Publikationsserver der Universitätsbibliothek Marburg

Titel:Signal Transduction Systems in the Myxococcus xanthus Developmental Program
Autor:Glaser, Maike
Weitere Beteiligte: Higgs, Penelope (PhD)
Veröffentlicht:2017
URI:https://archiv.ub.uni-marburg.de/diss/z2018/0041
DOI: https://doi.org/10.17192/z2018.0041
URN: urn:nbn:de:hebis:04-z2018-00413
DDC: Biowissenschaften, Biologie
Titel (trans.):Signal-Transduktions-Systeme im Entwicklungszyklus von Myxococcus xanthus
Publikationsdatum:2018-08-08
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Myxococcus xanthus, signal transduction, Signaltransduktion

Summary:
Myxococcus xanthus serves as a prokaryotic model organism for the regulation of complex social behaviors. During all aspects of its life cycle M. xanthus favors multicellular behavior, including a developmental program in which the population is segregated into at least three distinct cell fates (sporulation inside multicellular fruiting bodies, peripheral rods and cell lysis). Neither the evolutionary advantage of producing these distinct cell fates, nor the mechanism by which cell fate segregating is induced are fully understood. However, MrpC, a major developmental trans-criptional regulator, is a good candidate for the regulation of cell fate segregation. MrpC accumulation is controlled by multiple distinct signaling systems including the (orphan) histidine protein kinases (HPKs) Esp, TodK, Red and Hpk30. A strain lacking three of the pathways (Δesp Δred ΔtodK) massively over-accumulates MrpC and displays a striking phenotype in which all cells appear to sporulate inappropriately rapidly, producing lawns of spores. In this thesis research, I first report how M. xanthus benefits from production of spores inside of fruiting bodies. I next address how fruiting body formation and cell fate segregation can be controlled. To do so, I characterized the mechanisms by which Red, TodK and Hpk30 could control MrpC accumulation. We have previously observed that a strain lacking Esp, Red and TodK signaling systems is deficient in the formation of organized fruiting bodies and essentially produces lawns of spores. By taking advantage of this mutant strain, I addressed the role of cell fate segregation in dispersal and environmental resistance of M. xanthus fruiting bodies. I showed that loss of fruiting body morphology leads to enhanced dispersal by the vector Drosophila melanogaster. However, this comes at the expense of environmental resistance as could be demonstrated by the impact of UV exposure on mutant and wild type fruiting bodies as well as wild type single spores. To clarify how signaling systems may converge to regulate MrpC accumulation, I confirmed a putative connection between the Red signaling system and the Ser/Thr kinase cascade thought to control MrpC activity by phosphorylation. To start to identify possible mechanisms by which TodK and Hpk30 could affect MrpC accumulation, I carried out a detailed characterization of their respective signal flows. TodK functions as a bifunctional histidine protein kinase/phosphatase, whose activity is likely modulated by the two N-terminal PAS-domains. Hpk30 characterization revealed kinase activity as the signal output and that this activity is modulated by its two receiver domains as well as a hypothetical protein, MXAN_4466. Together, these data suggest a model in which separate signaling systems converge to regulate MrpC accumulation in distinct cell types leading to segregation of cells into either peripheral rods outside or spores inside fruiting bodies. Altering the spatial and/or temporal accumulation of MrpC within cells in the developing population is used to adapt fruiting body morphology to specific environmental conditions in which either dispersal or long-term resistance might enhance M. xanthus survival.

Bibliographie / References

  1. Bhardwaj, V., (2013) Characterization of the role of MrpC in Myxococcus xanthus developmental cell fate determination. In: Max-Planck-Institut für Terrestrische Mikrobiologie. Philipps-Universität Marburg, http://dx.doi.org/10.17192/z2013.0387.
  2. Thony-Meyer, L. and Kaiser, D., (1993) devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J Bacteriol 175: 7450-7462.
  3. Burchard, R.P. and Dworkin, M., (1966) A bacteriophage for Myxococcus xanthus: isolation, characterization and relation of infectivity to host morphogenesis. J Bacteriol 91: 1305-1313.
