The diversity and evolution of cell cycle regulation in alpha-proteobacteria: A comparative genomic analysis

BMC Systems Biology

Volumn 4, Issue , 2010, Pages

  Brilli, Matteo ^a,b   Fondi, Marco ^a   Fani, Renato ^a   Mengoni, Alessio ^a   Ferri, Lorenzo ^a   Bazzicalupo, Marco ^a   Biondi, Emanuele G ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CAULOBACTER; CAULOBACTER VIBRIOIDES; CAULOBACTERALES; RHIZOBIALES; RHODOBACTERALES;

BACTERIAL PROTEIN; CTRA PROTEIN, CAULOBACTER; DNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ALPHAPROTEOBACTERIA; ARTICLE; BINDING SITE; BIOLOGICAL MODEL; CAULOBACTER CRESCENTUS; CELL CYCLE; COMPARATIVE STUDY; DNA METHYLATION; GENETIC VARIABILITY; GENETICS; GENOMICS; MOLECULAR EVOLUTION; PHOSPHORYLATION; PHYLOGENY;

ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; BINDING SITES; CAULOBACTER CRESCENTUS; CELL CYCLE; DNA METHYLATION; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOMICS; MODELS, GENETIC; PHOSPHORYLATION; PHYLOGENY; TRANSCRIPTION FACTORS;

EID: 77951601819     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-4-52     Document Type: Article

References (65)

