Publikationsserver der Universitätsbibliothek Marburg
Titel:Regulation of secretion of the signalling protease PopC in Myxococcus xanthus
Autor:Konovalova, Anna
Weitere Beteiligte: Søgaard-Andersen, Lotte (Prof.)
Veröffentlicht:2011
URI:https://archiv.ub.uni-marburg.de/diss/z2011/0074
URN: urn:nbn:de:hebis:04-z2011-00745
DOI: https://doi.org/10.17192/z2011.0074
DDC:500 Naturwissenschaften
Titel (trans.):Regulation der Sekretion der signalling Protease PopC in Myxococcus xanthus
Publikationsdatum:2011-03-17
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Signal, Bacteria, Bakterien, Myxococcus xanthus, Signaling, Protease, Development, Secretion, Protease, Entwicklung, Sekretion

Summary:
In response to starvation Myxococcus xanthus initiates a developmental program that culminates in fruiting body formation. Completion of this developmental program depends on cell-cellcommunication involving at least two intercellular signals, the A-signal and the C-signal. The contact-dependent intercellular C-signal function to induce and coordinate the two morphogenetic events in fruiting body formation, aggregation and sporulation, temporally and spatially coordinated. The intercellular C-signal is a 17 kDa protein (p17), which is generated by proteolytic cleavage of the full-length 25 kDa csgA protein (p25), and is essential for fruiting body formation. p25 and PopC, the protease that cleaves p25, accumulate in the outer membrane and cytoplasm, respectively in vegetative cells. PopC is specifically secreted during starvation. Therefore, restriction of p25 cleavage to starving cells depends on a compartmentalization mechanism that involves the regulated secretion of PopC in response to starvation. In this report, the main focus is on understanding the mechanism underlying regulated secretion of the PopC protease. We first focused on the identification of proteins required for PopC secretion. PopC lacks a signal peptide and is secreted in an unprocessed form. We report that two incomplete type III secretion systems, a type VI secretion system and type I secretion systems are not involved in PopC secretion. From a collection of mutants generated by random transposon mutagenesis and unable to complete fruiting body formation, we identified seven mutants unable to secrete PopC. None of the insertions were in genes coding for known secretion systems. The mutations were divided into three classes based on the insertion sites. The class I mutation was in a gene cluster largely encoding proteins of unknown function, predicted to localize to the cell envelope, and with a narrow phylogenetic distribution except for a D,D-carboxypeptidase and two Ser/Thr kinases. The class II mutations were in two clusters encoding paralogous proteins of unknown function predicted to localize to the cytoplasm. Several of the class II genes are phylogenetically widely distributed and frequently present in gene clusters linked to genes encoding secretion systems. We speculate that the class I mutation affect a novel type of secretion system involved in PopC secretion and that the class II mutations either affect proteins with accessory or regulatory functions in PopC secretion. Next, we focused on elucidating the molecular mechanism underlying the activation of PopC secretion in response to starvation. Our data demonstrate that PopC secretion is controlled at the post-translational level by a regulatory cascade involving the RelA and PopD proteins. Specifically, RelA is required for activation of PopC secretion in response to starvation and PopD, which is encoded in an operon with PopC, interacts directly with PopC and acts as an inhibitor of PopC secretion. On the basis of genetic and biochemical data we suggest that PopC and PopD form a cytoplasmic complex that blocks PopC secretion in the presence of nutrients. In response to starvation, RelA is activated resulting in induction of the stringent response. Activated RelA by an unknown mechanism induces the proteolytic degradation of PopD in the PopC/PopD complex in that way releasing PopC for secretion. On the basis of these data, we suggest that the generation of p17 depends on a two-step proteolytic cascade involving degradation of PopD and, subsequently, the specific cleavage of p25 by PopC. The current model for intercellular A-signaling in M. xanthus proposes that starvation induces the release of extracellular A-signal proteases. These proteases are thought to cleave surface-exposed proteins and extracellular proteins thereby generating the A-signal amino acids and peptides, which serve to measure the density of starving cells early during development. DNA microarray analyses (S. Wegener-Feldbrügge, unpubl.) previously suggested that the primary defect in the asgA and asgB mutants, which are unable to generate the A-signal, is not a reduced capacity in protein secretion but a reduced expression of genes encoding secreted proteases including popC. Here, genetic analyses demonstrated that restored expression of popCD rescues development of asgA and asgB mutants without restoring A-signaling. Thus, ectopic expression of popCD leads to a bypass of the requirement for the A-signal during development. We suggest that the inability of asgA and asgB mutants to undergo development is the result of at least two defects: (i) reduced expression of the genes encoding the A-signal proteases; and, (ii) reduced expression of the popC gene.

Bibliographie / References

  1. Remenant, B., B. Coupat-Goutaland, A. Guidot, G. Cellier, E. Wicker, C. Allen, M. Fegan, O. Pruvost, M. Elbaz, A. Calteau, G. Salvignol, D. Mornico, S. Mangenot, V. Barbe, C. Medigue & P. Prior, (2010) Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics11: 379.
  2. Laemmli, U. K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227: 680-685.
  3. Krogh, A., B. Larsson, G. von Heijne & E. L. Sonnhammer, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol305: 567-580.
