MJ, Toman CJ, Fisher RF, Long SR. 2004. A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc. Natl. Acad. Sci. U. S. A. 101:16636-16641.
4. Bastiat B, Sauviac L, Bruand C. 2010. Dual control of Sinorhizobium meliloti RpoE2 sigma factor activity by two PhyR-type two-component response regulators. J. Bacteriol. 192:2255-2265.
5. Becker A, et al. 2004. Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol. Plant Microbe Interact. 17:292-303.
6. Bishop RE, Leskiw BK, Hodges RS, Kay CM, Weiner JH. 1998. The entericidin locus of Escherichia coli and its implications for programmed bacterial cell death. J. Mol. Biol. 280:583-596.
7. Bittner AN, Oke V. 2006. Multiple groESL operons are not key targets of RpoH1 and RpoH2 in Sinorhizobium meliloti. J. Bacteriol. 188:3507-3515.
8. Capela D, Filipe C, Bobik C, Batut J, Bruand C. 2006. Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection.Mol. Plant Microbe Interact. 19:363-372.
9. Delory M, Hallez R, Letesson JJ, De Bolle X. 2006. An RpoH-like heat shock sigma factor is involved in stress response and virulence in Brucella melitensis 16M. J. Bacteriol. 188:7707-7710.
10. de Lucena DK, Pühler A, Weidner S. 2010. The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Microbiol.10:265. doi:10.1186/1471-2180-10-265.
11. del Val C, Rivas E, Torres-Quesada O, Toro N, Jiménez-Zurdo JI. 2007. Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics.Mol. Microbiol. 66:1080-1091.
12. Dóminguez-Ferreras A, et al. 2006. Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J. Bacteriol. 188:7617-7625.
13. Downie JA. 2010. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol.Rev. 34:150-170.
14. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus:NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
15. Fischer HM. 1994. Genetic regulation of nitrogen fixation in rhizobia.Microbiol. Rev. 58:352-386.
16. Fisher RF, Long SR. 1992. Rhizobium-plant signal exchange. Nature 357:655-660.
17. Flechard M, et al. 2010. RpoE2 of Sinorhizobium meliloti is necessary for trehalose synthesis and growth in hyperosmotic media. Microbiology 156:1708-1718.
18. Flechard M, Fontenelle C, Trautwetter A, Ermel G, Blanco C. 2009.Sinorhizobium meliloti rpoE2 is necessary forH2O2 stress resistance during the stationary growth phase. FEMS Microbiol. Lett. 290:25-31.
19. Galibert F, et al. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
20. Gibson KE, Kobayashi H, Walker GC. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441.
21. Glazebrook J, Walker GC. 1991. Genetic techniques in Rhizobium meliloti. Methods Enzymol. 204:398-418.
22. Green HA, Donohue TJ. 2006. Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. J.Bacteriol. 188:5712-5721.
23. Gruber TM, Gross CA. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57:441-466.
24. Guisbert E, Yura T, Rhodius VA, Gross CA. 2008. Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol. Mol. Biol. Rev. 72:545-554.
25. Gunesekere IC, et al. 2006. Comparison of the RpoH-dependent regulon and general stress response in Neisseria gonorrhoeae. J. Bacteriol. 188:4769-4776.
26. Hellweg C, Pühler A, Weidner S. 2009. The time course of the transcrip-tomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol. 9:37. doi:10.1186/1471-2180-9-37.
27. Hengge-Aronis R, Klein W, Lange R, Rimmele M, Boos W. 1991.Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance inEscherichia coli. J. Bacteriol. 173:7918-7924.
28. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model.Nat. Rev. Microbiol. 5:619-633.
29. 32 suggests a composite-10 region with an 'extended -10' motif and a core -10 element. Mol. Microbiol.72:815-829.
30. Koo BM, Rhodius VA, Nonaka G, deHaseth PL, Gross CA. 2009.Reduced capacity of alternative Σs to melt promoters ensures stringent promoter recognition. Genes Dev. 23:2426-2436.
31. Krol E, Becker A. 2011. ppGpp in Sinorhizobium meliloti: biosynthesis in response to sudden nutritional downshifts and modulation of the transcriptome. Mol. Microbiol. 81:1233-1254.
32. MacLellan SR, MacLean AM, Finan TM. 2006. Promoter prediction in the rhizobia. Microbiology 152:1751-1763.
33. Martínez-Salazar JM, et al. 2009. The Rhizobium etli RpoH1 and RpoH2 sigma factors are involved in different stress responses. Microbiology 155:386-397.
34. McGrath PT, et al. 2007. High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat. Biotechnol.25:584-592.
35. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM. 1982.Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J.Bacteriol. 149:114-122.
36. Meilhoc E, Cam Y, Skapski A, Bruand C. 2010. The response to nitric oxide of the nitrogen-fixing symbiont Sinorhizobium meliloti. Mol. Plant Microbe Interact. 23:748-759.
