Myxococcus xanthus developmental cell fate production: Heterogeneous accumulation of developmental Regulatory proteins and reexamination of the role of MazF in developmental lysis

Journal of Bacteriology

Volumn 194, Issue 12, 2012, Pages 3058-3068

  Lee, Bongsoo ^a,c   Holkenbrink, Carina ^a   Treuner Lange, Anke ^a,b   Higgs, Penelope I ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MAZF ENDORIBONUCLEASE; REGULATOR PROTEIN; RIBONUCLEASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL SPORE; BACTERIAL STRAIN; BACTERIUM PILUS; CELL AGGREGATION; CELL DIFFERENTIATION; CELL FATE; CELL FRACTIONATION; CELL HETEROGENEITY; CELL SEPARATION; CYTOLYSIS; FRUITING BODY; GENE DELETION; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BACTERIOLYSIS; DNA-BINDING PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MYXOCOCCUS XANTHUS;

MYXOCOCCUS XANTHUS; PILA;

EID: 84864020098     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06756-11     Document Type: Article

References (68)

1. Berleman JE, Chumley T, Cheung P, Kirby JR. 2006. Rippling is a predatory behavior in Myxococcus xanthus. J. Bacteriol. 188:5888 -5895.
2. Berleman JE, et al. 2011. FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS One 6:e23920. doi:10.1371/journal.pone.0023920.
3. Bhandari P, Gowrishankar J. 1997. An Escherichia coli host strain useful for efficient overproduction of cloned gene products with NaCl as the inducer. J. Bacteriol. 179:4403- 4406.
4. Black WP, Xu Q, Yang Z. 2006. Type IV pili function upstream of the Dif chemotaxis pathway in Myxococcus xanthus EPS regulation. Mol. Microbiol. 61:447- 456.
5. Black WP, Yang Z. 2004. Myxococcus xanthus chemotaxis homologs DifD and DifG negatively regulate fibril polysaccharide production. J. Bacteriol. 186:1001-1008.
6. Blackhart BD, Zusman DR. 1985. " Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc. Natl. Acad. Sci. U. S. A. 82:8767- 8770.
7. Boysen A, Ellehauge E, Julien B, Sogaard-Andersen L. 2002. The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J. Bacteriol. 184:1540 -1546.
8. Bulyha I, et al. 2009. Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol. Microbiol. 74:691-706.
9. Campos JM, Zusman DR. 1975. Regulation of development in Myxococcus xanthus: effect of 3=:5=-cyclic AMP, ADP, and nutrition. Proc. Natl. Acad. Sci. U. S. A. 72:518 -522.
10. Curtis PD, Atwood J, 3rd, Orlando R, Shimkets LJ. 2007. Proteins associated with the Myxococcus xanthus extracellular matrix. J. Bacteriol. 189:7634 -7642.
11. Dworkin M. 1962. Nutritional requirements for vegetative growth of Myxococcus xanthus. J. Bacteriol. 84:250 -257.
12. Ellehauge E, Norregaard-Madsen M, Sogaard-Andersen L. 1998. The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol. Microbiol. 30:807- 817.
13. Higgs PI, Jagadeesan S, Mann P, Zusman DR. 2008. EspA, an orphan hybrid histidine protein kinase, regulates the timing of expression of key developmental proteins of Myxococcus xanthus. J. Bacteriol. 190:4416- 4426.
14. Janssen GR, Dworkin M. 1985. Cell-cell interactions in developmental lysis of Myxococcus xanthus. Dev. Biol. 112:194 -202.
15. Jelsbak L, Sogaard-Andersen L. 2000. Pattern formation: fruiting body morphogenesis in Myxococcus xanthus. Curr. Opin. Microbiol. 3:637- 642.
16. Julien B, Kaiser AD, Garza A. 2000. Spatial control of cell differentiation in Myxococcus xanthus. Proc. Natl. Acad. Sci. U. S. A. 97:9098 -9103.
17. Kim Y, et al. 2010. Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD. Environ. Microbiol. 12:1105-1121.
18. Kroos L. 2007. The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu. Rev. Genet. 41:13-39.
19. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
