Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators

Nature Communications

Volumn 5, Issue , 2014, Pages

  Fumeaux, Coralie ^a   Radhakrishnan, Sunish Kumar ^a,c   Ardissone, Silvia ^a,d   Théraulaz, Laurence ^a   Frandi, Antonio ^a   Martins, Daniel ^a   Nesper, Jutta ^b   Abel, Sören ^b   Jenal, Urs ^b   Viollier, Patrick H ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; MUCR1 PROTEIN; MUCR2 PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; BETA GALACTOSIDASE; REPRESSOR PROTEIN;

ANCESTRY; BACTERIUM; GENE EXPRESSION; HOMEOSTASIS; PROTEIN; VIRULENCE; ZINC;

AGROBACTERIUM; AMINO ACID SUBSTITUTION; ANTIBODY PRODUCTION; ARTICLE; AUTOREGULATION; BACTERIAL CELL; BACTERIAL VIRULENCE; BINDING SITE; BRUCELLA; CAULOBACTER CRESCENTUS; CONTROLLED STUDY; ESCHERICHIA COLI; G1 PHASE CELL CYCLE CHECKPOINT; GENETIC TRANSCRIPTION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; SINORHIZOBIUM; SYMBIOSIS; TRANSPOSON; BIOLOGICAL MODEL; CAULOBACTER; CELL CYCLE G1 PHASE; CHROMATIN IMMUNOPRECIPITATION; DIMERIZATION; DNA SEQUENCE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; S PHASE CELL CYCLE CHECKPOINT; SPECIES DIFFERENCE;

BACTERIAL PROTEINS; BASE SEQUENCE; BETA-GALACTOSIDASE; CAULOBACTER; CHROMATIN IMMUNOPRECIPITATION; DIMERIZATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; G1 PHASE; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOBLOTTING; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; S PHASE CELL CYCLE CHECKPOINTS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 84902772915     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5081     Document Type: Article

References (52)