  4. Bendtsen, J. D., H. Nielsen, G. von Heijne & S. Brunak, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol340: 783-795.
  5. Finn, R. D., J. Mistry, J. Tate, P. Coggill, A. Heger, J. E. Pollington, O. L. Gavin, P. Gunasekaran, G. Ceric, K. Forslund, L. Holm, E. L. Sonnhammer, S. R. Eddy & A. Bateman, (2010) The Pfam protein families database. Nucleic Acids Res38: D211-222.
  6. Jeong, H., J. H. Yim, C. Lee, S.-H. Choi, Y. K. Park, S. H. Yoon, C.-G. Hur, H.- Y. Kang, D. Kim, H. H. Lee, K. H. Park, S.-H. Park, H.-S. Park, H. K. Lee, T. K. Oh & J. F. Kim, (2005) Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucl. Acids Res.33: 7066– 7073.
  7. Rosario, C. J. & M. Singer, (2007) The Myxococcus xanthus developmental program can be delayed by inhibition of DNA replication. J. Bacteriol.189: 8793-8800.
  8. Berleman, J. E. & J. R. Kirby, (2007a) Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions. J. Bacteriol.189: 5675-5682.
  9. Artsimovitch, I., V. Patlan, S. Sekine, M. N. Vassylyeva, T. Hosaka, K. Ochi, S. Yokoyama & D. G. Vassylyev, (2004) Structural basis for transcription regulation by alarmone ppGpp. Cell117: 299-310.
  10. Berks, B. C., T. Palmer & F. Sargent, (2003) The Tat protein translocation pathway and its role in microbial physiology. Adv Microb Physiol47: 187- 254.
  11. Fronzes, R., E. Schafer, L. Wang, H. R. Saibil, E. V. Orlova & G. Waksman, (2009) Structure of a type IV secretion system core complex. Science323: 266-268.
  12. Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, (1990) Basic local alignment search tool. J Mol Biol215: 403-410.
  13. Deane, J. E., P. Abrusci, S. Johnson & S. M. Lea, (2010) Timing is everything: the regulation of type III secretion. Cell Mol Life Sci67: 1065-1075.
  14. Filloux, A., (2004) The underlying mechanisms of type II protein secretion. BBA1694: 163-179.
  15. Nariya, H. & M. Inouye, (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell132: 55-66.
  16. Kahnt, J., K. Aguiluz, J. Koch, A. Treuner-Lange, A. Konovalova, S. Huntley, M. Hoppert, L. Søgaard-Andersen & R. Hedderich, (2010) Profiling the outer membrane proteome during growth and development of the social bacterium Myxococcus xanthus by selective biotinylation and analyses of outer membrane vesicles. J. Proteome Res. 9: 5197-5208.
  17. Bowden, M. G. & H. B. Kaplan, (1998) The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol.30: 275-284.
  18. Ellehauge, E., M. Norregaard-Madsen & L. Sogaard-Andersen, (1998) The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol Microbiol30: 807-817.
  19. Garza, A. G., B. Z. Harris, J. S. Pollack & M. Singer, (2000b) The asgE locus is required for cell-cell signalling during Myxococcus xanthus development. Mol Microbiol35: 812-824.
  20. Pilhofer, M., A. P. Bauer, M. Schrallhammer, L. Richter, W. Ludwig, K. H. Schleifer & G. Petroni, (2007) Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel Two-Step Gene Walking method. Nucleic Acids Res35: e135.
  21. Letunic, I., T. Doerks & P. Bork, (2009) SMART 6: recent updates and new developments. Nucleic Acids Res37: D229-232.
  22. Rawlings, N. D., A. J. Barrett & A. Bateman, (2010) MEROPS: the peptidase database. Nucleic Acids Res38: D227-233.
  23. Peabody, C. R., Y. J. Chung, M.-R. Yen, D. Vidal-Ingigliardi, A. P. Pugsley & M. H. Saier Jr., (2003) Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology149: 3051-3072.
  24. Harris, B. Z., D. Kaiser & M. Singer, (1998) The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes & Dev.12: 1022-1035.
  25. Li, S., B.-U. Lee & L. J. Shimkets, (1992) csgA expression entrains Myxococcus xanthus development. Genes Dev.6: 401-410.
  26. Sager, B. & D. Kaiser, (1994) Intercellular C-signaling and the traveling waves of Myxococcus. Genes Dev.8: 2793-2804.
  27. Garza, A. G., B. Z. Harris, B. M. Greenberg & M. Singer, (2000a) Control of asgE expression during growth and development of Myxococcus xanthus. J. Bacteriol.182: 6622-6629.
  28. Feldman, M. F. & G. R. Cornelis, (2003) The multitalented type III chaperones: all you can do with 15 kDa. FEMS MICROBIOL LETT219: 151-158.
  29. Pallen, M. J., S. A. Beatson & C. M. Bailey, (2005) Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol Rev29: 201-229.
  30. Kaplan, H. B. & L. Plamann, (1996) A Myxococcus xanthus cell density-sensing system required for multicellular development. FEMS Microbiol. Letters139: 89-95.
  31. Konovalova, A., T. Petters & L. Sogaard-Andersen, (2010a) Extracellular biology of Myxococcus xanthus. FEMS Microbiol Rev34: 89-106.