20. Lee B, et al. 2011. The Myxococcus xanthus spore cuticula protein C is a fragment of FibA, an extracellular metalloprotease produced exclusively in aggregated cells. PLoS One 6:e28968. doi:10.1371/journal.pone.0028968.
21. Lee B, Schramm A, Jagadeesan S, Higgs PI. 2010. Two-component systems and regulation of developmental progression in Myxococcus xanthus. Methods Enzymol. 471:253-278.
22. Lee JS, Son B, Viswanathan P, Luethy PM, Kroos L. 2011. Combinatorial regulation of fmgD by MrpC2 and FruA during Myxococcus xanthus development. J. Bacteriol. 193:1681-1689.
23. Li Y, et al. 2003. Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc. Natl. Acad. Sci. U. S. A. 100:5443-5448.
24. Lobedanz S, Sogaard-Andersen L. 2003. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev. 17:2151-2161.
25. Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K. 2011. Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U. S. A. 108:13206 -13211.
26. Makarova KS, Wolf YI, Koonin EV. 2009. Comprehensive comparativegenomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4:19. doi:10.1186/ 1745-6150-4-19.
27. Maniatis T, Fritsch EF, Sambrook J. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Mauriello EM, Astling DP, Sliusarenko O, Zusman DR. 2009. Localization of a bacterial cytoplasmic receptor is dynamic and changes with cellcell contacts. Proc. Natl. Acad. Sci. U. S. A. 106:4852- 4857.
29. McBride MJ, Kohler T, Zusman DR. 1992. Methylation of FrzCD, a methyl-accepting taxis protein of Myxococcus xanthus, is correlated with factors affecting cell behavior. J. Bacteriol. 174:4246-4257.
30. McBride MJ, Zusman DR. 1993. FrzCD, a methyl-accepting taxis protein from Myxococcus xanthus, shows modulated methylation during fruiting body formation. J. Bacteriol. 175:4936-4940.
31. McCleary WR, Esmon B, Zusman DR. 1991. Myxococcus xanthus protein C is a major spore surface protein. J. Bacteriol. 173:2141-2145.
32. McCleary WR, McBride MJ, Zusman DR. 1990. Developmental sensory transduction in Myxococcus xanthus involves methylation and demethylation of FrzCD. J. Bacteriol. 172:4877- 4887.
33. Mittal S, Kroos L. 2009. A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc. Natl. Acad. Sci. U. S. A. 106:1965-1970.
34. Mittal S, Kroos L. 2009. Combinatorial regulation by a novel arrangement of FruA and MrpC2 transcription factors during Myxococcus xanthus development. J. Bacteriol. 191:2753-2763.
35. Müller FD, Treuner-Lange A, Heider J, Huntley SM, Higgs PI. 2010. Global transcriptome analysis of spore formation in Myxococcus xanthus reveals a locus necessary for cell differentiation. BMC Genomics 11:264. doi:10.1186/1471-2164-11-264.
36. Nariya H, Inouye M. 2008. MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132:55- 66.
37. Nariya H, Inouye S. 2005. Identification of a protein Ser/Thr kinase cascade that regulates essential transcriptional activators in Myxococcus xanthus development. Mol. Microbiol. 58:367-379.
38. Nariya H, Inouye S. 2006. A protein Ser/Thr kinase cascade negatively regulates the DNA-binding activity of MrpC, a smaller form of which may be necessary for the Myxococcus xanthus development. Mol. Microbiol. 60:1205-1217.
39. O'Connor KA, Zusman DR. 1991. Analysis of Myxococcus xanthus cell types by two-dimensional polyacrylamide gel electrophoresis. J. Bacteriol. 173:3334 -3341.
40. O'Connor KA, Zusman DR. 1991. Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J. Bacteriol. 173:3342-3355.
41. O'Connor KA, Zusman DR. 1991. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol. 173:3318 -3333.
42. O'Connor KA, Zusman DR. 1988. Reexamination of the role of autolysis in the development of Myxococcus xanthus. J. Bacteriol. 170:4103- 4112.