1. Laub, M. T., Shapiro, L. & McAdams, H. H. Systems biology of Caulobacter. Annu. Rev. Genet. 41, 429-441 (2007).
2. Murray, S. M., Panis, G., Fumeaux, C., Viollier, P. H. & Howard, M. Computational and genetic reduction of a cell cycle to its simplest, primordial components. PLoS Biol. 11, e1001749 (2013).
3. Hallez, R., Bellefontaine, A. F., Letesson, J. J. & De Bolle, X. Morphological and functional asymmetry in alpha-proteobacteria. Trends Microbiol. 12, 361-365 (2004).
4. Kahng, L. S. & Shapiro, L. The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J. Bacteriol. 183, 3065-3075 (2001). (Pubitemid 32433523)
5. De Nisco, N. J., Abo, R. P., Wu, C. M., Penterman, J. & Walker, G. C. Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti. Proc. Natl Acad. Sci. USA 111, 3217-3224 (2014).
6. Brilli, M. et al. The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst. Biol. 4, 52 (2010).
7. Rockey, D. D. & Matsumoto, A. inThe chlamydial developmental cycle. (eds Brun, Y V. & Shimkets, L J.) 403-425 (Prokaryotic development ASM Press, 1999).
8. Christen, M. et al. Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328, 1295-1297 (2010).
9. Santi, I., Dhar, N., Bousbaine, D., Wakamoto, Y. & McKinney, J. D. Single-cell dynamics of the chromosome replication and cell division cycles in mycobacteria. Nat. Commun. 4, 2470 (2013).
10. Evinger, M. & Agabian, N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J. Bacteriol. 132, 294-301 (1977). (Pubitemid 8194548)
11. Skerker, J. M. & Shapiro, L. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J. 19, 3223-3234 (2000). (Pubitemid 30428201)
12. Quon, K. C., Marczynski, G. T. & Shapiro, L. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84, 83-93 (1996). (Pubitemid 26031463)
13. Tsokos, C. G. & Laub, M. T. Polarity and cell fate asymmetry in Caulobacter crescentus. Curr. Opin. Microbiol. 15, 744-750 (2012).
14. Wu, J. & Newton, A. Regulation of the Caulobacter flagellar gene hierarchy; not just for motility. Mol. Microbiol. 24, 233-239 (1997). (Pubitemid 27223854)
15. Chen, J. C. et al. Cytokinesis signals truncation of the PodJ polarity factor by a cell cycle-regulated protease. EMBO J. 25, 377-386 (2006). (Pubitemid 43152858)
16. McGrath, P. T. et al. High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat. Biotechnol. 25, 584-592 (2007). (Pubitemid 46838746)
17. Tan, M. H., Kozdon, J. B., Shen, X., Shapiro, L. & McAdams, H. H. An essential transcription factor, SciP, enhances robustness of Caulobacter cell cycle regulation. Proc. Natl Acad. Sci. USA 107, 18985-18990 (2010).
18. Gora, K. G. et al. A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus. Mol. Cell 39, 455-467 (2010).
19. Gora, K. G. et al. Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus. Mol. Microbiol. 87, 1277-1289 (2013).
20. Klug, A. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79, 213-231 (2010).
21. Gray, M. W., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476-1481 (1999).
22. McGrath, P. T., Iniesta, A. A., Ryan, K. R., Shapiro, L. & McAdams, H. H. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124, 535-547 (2006). (Pubitemid 43199439)
23. Lee, J. S., Son, B., Viswanathan, P., Luethy, P. M. & Kroos, L. Combinatorial regulation of fmgD by MrpC2 and FruA during Myxococcus xanthus development. J. Bacteriol. 193, 1681-1689 (2011).
24. Malgieri, G. et al. The prokaryotic Cys2His2 zinc-finger adopts a novel fold as revealed by the NMR structure of Agrobacterium tumefaciens Ros DNA-binding domain. Proc. Natl Acad. Sci. USA 104, 17341-17346 (2007). (Pubitemid 350219844)
25. Mirabella, A. et al. Brucella melitensis MucR, an orthologue of Sinorhizobium meliloti MucR, is involved in resistance to oxidative, detergent, and saline stresses and cell envelope modifications. J. Bacteriol. 195, 453-465 (2013).
26. Kado, C. I. Negative transcriptional regulation of virulence and oncogenes of the Ti plasmid by Ros bearing a conserved C2H2-zinc finger motif. Plasmid 48, 179-185 (2002). (Pubitemid 36034659)
27. Bahlawane, C., McIntosh, M., Krol, E. & Becker, A. Sinorhizobium meliloti regulator MucR couples exopolysaccharide synthesis and motility. Mol. Plant Microbe Interact. 21, 1498-1509 (2008).
28. Doyon, Y. et al. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat. Methods 8, 74-79 (2011).
29. Fiebig, A. et al. A cell cycle and nutritional checkpoint controlling bacterial surface adhesion. PLoS Genet. 10, e1004101 (2014).
30. Marks, M. E. et al. The genetic basis of laboratory adaptation in Caulobacter crescentus. J. Bacteriol. 192, 3678-3688 (2010).
31. D'Souza, J. M., Wang, L. & Reeves, P. Sequence of the Escherichia coli O26 O antigen gene cluster and identification of O26 specific genes. Gene 297, 123-127 (2002). (Pubitemid 35217787)
32. Bahlawane, C., Baumgarth, B., Serrania, J., Ruberg, S. & Becker, A. Fine-tuning of galactoglucan biosynthesis in Sinorhizobium meliloti by differential WggR (ExpG)-, PhoB-, and MucR-dependent regulation of two promoters. J Bacteriol 190, 3456-3466 (2008).
33. Radhakrishnan, S. K., Pritchard, S. & Viollier, P. H. Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev. Cell 18, 90-101 (2010).
34. Llewellyn, M., Dutton, R. J., Easter, J., O'Donnol, D. & Gober, J. W. The conserved flaF gene has a critical role in coupling flagellin translation and assembly in Caulobacter crescentus. Mol. Microbiol. 57, 1127-1142 (2005). (Pubitemid 41139871)
35. Ardissone, S. & Viollier, P. H. Developmental and environmental regulatory pathways in alpha-proteobacteria. Front. Biosci. 17, 1695-1714 (2012).
36. Schmeisser, C. et al. Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl. Environ. Microbiol. 75, 4035-4045 (2009).
37. Simon, R., Priefer, U. & Puhler, A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1, 784-790 (1983).
38. Ely, B. Genetics of Caulobacter crescentus. Methods Enzymol. 204, 372-384 (1991).
39. Chen, J. C., Viollier, P. H. & Shapiro, L. A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant. Mol. Microbiol. 55, 1085-1103 (2005). (Pubitemid 40299179)
40. Viollier, P. H. & Shapiro, L. A lytic transglycosylase homologue, PleA, is required for the assembly of pili and the flagellum at the Caulobacter crescentus cell pole. Mol. Microbiol. 49, 331-345 (2003). (Pubitemid 36851191)
41. Suh, S. J., Silo-Suh, L. A. & Ohman, D. E. Development of tools for the genetic manipulation of Pseudomonas aeruginosa. J. Microbiol. Methods 58, 203-212 (2004). (Pubitemid 38952698)
42. Aldridge, P., Paul, R., Goymer, P., Rainey, P. & Jenal, U. Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol. 47, 1695-1708 (2003). (Pubitemid 36363349)
43. Wang, S. P., Sharma, P. L., Schoenlein, P. V. & Ely, B. A histidine protein kinase is involved in polar organelle development in Caulobacter crescentus. Proc. Natl Acad. Sci. USA 90, 630-634 (1993). (Pubitemid 23028917)
44. Domian, I. J., Quon, K. C. & Shapiro, L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 415-424 (1997). (Pubitemid 27347232)
45. Jacobs, C., Ausmees, N., Cordwell, S. J., Shapiro, L. & Laub, M. T. Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol. Microbiol. 47, 1279-1290 (2003). (Pubitemid 36307851)
46. Viollier, P. H. et al. From The Cover: Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl Acad. Sci. USA 101, 9257-9262 (2004). (Pubitemid 38812862)
47. Radhakrishnan, S. K., Thanbichler, M. & Viollier, P. H. The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev. 22, 212-225 (2008).
48. Davis, N. J. & Viollier, P. H. Probing flagellar promoter occupancy in wild-type and mutant Caulobacter crescentus by chromatin immunoprecipitation. FEMS Microbiol. Lett. 319, 146-152 (2011).
49. Viollier, P. H., Sternheim, N. & Shapiro, L. A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J. 21, 4420-4428 (2002). (Pubitemid 34984329)
50. Mohr, C. D., Jenal, U. & Shapiro, L. Flagellar assembly in Caulobacter crescentus: a basal body P-ring null mutation affects stability of the L-ring protein. J. Bacteriol. 178, 675-682 (1996). (Pubitemid 26036637)
51. Figge, R. M., Divakaruni, A. V. & MreB, Gober JW. the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51, 1321-1332 (2004).
52. Hahnenberger, K. M. & Shapiro, L. Identification of a gene cluster involved in flagellar basal body biogenesis in Caulobacter crescentus. J. Mol. Biol. 194, 91-103 (1987).