  32. Yu, X. J., K. McGourty, M. Liu, K. E. Unsworth & D. W. Holden, (2010) pH sensing by intracellular Salmonella induces effector translocation. Science328: 1040-1043.
  33. Gomis-Ruth, F. X. & M. Coll, (2006) Cut and move: protein machinery for DNA processing in bacterial conjugation. Curr Opin Struct Biol16: 744-752.
  34. Tojo, N., S. Inouye & T. Komano, (1993a) Cloning and nucleotide sequence of the Myxococcus xanthus lon gene: indispensability of lon for vegetative growth. J Bacteriol175: 2271-2277.
  35. Shi, X., S. Wegener-Feldbrugge, S. Huntley, N. Hamann, R. Hedderich & L. Sogaard-Andersen, (2008) Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J Bacteriol190: 613-624.
  36. Young, J. & I. B. Holland, (1999) ABC transporters: bacterial exporters-revisited five years on. BBA1461: 177-200.
  37. Kroos, L., A. Kuspa & D. Kaiser, (1986) A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev. Biol.117: 252-266.
  38. Kroos, L., P. Hartzell, K. Stephens & D. Kaiser, (1988) A link between cell movement and gene expression argues that motility is required for cell- cell signaling during fruiting body development. Genes Dev.2: 1677- 1685.
  39. Davis, J. M., J. Mayor & L. Plamann, (1995) A missense mutation in rpoD results in an A-signalling defect in Myxococcus xanthus. J. Bacteriol.18: 943-952.
  40. Caetano-Anolles, G., (1993) Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl3: 85-94.
  41. Wang, R. C., S. J. Seror, M. Blight, J. M. Pratt, J. K. Broome-Smith & I. B. Holland, (1991) Analysis of the membrane organization of an Escherichia coli protein translocator, HlyB, a member of a large family of prokaryote and eukaryote surface transport proteins. J Mol Biol217: 441-454.
  42. Zhang, Y., F. Buchholz, J. P. Muyrers & A. F. Stewart, (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet.20: 123-128.
  43. Das, S., J. C. Noe, S. Paik & T. Kitten, (2005) An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites. J Microbiol Methods63: 89-94.
  44. Sisto, A., M. Cipriani, M. Morea, S. Lonigro, F. Valerio & P. Lavermicocca, (2010) An Rhs-like genetic element is involved in bacteriocin production by Pseudomonas savastanoi pv. savastano. Antonie Van Leeuwenhoek: 1-13.
  45. Rosenberg, E. & M. Varon, (1984) Antibiotics and lytic enzymes. In: Myxobacteria: Development and cell interactions. E. Rosenberg (ed).
  46. Kuroda, A., (2006) A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci Biotechnol Biochem70: 325-331.
  47. Kuspa, A., L. Plamann & D. Kaiser, (1992b) A-signalling and the cell density requirement for Myxococcus xanthus development. J. Bacteriol.174: 7360-7369.
  48. Kaimer, C. & P. Graumann, (2010) Bacillus subtilis CinA is a stationary phase– induced protein that localizes to the nucleoid and plays a minor role in competent cells. Arch. Microbiol.192: 549-557.
  49. Pallen, M., R. Chaudhuri & A. Khan, (2002) Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol.10: 556-563.
  50. Gottschalk, G., (1986) Bacterial metabolism. Springer Verlag, New York.
  51. O'Connor, K. A. & D. R. Zusman, (1991a) Behaviour of peripheral rods and their role in the life cycle of Myxococcus xanthus. J. Bacteriol.173: 3342-3355.
  52. Tse, H. & R. E. Gill, (2002) Bypass of A-and B-signaling requirements for Myxococcus xanthus development by mutations in spdR. J. Bacteriol.184: 1455-1457.
  53. Kim, S. K. & D. Kaiser, (1990b) Cell alignment required in differentiation of Myxococcus xanthus. Science249: 926-928.
  54. Rosenbluh, A., R. Nir, E. Sahar & E. Rosenberg, (1989) Cell-density-dependent lysis and sporulation of Myxococcus xanthus in agarose beads. J. Bacteriol.171: 4923-4929.
  55. Kim, S. K. & D. Kaiser, (1990c) Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus. Genes & Dev.4: 896-904.
  56. Kim, S. K. & D. Kaiser, (1990a) C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell61: 19-26.
  57. Akeda, Y. & J. E. Galan, (2005) Chaperone release and unfolding of substrates in type III secretion. Nature437: 911-915.
  58. Page, A. L. & C. Parsot, (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol46: 1-11.
  59. Konovalova, A., S. O. Shylin & P. V. Rokytko, (2007) Characteristics of carotenoids of methylotrophic bacteria of Methylobacterium genus.Mikrobiol Z69: 35-41 (in Ukranian)
  60. W. Hancock, S. Lory & M. V. Olson, (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature406: 959-964.
  61. Moraleda-Munoz, A., J. Perez, A. L. Extremera & J. Munoz-Dorado, (2010) Complexity of the Myxococcus xanthus copper response: differential regulation of six heavy metal efflux systems. Appl. Environ. Microbiol.76: 6069-6076.
  62. Striebel, F., W. Kress & E. Weber-Ban, (2009) Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukaryotes. Curr Opin Struct Biol19: 209-217.