37. Mergaert P, et al. 2006. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl. Acad. Sci.U. S. A. 103:5230-5235.
38. Minder AC, Fischer HM, Hennecke H, Narberhaus F. 2000. Role of HrcA and CIRCE in the heat shock regulatory network of Bradyrhizobium japonicum. J. Bacteriol. 182:14-22.
39. 32-dependent class of heat shock genes in Bradyrhizobium japonicum. Mol. Gen. Genet. 254:195-206.
40. Mitsui H, Sato T, Sato Y, Ito N, Minamisawa K. 2004. Sinorhizobium meliloti RpoH1 is required for effective nitrogen-fixing symbiosis with alfalfa. Mol. Genet. Genomics 271:416-425.
41. 32 homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens. J. Bacteriol. 181:7509-7515.
42. Narberhaus F. 1999. Negative regulation of bacterial heat shock genes. Mol. Microbiol. 31:1-8.
43. 32-like transcription factors in Bradyrhizobium japonicum. Mol. Microbiol. 24:93-104.
44. Neumann M, et al. 2009. A periplasmic aldehyde oxidoreductase represents the first molybdopterin cytosine dinucleotide cofactor containing molybdo-flavoenzyme from Escherichia coli. FEBS J. 276:2762-2774.
45. 32, reveals a multifaceted cellular response to heat stress. Genes Dev. 20:1776-1789.
46. Nuss AM, Glaeser J, Berghoff BA, Klug G. 2010. Overlapping alternative sigma factor regulons in the response to singlet oxygen in Rhodobacter sphaeroides. J. Bacteriol. 192:2613-2623.
47. Oke V, Rushing BG, Fisher EJ, Moghadam-Tabrizi M, Long SR. 2001. Identification of the heat-shock sigma factor RpoH and a second RpoHlike protein in Sinorhizobium meliloti. Microbiology 147:2399-2408.
48. Ono Y, Mitsui H, Sato T, Minamisawa K. 2001. Two RpoH homologs responsible for the expression of heat shock protein genes in Sinorhizobium meliloti. Mol. Gen. Genet. 264:902-912.
49. Österberg S, Del Peso-Santos T, Shingler V. 2011. Regulation of alternative sigma factor use. Annu. Rev. Microbiol. 65:37-55.
50. E promoters. Nucleic Acids Res. 40:2907-2924.
51. E stress response in related genomes. PLoSBiol. 4:e2. doi:10.1371/journal.pbio.0040002.
52. Sauviac L, Philippe H, Phok K, Bruand C. 2007. An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. J. Bacteriol. 189:4204-4216.
53. Schlüter JP, et al. 2010. A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti. BMC Genomics 11:245. doi:10.1186/1471-2164-11-245.
54. Slamti L, Livny J, Waldor MK. 2007. Global gene expression and phenotypic analysis of a Vibrio cholerae rpoH deletion mutant. J. Bacteriol.189:351-362.
55. Srivatsan A, Wang JD. 2008. Control of bacterial transcription, translation and replication by (p)ppGpp. Curr. Opin. Microbiol. 11:100-105.
56. Staron' A, et al. 2009. The third pillar of bacterial signal transduction:classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol. Microbiol. 74:557-581.
57. Storz G, Hengge R (ed). 2011. Bacterial stress responses, 2nd ed. ASM Press, Washington, DC.
58. Storz G, Vogel J, Wassarman KM. 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43:880-891.
59. Turatsinze JV, Thomas-Chollier M, Defrance M, van Helden J. 2008.Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nat. Protoc. 3:1578-1588.
60. E subunit of RNA polymerase. Mol. Microbiol.63:1296-1306.
61. Ulvé VM, Sevin EW, Cheron A, Barloy-Hubler F. 2007. Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021. BMCGenomics 8:467. doi:10.1186/1471-2164-8-467.
62. Valverde C, et al. 2008. Prediction of Sinorhizobium meliloti sRNA genes and experimental detection in strain 2011. BMC Genomics 9:416. doi:10.1186/1471-2164-9-416.
63. Wade JT, et al. 2006. Extensive functional overlap between sigma factors in Escherichia coli. Nat. Struct. Mol. Biol. 13:806-814.
64. Waldminghaus T, Fippinger A, Alfsmann J, Narberhaus F. 2005. RNA thermometers are common in α- and -proteobacteria. Biol. Chem. 386:1279-1286.
65. Waldminghaus T, Skarstad K. 2010. ChIP on Chip: surprising results are often artifacts. BMC Genomics 11:414. doi:10.1186/1471-2164-11-414.
66. Wells DH, Long SR. 2002. The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis. Mol. Microbiol. 43:1115-1127.
67. White J, Prell J, James EK, Poole P. 2007. Nutrient sharing between symbionts. Plant Physiol. 144:604-614.
68. Wood JM. 2007. Bacterial osmosensing transporters. Methods Enzymol.428:77-107.
69. 32 in vivo. J. Biol. Chem.280:17758-17768.