1. Fawcett P, Eichenberger P, Losick R, Youngman P. The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 2000, 97:8063-8068. 10.1073/pnas.140209597, 16670, 10869437.
2. Haeusser DP, Levin PA. The great divide: coordinating cell cycle events during bacterial growth and division. Curr Opin Microbiol 2008, 11:94-99. 10.1016/j.mib.2008.02.008, 2397022, 18396093.
3. Bowers LM, Shapland EB, Ryan KR. Who's in charge here? Regulating cell cycle regulators. Curr Opin Microbiol 2008, 11:547-552. 10.1016/j.mib.2008.09.019, 18955157.
4. Laub MT, Shapiro L, McAdams HH. Systems biology of Caulobacter. Annu Rev Genet 2007, 41:429-441. 10.1146/annurev.genet.41.110306.130346, 18076330.
5. Purcell EB, Boutte CC, Crosson S. Two-component signaling systems and cell cycle control in Caulobacter crescentus. Adv Exp Med Biol 2008, 631:122-130. full_text, 18792685.
6. Skerker JM, Laub MT. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2004, 2:325-337. 10.1038/nrmicro864, 15031731.
7. Domian IJ, Quon KC, Shapiro L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 1997, 90:415-424. 10.1016/S0092-8674(00)80502-4, 9267022.
8. Quon KC, Marczynski GT, Shapiro L. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 1996, 84:83-93. 10.1016/S0092-8674(00)80995-2, 8548829.
9. Reisenauer A, Quon K, Shapiro L. The CtrA response regulator mediates temporal control of gene expression during the Caulobacter cell cycle. J Bacteriol 1999, 181:2430-2439. 93667, 10198005.
10. Biondi EG, Skerker JM, Arif M, Prasol MS, Perchuk BS, Laub MT. A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 2006, 59:386-401. 10.1111/j.1365-2958.2005.04970.x, 16390437.
11. Collier J, McAdams HH, Shapiro L. A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc Natl Acad Sci USA 2007, 104:17111-17116. 10.1073/pnas.0708112104, 2040471, 17942674.
12. Jones SE, Ferguson NL, Alley MR. New members of the ctrA regulon: the major chemotaxis operon in Caulobacter is CtrA dependent. Microbiology 2001, 147:949-958.
13. Laub MT, Chen SL, Shapiro L, McAdams HH. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci USA 2002, 99:4632-4637. 10.1073/pnas.062065699, 123699, 11930012.
14. Skerker JM, Shapiro L. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 2000, 19:3223-3234. 10.1093/emboj/19.13.3223, 313932, 10880436.
15. Wortinger M, Sackett MJ, Brun YV. CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 2000, 19:4503-4512. 10.1093/emboj/19.17.4503, 302065, 10970844.
16. Collier J, Murray SR, Shapiro L. DnaA couples DNA replication and the expression of two cell cycle master regulators. EMBO J 2006, 25:346-356. 10.1038/sj.emboj.7600927, 1383511, 16395331.
17. Gorbatyuk B, Marczynski GT. Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus. Mol Microbiol 2005, 55:1233-1245. 10.1111/j.1365-2958.2004.04459.x, 15686567.
18. Hottes AK, Shapiro L, McAdams HH. DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 2005, 58:1340-1353.
19. Holtzendorff J, Hung D, Brende P, Reisenauer A, Viollier PH, McAdams HH, Shapiro L. Oscillating global regulators control the genetic circuit driving a bacterial cell cycle. Science 2004, 304:983-987. 10.1126/science.1095191, 15087506.
20. Biondi EG, Reisinger SJ, Skerker JM, Arif M, Perchuk BS, Ryan KR, Laub MT. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 2006, 444:899-904. 10.1038/nature05321, 17136100.
21. Jacobs C, Domian IJ, Maddock JR, Shapiro L. Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 1999, 97:111-120. 10.1016/S0092-8674(00)80719-9, 10199407.
22. Burton GJ, Hecht GB, Newton A. Roles of the histidine protein kinase pleC in Caulobacter crescentus motility and chemotaxis. J Bacteriol 1997, 179:5849-5853. 179476, 9294444.
23. Ohta N, Lane T, Ninfa EG, Sommer JM, Newton A. A histidine protein kinase homologue required for regulation of bacterial cell division and differentiation. Proc Natl Acad Sci USA 1992, 89:10297-10301. 10.1073/pnas.89.21.10297, 50325, 1438215.
24. Sommer JM, Newton A. Pseudoreversion analysis indicates a direct role of cell division genes in polar morphogenesis and differentiation in Caulobacter crescentus. Genetics 1991, 129:623-630. 1204729, 1752411.
25. Wu J, Ohta N, Newton A. An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter. Proc Natl Acad Sci USA 1998, 95:1443-1448. 10.1073/pnas.95.4.1443, 19037, 9465034.
26. Weiss V, Kramer G, Dunnebier T, Flotho A. Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. J Mol Microbiol Biotechnol 2002, 4:229-233.
27. Jacobs C, Hung D, Shapiro L. Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc Natl Acad Sci USA 2001, 98:4095-4100. 10.1073/pnas.051609998, 31185, 11274434.
28. Wheeler RT, Shapiro L. Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol Cell 1999, 4:683-694. 10.1016/S1097-2765(00)80379-2, 10619016.
29. Radhakrishnan SK, Thanbichler M, Viollier PH. The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev 2008, 22:212-225. 10.1101/gad.1601808, 2192755, 18198338.
30. Iniesta AA, McGrath PT, Reisenauer A, McAdams HH, Shapiro L. A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci USA 2006, 103:10935-10940. 10.1073/pnas.0604554103, 1544152, 16829582.
31. Jenal U, Fuchs T. An essential protease involved in bacterial cell-cycle control. EMBO J 1998, 17:5658-5669. 10.1093/emboj/17.19.5658, 1170894, 9755166.
32. McGrath PT, Iniesta AA, Ryan KR, Shapiro L, McAdams HH. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 2006, 124:535-547. 10.1016/j.cell.2005.12.033, 16469700.
33. Ryan KR. Partners in crime: phosphotransfer profiling identifies a multicomponent phosphorelay. Mol Microbiol 2006, 59:361-363. 10.1111/j.1365-2958.2005.04980.x, 16390433.