  63. Huang, W., J. Jia, P. Edwards, K. Dehesh, G. Schneider & Y. Lindqvist, (1998) Crystal structure of β-ketoacyl-acyl carrier protein synthase II from E.coli reveals the molecular architecture of condensing enzymes. EMBO J.17: 1183-1191.
  64. Koronakis, V., A. Sharff, E. Koronakis, B. Luisi & C. Hughes, (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature405: 914-919.
  65. Kruse, T., S. Lobedanz, N. M. S. Berthelsen & L. Søgaard-Andersen, (2001) C- signal: A cell surface-associated morphogen that induces and coordinates multicellular fruiting body morphogenesis and sporulation in M. xanthus. Mol. Microbiol.40: 156-168.
  66. Curriculum Vitae Personal data Name Anna Konovalova Date of birth 17 July 1984
  67. Maurizi, M. R. & F. Rasulova, (2002) Degradation of L-glutamate dehydrogenase from Escherichia coli: allosteric regulation of enzyme stability. Arch Biochem Biophys397: 206-216.
  68. Langille, M. G. I., W. W. L. Hsiao & F. S. L. Brinkman, (2010) Detecting genomic islands using bioinformatics approaches. Nat. Rev. Micro.8: 373-382.
  69. O'Connor, K. A. & D. R. Zusman, (1991b) Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J. Bacteriol.173: 3318-3333.
  70. Boyer, F., G. Fichant, J. Berthod, Y. Vandenbrouck & I. Attree, (2009) Dissecting the bacterial type VI secretion system by a genome wide in 7. References 120 silico analysis: what can be learned from available microbial genomic resources? BMC Genomics10: 104.
  71. Zheng, J. & K. Y. Leung, (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol66: 1192-1206.
  72. Ireton, K. & A. D. Grossman, (1994) DNA-related conditions controlling the initiation of sporulation in Bacillus subtilis. Cell. Mol. Biol. Res.40: 193- 198.
  73. Hillesland, K. L., R. E. Lenski & G. J. Velicer, (2007) Ecological variables affecting predatory success in Myxococcus xanthus. Microb Ecol53: 571- 578.
  74. Singer, M. & D. Kaiser, (1995) Ectopic production of guanosine penta-and teraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes Dev.9: 1633-1644.
  75. Plamann, L., J. M. Davis, B. Cantwell & J. Mayor, (1994) Evidence that asgB encodes a DNA-binding protein essential for growth and development of Myxococcus xanthus. J. Bacteriol.176: 2013-2020.
  76. Kroos, L. & D. Kaiser, (1987a) Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes & Dev.1: 840-854.
  77. Shi, W. & D. R. Zusman, (1993) Fatal attraction. Nature366: 414-415.
  78. Ogawa, M., S. Fujitani, X. Mao, S. Inouye & T. Komano, (1996) FruA, a putative transcription factor essential for the development of Myxococus xanthus. Mol. Microbiol.22: 757-767.
  79. Kuspa, A. & D. Kaiser, (1989) Genes required for developmental signalling in Myxococcus xanthus: three asg loci. J. Bacteriol.171: 2762-2772.
  80. Dunmire, V., L. D. Tatar & L. Plamann, (1999) Genetic suppression analysis of an asgA missense mutation in Myxococcus xanthus. Microbiology145 ( Pt 6): 1299-1306.
  81. Goodner, B., G. Hinkle, S. Gattung, N. Miller, M. Blanchard, B. Qurollo, B. S. Goldman, Y. Cao, M. Askenazi, C. Halling, L. Mullin, K. Houmiel, J. Gordon, M. Vaudin, O. Iartchouk, A. Epp, F. Liu, C. Wollam, M. Allinger, D. Doughty, C. Scott, C. Lappas, B. Markelz, C. Flanagan, C. Crowell, J. Gurson, C. Lomo, C. Sear, G. Strub, C. Cielo & S. Slater, (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science294: 2323-2328.
  82. Clausen, M., V. Jakovljevic, L. Søgaard-Andersen & B. Maier, (2009) High force generation is a conserved property of type IV pilus systems. J. Bacteriol.: In press.
  83. Guo, D., Y. Wu & H. B. Kaplan, (2000) Identification and characterization of genes required for early Myxococcus xanthus developmental gene expression. J Bacteriol182: 4564-4571.
  84. Lobedanz, S. & L. Søgaard-Andersen, (2003) Identification of the C-signal, a contact dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev.17: 2151-2161.
  85. Diodati, M. E., R. E. Gill, L. Plamann & H. B. Kaplan, (2008) Initiation and early developmental events. In: Myxobacteria: Multicellularity and differentiation. D. E. Whitworth (ed). Washington, D.C.: ASM Press, pp. 43-76.
  86. Kuspa, A., L. Kroos & D. Kaiser, (1986) Intercellular signaling is required for developmental gene expression in Myxococcus xanthus. Dev. Biol.117: 267-276.
  87. Goldberg, A. L. & A. C. St John, (1976) Intracellular protein degradation in mammalian and bacterial cells: Part 2. Annu Rev Biochem45: 747-803.
  88. Orlowski, M. & D. White, (1974) Intracellular proteolytic activity in developing myxospores of Myxococcus xanthus. Arch Microbiol97: 347-357.