  4. Porter, S.L., Roberts, M.A., Manning, C.S. and Armitage, J.P., (2008b) A bifunctional kinase-phosphatase in bacterial chemotaxis. Proc Natl Acad Sci U S A 105: 18531-18536.
  5. Munoz-Dorado, J., Higgs, P.I. and Elias-Arnanz, M., (2014) Abundance and Complexity of Signalling Mechanisms in Myxobacteria. In: Myxobacteria: Genomics, Cellular and Molecular Biology. Yang, Z. and Higgs, P.I. (eds).
  6. Burger, L. and van Nimwegen, E., (2008) Accurate prediction of protein-protein interactions from sequence alignments using a Bayesian method. Mol Syst Biol 4: 165.
  7. Mann, T.H., Seth Childers, W., Blair, J.A., Eckart, M.R. and Shapiro, L., (2016) A cell cycle kinase with tandem sensory PAS domains integrates cell fate cues. Nat Commun 7: 11454.
  8. Galperin, M.Y., (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35.
  9. Barak, R., Welch, M., Yanovsky, A., Oosawa, K. and Eisenbach, M., (1992) Acetyladenylate or its derivative acetylates the chemotaxis protein CheY in vitro and increases its activity at the flagellar switch. Biochemistry 31: 10099- 10107.
  10. Roman, S.J., Meyers, M., Volz, K. and Matsumura, P., (1992) A chemotactic signaling surface on CheY defined by suppressors of flagellar switch mutations. J Bacteriol 174: 6247-6255.
  11. Mittal, S. and Kroos, L., (2009b) 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.
  12. Garre, S., Senevirathne, C. and Pflum, M.K., (2014) A comparative study of ATP analogs for phosphorylation-dependent kinase-substrate crosslinking. Bioorg Med Chem 22: 1620-1625.
  13. Nariya, H. and Inouye, S., (2002) Activation of 6-phosphofructokinase via phosphorylation by Pkn4, a protein Ser/Thr kinase of Myxococcus xanthus. Mol Microbiol 46: 1353-1366.
  14. Wilke, K.E., Francis, S. and Carlson, E.E., (2012) Activity-based probe for histidine kinase signaling. J Am Chem Soc 134: 9150-9153.
  15. Moglich, A., Ayers, R.A. and Moffat, K., (2010) Addition at the molecular level: signal integration in designed Per-ARNT-Sim receptor proteins. J Mol Biol 400: 477- 486.
  16. Munoz-Dorado, J., Inouye, S. and Inouye, M., (1991) A gene encoding a protein serine/threonine kinase is required for normal development of M. xanthus, a gram-negative bacterium. Cell 67: 995-1006.
  17. Inouye, S., Jain, R., Ueki, T., Nariya, H., Xu, C.Y., Hsu, M.Y., Fernandez-Luque, B.A., Munoz-Dorado, J., Farez-Vidal, E. and Inouye, M., (2000) A large family of eukaryotic-like protein Ser/Thr kinases of Myxococcus xanthus, a developmental bacterium. Microb Comp Genomics 5: 103-120.
  18. Paul, R., Jaeger, T., Abel, S., Wiederkehr, I., Folcher, M., Biondi, E.G., Laub, M.T. and Jenal, U., (2008) Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell 133: 452-461.
  19. Tan, C.H., Lee, K.W., Burmolle, M., Kjelleberg, S. and Rice, S.A., (2017) All together now: experimental multispecies biofilm model systems. Environ Microbiol 19: 42-53.
  20. Moore, J.B., Shiau, S.P. and Reitzer, L.J., (1993) Alterations of highly conserved residues in the regulatory domain of nitrogen regulator I (NtrC) of Escherichia coli. J Bacteriol 175: 2692-2701.
  21. Sun, H. and Shi, W., (2001a) Analyses of mrp genes during Myxococcus xanthus development. J Bacteriol 183: 6733-6739.
  22. Hu, W., Lux, R. and Shi, W., (2013) Analysis of exopolysaccharides in Myxococcus xanthus using confocal laser scanning microscopy. Methods Mol Biol 966: 121-131.
  23. O'Connor, K.A. and Zusman, D.R., (1991b) Analysis of Myxococcus xanthus cell types by two-dimensional polyacrylamide gel electrophoresis. J Bacteriol 173: 3334-3341.