43. Ogawa M, Fujitani S, Mao X, Inouye S, Komano T. 1996. FruA, a putative transcription factor essential for the development of Myxococcus xanthus. Mol. Microbiol. 22:757-767.
44. Pedersen K, Christensen SK, Gerdes K. 2002. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol. 45:501-510.
45. Ramage HR, Connolly LE, Cox JS. 2009. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet. 5:e1000767. doi:10.1371/journal.pgen.1000767.
46. Rolbetzki A, Ammon M, Jakovljevic V, Konovalova A, Sogaard-Andersen L. 2008. Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Dev. Cell 15:627- 634.
47. Rosenberg E, Keller KH, Dworkin M. 1977. Cell density-dependent growth of Myxococcus xanthus on casein. J. Bacteriol. 129:770 -777.
48. Rosenbluh A, Nir R, Sahar E, Rosenberg E. 1989. Cell-densitydependent lysis and sporulation of Myxococcus xanthus in agarose microbeads. J. Bacteriol. 171:4923- 4929.
49. Rudd K, Zusman DR. 1979. Rifampin-resistant mutants of Myxococcus xanthus defective in development. J. Bacteriol. 137:295-300.
50. Schagger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368 -379.
51. Shi W, Ngok FK, Zusman DR. 1996. Cell density regulates cellular reversal frequency in Myxococcus xanthus. Proc. Natl. Acad. Sci. U. S. A. 93:4142- 4146.
52. Sliusarenko O, Zusman DR, Oster G. 2007. Aggregation during fruiting body formation in Myxococcus xanthus is driven by reducing cell movement. J. Bacteriol. 189:611- 619.
53. Sogaard-Andersen L. 2004. Cell polarity, intercellular signalling and mor-phogenetic cell movements in Myxococcus xanthus. Curr. Opin. Microbiol. 7:587-593.
54. Sogaard-Andersen L, Kaiser D. 1996. C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. Proc. Natl. Acad. Sci. U. S. A. 93:2675-2679.
55. Son B, Liu Y, Kroos L. 2011. Combinatorial regulation by MrpC2 and FruA involves three sites in the fmgE promoter region during Myxococcus xanthus development. J. Bacteriol. 193:2756 -2766.
56. Sun H, Shi W. 2001. Analyses of mrp genes during Myxococcus xanthus development. J. Bacteriol. 183:6733- 6739.
57. Sun H, Shi W. 2001. Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J. Bacteriol. 183:4786-4795.
58. Syed MA, et al. 2011. The chromosomal mazEF locus of Streptococcus mutans encodes a functional type II toxin-antitoxin addiction system. J. Bacteriol. 193:1122-1130.
59. Thony-Meyer L, Kaiser D. 1993. devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J. Bacteriol. 175:7450 -7462.
60. Ueki T, Inouye S. 2003. Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. Proc. Natl. Acad. Sci. U. S. A. 100:8782- 8787.
61. Ueki T, Inouye S, Inouye M. 1996. Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183:153-157.
62. Viswanathan P, Ueki T, Inouye S, Kroos L. 2007. Combinatorial regulation of genes essential for Myxococcus xanthus development involves a response regulator and a LysR-type regulator. Proc. Natl. Acad. Sci. U. S. A. 104:7969 -7974.
63. Wall D, Kolenbrander PE, Kaiser D. 1999. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J. Bacteriol. 181:24 -33.
64. Wireman JW, Dworkin M. 1977. Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J. Bacteriol. 129: 798-802.
65. Wu SS, Kaiser D. 1997. Regulation of expression of the pilA gene in Myxococcus xanthus. J. Bacteriol. 179:7748 -7758.
66. Wu SS, Wu J, Kaiser D. 1997. The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol. Microbiol. 23:109 -121.
67. Yang Z, Lux R, Hu W, Hu C, Shi W. 2010. PilA localization affects extracellular polysaccharide production and fruiting body formation in Myxococcus xanthus. Mol. Microbiol. 76:1500 -1513.
68. Zusman DR, Scott AE, Yang Z, Kirby JR. 2007. Chemosensory pathways, motility and development in Myxococcus xanthus. Nat. Rev. Microbiol. 5:862- 872.