  89. Spratt, B. G., P. J. Hedge, S. te Heesen, A. Edelman & J. K. Broome-Smith, (1986) Kanamycin-resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. Gene41: 337-342.
  90. Hill, C. W., (1999) Large genomic sequence repetitions in bacteria: lessons from rRNA operons and Rhs elements. Res. Microbiol.150: 665-674.
  91. Wai, S. N., M. Westermark, J. Oscarsson, Y. Mizunoe & B. E. Uhlin, (2000) Localization and export of the ClyA cytotoxin in Escherichia coli. Med. Microbiol. Immunol.189: 51-.
  92. Koraimann, G., (2003) Lytic transglycosylases in macromolecular transport systems of Gram-negative bacteria. Cell. Mol. Life Sci.60: 2371-2388.
  93. Masure, H. R., B. J. Pearce, H. Shio & B. Spellerberg, (1998) Membrane targeting of RecA during genetic transformation. Mol Microbiol27: 845- 852.
  94. Kimura, Y., H. Saiga, H. Hamanaka & H. Matoba, (2006) Myxococcus xanthus twin-arginine translocation system is important for growth and development. Arch. Microbiol.184: 387-396.
  95. Wilharm, G., S. Dittmann, A. Schmid & J. Heesemann, (2007) On the role of specific chaperones, the specific ATPase, and the proton motive force in type III secretion. Int J Med Microbiol297: 27-36.
  96. Welch, R. & D. Kaiser, (2001) Pattern formation and traveling waves in myxobacteria: Experimental demonstration. Proc. Natl. Acad. Sci. USA98: 14907-14912.
  97. Murphy, K. C., K. G. Campellone & A. R. Poteete, (2000) PCR-mediated gene replacement in Escherichia coli. Gene246: 321-330.
  98. Gust, B., G. L. Challis, K. Fowler, T. Kieser & K. F. Chater, (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA100: 1541-1546.
  99. Place of birth Kamyanets-Podilskiy, Ukraine Education 10/2007-10/2010 PhD (Dr. rer. nat.) Philipps-University Marburg Max-Planck-Institute for Terrestrial Microbiology, Marburg, Germany Supervisor: Prof. MD, PhD Lotte Søgaard-Andersen PhD thesis: Regulation of secretion of the signalling protease PopC in Myxococcus xanthus 09/2005-06/2007 Master in Biology Specialization: Microbiology and Virology Taras Shevchenko National University of Kyiv, Kyiv, Ukraine Faculty of Biology, Department of Microbiology and General Immunology Master thesis: Expression of recombinant p24 protein of bovine leukaemia virus in Escherichia coli Supervisor: Dr. Natalia Grabchenko, JSC " Diaproph Med " 09/2001-06/2005 Bachelor in Biology Specialization: Microbiology Taras Shevchenko National University of Kyiv Kyiv, Ukraine Faculty of Biology, Department of Microbiology and General Immunology Bachelor thesis: Characterization of carotenoid pigments of Methylobacterium Supervisor: Dr. Pavlo Rokitko, Institute of Microbiology and Virology, National Academy of Sciences of Ukraine 09/1991-06/2001 High school certificate Gymnasium, Kamyanets-Podilskiy, Ukraine List of publications Konovalova, A., S. Wegener-Feldbrügge, S. Lindow, N. Hamann & L. Søgaard-Andersen, (2010) Proteins of unknown function are required for regulated secretion of the signalling protease PopC in Myxococcus xanthus. Submitted.
  100. Ghosh, A. S., C. Chowdhury & D. E. Nelson, (2008) Physiological functions of D-alanine carboxypeptidases in Escherichia coli. Trends Microbiol.16: 309-317.
  101. Jakovljevic, V., S. Leonardy, M. Hoppert & L. Søgaard-Andersen, (2008) PilB and PilT are ATPases acting antagonistically in type IV pili function in Myxococcus xanthus. J. Bacteriol.190: 2411-2421.
  102. Nudleman, E., D. Wall & D. Kaiser, (2006) Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol. Microbiol.60: 16-29.
  103. Bendtsen, J. D., H. Nielsen, D. Widdick, T. Palmer & S. Brunak, (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics6: 167.
  104. Galan, J. E. & H. Wolf-Watz, (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature444: 567-573.
  105. Andersen, C., C. Hughes & V. Koronakis, (2001) Protein export and drug efflux through bacterial channel-tunnels Curr. Opin. Cell Biol.4: 412-416.
  106. Inouye, S., H. Nariya & J. Munoz-Dorado, (2008) Protein Ser/Thr kinases and phosphatases in Myxococcus xanthus. In: Myxobacteria: Multicellularity and differentiation. D. E. Whitworth (ed). Washington, D.C.: ASM Press, pp. 191-210.
  107. Konovalova, A., S. Wegener-Feldbrügge, S. Lindow, N. Hamann & L. Søgaard- Andersen, (2010b) Proteins of unknown function are required for regulated secretion of the PopC protease in Myxococcus xanthus. In preparation.
  108. Plamann, L., A. Kuspa & D. Kaiser, (1992) Proteins that rescue A-signal- defective mutants of Myxococcus xanthus. J. Bacteriol.174: 3311-3318.