34. Ryan KR, Huntwork S, Shapiro L. Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis. Proc Natl Acad Sci USA 2004, 101:7415-7420. 10.1073/pnas.0402153101, 409933, 15123835.
35. Hallez R, Bellefontaine AF, Letesson JJ, De Bolle X. Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol 2004, 12:361-365. 10.1016/j.tim.2004.06.002, 15276611.
36. Lang AS, Beatty JT. Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci USA 2000, 97:859-864. 10.1073/pnas.97.2.859, 15421, 10639170.
37. Lang AS, Beatty JT. A bacterial signal transduction system controls genetic exchange and motility. J Bacteriol 2002, 184:913-918. 10.1128/jb.184.4.913-918.2002, 134786, 11807050.
38. Bellefontaine AF, Pierreux CE, Mertens P, Vandenhaute J, Letesson JJ, De Bolle X. Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 2002, 43:945-960. 10.1046/j.1365-2958.2002.02777.x, 11929544.
39. Robertson GT, Reisenauer A, Wright R, Jensen RB, Jensen A, Shapiro L, Roop RM. The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 2000, 182:3482-3489. 10.1128/JB.182.12.3482-3489.2000, 101938, 10852881.
40. Miller TR, Belas R. Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environ Microbiol 2006, 8:1648-1659. 10.1111/j.1462-2920.2006.01071.x, 16913924.
41. Kahng LS, Shapiro L. The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 2001, 183:3065-3075. 10.1128/JB.183.10.3065-3075.2001, 95206, 11325934.
42. Gupta RS, Mok A. Phylogenomics and signature proteins for the alpha proteobacteria and its main groups. BMC Microbiol 2007, 7:106. 10.1186/1471-2180-7-106, 2241609, 18045498.
43. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 1999, 96:4285-4288. 10.1073/pnas.96.8.4285, 16324, 10200254.
44. Laub MT, McAdams HH, Feldblyum T, Fraser CM, Shapiro L. Global analysis of the genetic network controlling a bacterial cell cycle. Science 2000, 290:2144-2148. 10.1126/science.290.5499.2144, 11118148.
45. Roth FP, Hughes JD, Estep PW, Church GM. Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation. Nat Biotechnol 1998, 16:939-945. 10.1038/nbt1098-939, 9788350.
46. Brassinga AK, Siam R, McSween W, Winkler H, Wood D, Marczynski GT. Conserved response regulator CtrA and IHF binding sites in the alpha-proteobacteria Caulobacter crescentus and Rickettsia prowazekii chromosomal replication origins. J Bacteriol 2002, 184:5789-5799. 10.1128/JB.184.20.5789-5799.2002, 139603, 12270838.
47. Stephens C, Reisenauer A, Wright R, Shapiro L. A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 1996, 93:1210-1214. 10.1073/pnas.93.3.1210, 40058, 8577742.
48. Wright R, Stephens C, Shapiro L. The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 1997, 179:5869-5877. 179479, 9294447.
49. Hansen FG, Christensen BB, Atlung T. Sequence characteristics required for cooperative binding and efficient in vivo titration of the replication initiator protein DnaA in E. coli. J Mol Biol 2007, 367:942-952. 10.1016/j.jmb.2007.01.056, 17316685.
50. Ishikawa S, Ogura Y, Yoshimura M, Okumura H, Cho E, Kawai Y, Kurokawa K, Oshima T, Ogasawara N. Distribution of stable DnaA-binding sites on the Bacillus subtilis genome detected using a modified ChIP-chip method. DNA Res 2007, 14:155-168. 10.1093/dnares/dsm017, 2533591, 17932079.
51. Collier J, Shapiro L. Spatial complexity and control of a bacterial cell cycle. Curr Opin Biotechnol 2007, 18:333-340. 10.1016/j.copbio.2007.07.007, 2716793, 17709236.
52. Barnett MJ, Hung DY, Reisenauer A, Shapiro L, Long SR. A homolog of the CtrA cell cycle regulator is present and essential in Sinorhizobium meliloti. J Bacteriol 2001, 183:3204-3210. 10.1128/JB.183.10.3204-3210.2001, 95222, 11325950.
53. McGrath PT, Lee H, Zhang L, Iniesta AA, Hottes AK, Tan MH, Hillson NJ, Hu P, Shapiro L, McAdams HH. High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat Biotechnol 2007, 25:584-592. 10.1038/nbt1294, 17401361.
54. Sibley CD, MacLellan SR, Finan T. The Sinorhizobium meliloti chromosomal origin of replication. Microbiology 2006, 152:443-455. 10.1099/mic.0.28455-0, 16436432.
55. Ohta N, Newton A. The core dimerization domains of histidine kinases contain recognition specificity for the cognate response regulator. J Bacteriol 2003, 185:4424-4431. 10.1128/JB.185.15.4424-4431.2003, 165744, 12867451.
56. Reisinger SJ, Huntwork S, Viollier PH, Ryan KR. DivL performs critical cell cycle functions in Caulobacter crescentus independent of kinase activity. J Bacteriol 2007, 189:8308-8320. 10.1128/JB.00868-07, 2168681, 17827294.
57. Gupta RS. Protein signatures distinctive of alpha proteobacteria and its subgroups and a model for alpha-proteobacterial evolution. Crit Rev Microbiol 2005, 31:101-135. 10.1080/10408410590922393, 15986834.
58. Sallstrom B, Andersson SG. Genome reduction in the alpha-Proteobacteria. Curr Opin Microbiol 2005, 8:579-585. 10.1016/j.mib.2005.08.002, 16099701.
59. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009, 37:D141-145. 10.1093/nar/gkn879, 2686447, 19004872.
60. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113. 10.1186/1471-2105-5-113, 517706, 15318951.
61. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
62. Schneider TD, Stormo GD, Gold L, Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J Mol Biol 1986, 188:415-431. 10.1016/0022-2836(86)90165-8, 3525846.
63. Liu XS, Brutlag DL, Liu JS. An algorithm for finding protein-DNA binding sites with applications to chromatin-immunoprecipitation microarray experiments. Nat Biotechnol 2002, 20:835-839.
64. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001, 29:22-28. 10.1093/nar/29.1.22, 29819, 11125040.
65. Whelan S, Lio P, Goldman N. Molecular phylogenetics: state-of-the-art methods for looking into the past. Trends Genet 2001, 17:262-272. 10.1016/S0168-9525(01)02272-7, 11335036.