  109. Driessen, A. J. & N. Nouwen, (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem77: 643-667.
  110. Rolbetzki, A., M. Ammon, V. Jakovljevic, A. Konovalova & L. Søgaard- Andersen, (2008) Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Dev. Cell15: 627-634.
  111. Straley, S. C., G. V. Plano, E. Skrzypek, P. L. Haddix & K. A. Fields, (1993) Regulation by Ca2+ in the Yersinia low-Ca2+ response. Mol Microbiol8: 1005-1010.
  112. Slominska, M., P. Neubauer & G. Wegrzyn, (1999) Regulation of bacteriophage lambda development by guanosine 5'-diphosphate-3'-diphosphate. Virology262: 431-441.
  113. Reichenbach, H., (1965) Rhythmische vorgänge bei der Schwarmenfaltung von Myxobakterien. Ber. Deutsch. Bot. Ges.78: 102-105.
  114. Kuroda, A., K. Nomura, R. Ohtomo, J. Kato, T. Ikeda, N. Takiguchi, H. Ohtake & A. Kornberg, (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science293: 705-708.
  115. Gros, (2004) Structure of the translocator domain of a bacterial autotransporter. Embo J23: 1257-1266.
  116. Kaplan, H. B., A. Kuspa & D. Kaiser, (1991) Suppressors that permit A-signal- independent developmental gene expression in Myxococcus xanthus. J. Bacteriol.173: 1460-1470.
  117. Hagen, D. C., A. P. Bretscher & D. Kaiser, (1978) Synergism between morphogenetic mutants of Myxococcus xanthus. Dev. Biol.64: 284-296.
  118. Konovalova, A., Y. Kobozyev, N. Grabchenko & I. Ganova, (2008) Synthesis of recombinant analogue of p24 protein of BLV.Biotechnology1 (in Ukranian)
  119. Pallen, M. J., M. S. Francis & K. Futterer, (2003) Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators. FEMS Microbiol. Lett. 223: 53-60.
  120. Filloux, A., A. Hachani & S. Bleves, (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology154: 1570-1583.
  121. Reichenbach, H., (1999) The ecology of the myxobacteria. Env. Microbiol.1: 15- 21.
  122. Tojo, N., S. Inouye & T. Komano, (1993b) The lonD gene is homologous to the lon gene encoding an ATP-dependent protease and is essential for the development of Myxococcus xanthus. J Bacteriol175: 4545-4549.
  123. Plamann, L., Y. Li, B. Cantwell & J. Mayor, (1995) The Myxococcus xanthus asgA gene encodes a novel signal transduction protein required for multicellular development. J. Bacteriol.177: 2014-2020.
  124. Guo, D., M. G. Bowden, R. Pershad & H. B. Kaplan, (1996) The Myxococcus xanthus rfbABC operon encodes an ATP-binding cassette transporter homolog required for O-antigen biosynthesis and multicellular development. J Bacteriol178: 1631-1639.
  125. Overgaard, M., S. Wegener-Feldbrugge & L. Sogaard-Andersen, (2006) The orphan response regulator DigR is required for synthesis of extracellular matrix fibrils in Myxococcus xanthus. J Bacteriol188: 4384-4394.
  126. Cashel, M., D. R. Gentry, V. J. Hernandez & D. Vinella, (1996) The stringent response. In: Escherichia coli and Salmonella: cellular and molecular biology. F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter & H. E. Umbarger (eds). Washington, DC: ASM Press, pp. 1458–1496.
  127. Cornelis, G. R., (2006) The type III secretion injectisome. Nat Rev Micro4: 811- 825.
  128. Cascales, E. & P. J. Christie, (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol1: 137-149.
  129. Mougous, J. D., C. A. Gifford, T. L. Ramsdell & J. J. Mekalanos, (2007b) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol.9: 797-803.
  130. Bönemann, G., A. Pietrosiuk & A. Mogk, (2010) Tubules and donuts: a type VI secretion story. Mol Microbiol76: 815-821.
  131. Jacob-Dubuisson, F., C. Locht & R. Antoine, (2001) Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol40: 306-313.
  132. Desvaux, M., N. J. Parham & I. R. Henderson, (2004) Type V protein secretion: simplicity gone awry? Curr Issues Mol Biol6: 111-124.
  133. Wai, S. N., B. Lindmark, T. Soderblom, A. Takade, M. Westermark, J. Oscarsson, J. Jass, A. Richter-Dahlfors, Y. Mizunoe & B. E. Uhlin, (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell115: 25-35.
  134. Schwarz, S., R. D. Hood & J. D. Mougous, (2010) What is type VI secretion doing in all those bugs? Trends Microbiol18: 531-537.
  135. Cho, K. & D. R. Zusman, (1999) AsgD, a new two-component regulator required for A-signalling and nutrient sensing during early development of Myxococcus xanthus. Mol. Microbiol.34: 268-281.
  136. Hager, A. J., D. L. Bolton, M. R. Pelletier, M. J. Brittnacher, L. A. Gallagher, R. Kaul, S. J. Skerrett, S. I. Miller & T. Guina, (2006) Type IV pili-mediated secretion modulates Francisella virulence. Mol. Microbiol.62: 227-237.
  137. Emanuelsson, O., S. Brunak, G. von Heijne & H. Nielsen, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc2: 953-971.
  138. Lueders, T., R. Kindler, A. Miltner, M. W. Friedrich & M. Kaestner, (2006) Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl Environ Microbiol72: 5342-5348.
  139. Bingle, L. E., C. M. Bailey & M. J. Pallen, (2008) Type VI secretion: a beginner's guide. Curr. Opin. Microbiol.11: 3-8.
  140. Jackson, A., G. Thomas, J. Parkhill & N. Thomson, (2009) Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics10: 584.
  141. McNulty, C., J. Thompson, B. Barrett, L. Lord, C. Andersen & I. S. Roberts, (2006) The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol. Microbiol.59: 907-922.
  142. Wang, Y.-D., S. Zhao & C. W. Hill, (1998) Rhs elements comprise three subfamilies which diverged prior to acquisition by Escherichia coli. J. Bacteriol.180: 4102-4110.
  143. Xu, D., C. Yang & H. B. Kaplan, (1998) Myxococcus xanthus sasN encodes a regulator that prevents developmental gene expression during growth. J. Bacteriol.180: 6215-6223.
  144. Zhang, H., N. N. Rao, T. Shiba & A. Kornberg, (2005) Inorganic polyphosphate in the social life of Myxococcus xanthus: motility, development, and predation. Proc Natl Acad Sci U S A102: 13416-13420.
  145. Krall, L., U. Wiedemann, G. Unsin, S. Weiss, N. Domke & C. Baron, (2002) Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A99: 11405-11410.
  146. Kearns, D. B., P. J. Bonner, D. R. Smith & L. J. Shimkets, (2002) An extracellular matrix-associated zinc metalloprotease is required for dilauroyl phosphatidylethanolamine chemotactic excitation in Myxococcus xanthus. J Bacteriol184: 1678-1684.
  147. Sliusarenko, O., J. Neu, D. R. Zusman & G. Oster, (2006) Accordion waves in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA103: 1534-1539.
  148. Sambrook, J. & D. W. Russell, (2001) Molecular cloning : a laboratory manual.Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
  149. Berleman, J. E., T. Chumley, P. Cheung & J. R. Kirby, (2006) Rippling is a predatory behavior in Myxococcus xanthus. J. Bacteriol.188: 5888-5895.
  150. Roggenkamp, A., N. Ackermann, C. A. Jacobi, K. Truelzsch, H. Hoffmann & J. Heesemann, (2003) Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol185: 3735-3744.
  151. Eisen, C. M. Ronning, W. B. Barbazuk, M. Blanchard, C. Field, C. Halling, G. Hinkle, O. Iartchuk, H. S. Kim, C. Mackenzie, R. Madupu, N. Miller, A. Shvartsbeyn, S. A. Sullivan, M. Vaudin, R. Wiegand & H. B. Kaplan, (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc. Natl. Acad Sci. USA103: 15200-15205.
  152. Julien, B., A. D. Kaiser & A. Garza, (2000) Spatial control of cell differentiation in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA97: 9098-9103.
  153. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins & J. D. Thompson, (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res31: 3497-3500.
  154. Meiser, P., H. B. Bode & R. Müller, (2006) The unique DKxanthene secondary metabolite family from the myxobacterium Myxococcus xanthus is required for developmental sporulation. Proc. Natl. Acad Sci. USA12: 19128-19133.
  155. Wu, S. & D. Kaiser, (1997) Regulation of expression of the pilA gene in Myxococcus xanthus. J. Bacteriol.179: 7748-7758.
  156. Yang, C. & H. B. Kaplan, (1997) Myxococcus xanthus sasS encodes a sensor histidine kinase required for early developmental gene expression. J Bacteriol179: 7759-7767.
  157. Datsenko, K. A. & B. L. Wanner, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA97: 6640-6645.
  158. Pukatzki, S., A. T. Ma, A. T. Revel, D. Sturtevant & J. J. Mekalanos, (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A104: 15508-15513.
  159. Gill, R. E., M. Karlok & D. Benton, (1993) Myxococcus xanthus encodes an ATP-dependent protease which is required for developmental gene transcription and intercellular signaling. J. Bacteriol.175: 4538-4544.
  160. Kuspa, A., L. Plamann & D. Kaiser, (1992a) Identification of heat-stable A-factor from Myxococcus xanthus. J. Bacteriol.174: 3319-3326.
  161. Downard, J., S. V. Ramaswamy & K. S. Kil, (1993) Identification of esg, a genetic locus involved in cell-cell signaling during Myxococcus xanthus development. J. Bacteriol.175: 7762-7770.
  162. Kim, S. K. & D. Kaiser, (1991) C-factor has distinct aggregation and sporulation thresholds during Myxococcus development. J. Bacteriol.173: 1722- 1728.
  163. Shimkets, L. J. & H. Rafiee, (1990) CsgA, an extracellular protein essential for Myxococcus xanthus development. J. Bacteriol.172: 5299-5306.
  164. Morrison, C. E. & D. R. Zusman, (1979) Myxococcus xanthus mutants with temperature-sensitive, stage-specific defects: Evidence for independent pathways in development. J. Bacteriol.140: 1036-1042.
  165. Kuner, J. M. & D. Kaiser, (1982) Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus. J. Bacteriol.151: 458-461.
  166. Shimkets, L. J. & D. Kaiser, (1982) Induction of coordinated movement of Myxococcus xanthus cells. J. Bacteriol.152: 451-461.
  167. Wu, H.-Y., P.-C. Chung, H.-W. Shih, S.-R. Wen & E.-M. Lai, (2008) Secretome analysis uncovers an Hcp-family protein secreted via a Type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol.190: 2841-2850.
  168. Juncker, A. S., H. Willenbrock, G. Von Heijne, S. Brunak, H. Nielsen & A. Krogh, (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci12: 1652-1662.
  169. Brutinel, E. D. & T. L. Yahr, (2008) Control of gene expression by type III secretory activity. Curr Opin Microbiol11: 128-133.
  170. Dworkin, M., (1996) Recent advances in the social and developmental biology of the Myxobacteria. Microbiol. Rev.60: 70-102.
  171. Cascales, E., (2008) The type VI secretion toolkit. EMBO Rep.9: 735-741.
  172. Bönemann, G., A. Pietrosiuk, A. Diemand, H. Zentgraf & A. Mogk, (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. Embo J28: 315-325.
  173. Tseng, T. T., B. M. Tyler & J. C. Setubal, (2009) Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol9 Suppl 1: S2.
  174. Bulyha, I., C. Schmidt, P. Lenz, V. Jakovljevic, A. Höne, B. Maier, M. Hoppert & L. Søgaard-Andersen, (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol. Microbiol. 74: 691–706.
  175. Alvarez-Martinez, C. E. & P. J. Christie, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev73: 775-808.
  176. Chandran, V., R. Fronzes, S. Duquerroy, N. Cronin, J. Navaza & G. Waksman, (2009) Structure of the outer membrane complex of a type IV secretion system. Nature462: 1011-1015.
  177. Joachimiak & J. J. Mekalanos, (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science312: 1526- 1530.
  178. Rhodes & K. Nakayama, (2010) A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc. Natl. Acad Sci. USA107: 276-281.
  179. Barker, J. R., A. Chong, T. D. Wehrly, J. J. Yu, S. A. Rodriguez, J. Liu, J. Celli, B. P. Arulanandam & K. E. Klose, (2009) The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol. Microbiol.74: 1459-1470.
  180. Hood, R. D., P. Singh, F. Hsu, T. Guvener, M. A. Carl, R. R. Trinidad, J. M. Silverman, B. B. Ohlson, K. G. Hicks, R. L. Plemel, M. Li, S. Schwarz, W. Y. Wang, A. J. Merz, D. R. Goodlett & J. D. Mougous, (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe7: 25-37.
  181. Spreter, T., C. K. Yip, S. Sanowar, I. Andre, T. G. Kimbrough, M. Vuckovic, R. A. Pfuetzner, W. Deng, A. C. Yu, B. B. Finlay, D. Baker, S. I. Miller & N. C. Strynadka, (2009) A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat Struct Mol Biol16: 468-476.
  182. Jani, A. J. & P. A. Cotter, (2010) Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe8: 2-6.
  183. Masi, M. & C. Wandersman, (2010) Multiple signals direct the assembly and function of a type 1 secretion system. J. Bacteriol.192: 3861-3869.
  184. Cunningham, K. & W. Wickner, (1989) Specific recognition of the leader region of precursor proteins is required for the activation of translocation ATPase of Escherichia coli. Proc Natl Acad Sci U S A86: 8630-8634.
  185. Planet, P. J., S. C. Kachlany, R. DeSalle & D. H. Figurski, (2001) Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA98: 2503-2508.
  186. McDermott, J. E., A. Corrigan, E. Peterson, C. Oehmen, G. Niemann, E. D. Cambronne, D. Sharp, J. N. Adkins, R. Samudrala & F. Heffron, (2010) Computational prediction of type III and IV secreted effectors in Gram- negative bacteria. Infect Immun.
  187. Economou, A., P. J. Christie, R. C. Fernandez, T. Palmer, G. V. Plano & A. P. Pugsley, (2006) Secretion by numbers: Protein traffic in prokaryotes. Mol. Microbiol.62: 308-319.
  188. Shimkets, L. J., R. E. Gill & D. Kaiser, (1983) Developmental cell interactions in Myxococcus xanthus and the spoC locus. Proc. Natl. Acad. Sci. USA80: 1406-1410.
  189. Henrichsen, J., (1972) Bacterial surface translocation: a survey and a classification. Bacteriol. Reviews36: 478-503.
  190. Kaiser, D., (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA76: 5952-5956.
  191. Hodgkin, J. & D. Kaiser, (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc. Natl. Acad. Sci. USA74: 2938- 2942.
  192. Kim, S. K. & D. Kaiser, (1990d) Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc. Natl. Acad. Sci. USA87: 3635-3639.
  193. Driessen, A. J., (1992) Precursor protein translocation by the Escherichia coli translocase is directed by the protonmotive force. Embo J11: 847-853.
  194. Nasu, H., T. Iida, T. Sugahara, Y. Yamaichi, K.-S. Park, K. Yokoyama, K. Makino, H. Shinagawa & T. Honda, (2000) A filamentous phage associated with recent pandemic Vibrio parahaemolyticus O3:K6 strains. J. Clin. Microbiol.38: 2156-2161.

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