  24. Romeralo, M., Skiba, A., Gonzalez-Voyer, A., Schilde, C., Lawal, H., Kedziora, S., Cavender, J.C., Glockner, G., Urushihara, H. and Schaap, P., (2013) Analysis of phenotypic evolution in Dictyostelia highlights developmental plasticity as a likely consequence of colonial multicellularity. Proc Biol Sci 280: 20130976.
  25. Shi, X., (2008) An analysis of two-component regulatory systems in Myxococcus xanthus. In: Max-Planck-Institut für terrestrische Mikrobiologie. Philipps- Universität Marburg.
  26. Nariya, H. and Inouye, S., (2003) An effective sporulation of Myxococcus xanthus requires glycogen consumption via Pkn4-activated 6-phosphofructokinase.
  27. Bhandari, P. and 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.
  28. Jagadeesan, S., Mann, P., Schink, C.W. and Higgs, P.I., (2009) A novel "four- component" two-component signal transduction mechanism regulates developmental progression in Myxococcus xanthus. J Biol Chem 284: 21435- 21445.
  29. Canova, M.J., Baronian, G., Brelle, S., Cohen-Gonsaud, M., Bischoff, M. and Molle, V., (2014) A novel mode of regulation of the Staphylococcus aureus Vancomycin-resistance-associated response regulator VraR mediated by Stk1 protein phosphorylation. Biochem Biophys Res Commun 447: 165-171.
  30. Moon, K. and Gottesman, S., (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314- 1330.
  31. Nariya, H. and 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.
  32. Childers, W.S. and Shapiro, L., (2014) A pseudokinase couples signaling pathways to enable asymmetric cell division in a bacterium. Microb Cell 2: 29-32.
  33. Birnboim, H.C. and Doly, J., (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513-1523.
  34. Smith, J.G., Latiolais, J.A., Guanga, G.P., Pennington, J.D., Silversmith, R.E. and Bourret, R.B., (2004) A search for amino acid substitutions that universally activate response regulators. Mol Microbiol 51: 887-901.
  35. Allen, J.J., Li, M., Brinkworth, C.S., Paulson, J.L., Wang, D., Hubner, A., Chou, W.H., Davis, R.J., Burlingame, A.L., Messing, R.O., Katayama, C.D., Hedrick, S.M. and Shokat, K.M., (2007) A semisynthetic epitope for kinase substrates. Nat Methods 4: 511-516.
  36. Christen, M., Kulasekara, H.D., Christen, B., Kulasekara, B.R., Hoffman, L.R. and Miller, S.I., (2010) Asymmetrical distribution of the second messenger c-di- GMP upon bacterial cell division. Science 328: 1295-1297.
  37. Szurmant, H., Bunn, M.W., Cannistraro, V.J. and Ordal, G.W., (2003) Bacillus subtilis hydrolyzes CheY-P at the location of its action, the flagellar switch. J Biol Chem 278: 48611-48616.
  38. Koch, M.K., McHugh, C.A. and Hoiczyk, E., (2011) BacM, an N-terminally processed bactofilin of Myxococcus xanthus, is crucial for proper cell shape. Mol Microbiol 80: 1031-1051.
  39. Shapiro, J.A., (1988) Bacteria as Multicellular Organisms. Scientific American 258: 82-89.
  40. Pallen, M., Chaudhuri, R. and Khan, A., (2002) Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 10: 556- 563.
  41. Gajdiss, M., Turck, M. and Bierbaum, G., (2017) Bacterial Histidine Kinases: Overexpression, Purification, and Inhibitor Screen. Methods Mol Biol 1520: 247-259.
  42. Claessen, D., Rozen, D.E., Kuipers, O.P., Sogaard-Andersen, L. and van Wezel, G.P., (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12: 115-124.
  43. O'Connor, K.A. and Zusman, D.R., (1991c) Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J Bacteriol 173: 3342-3355.
  44. Shi, X., Wegener-Feldbrugge, S., Huntley, S., Hamann, N., Hedderich, R. and Sogaard-Andersen, L., (2008) Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J Bacteriol 190: 613-624.
  45. Gao, R. and Stock, A.M., (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63: 133-154.
  46. Dworkin, M., (1966) Biology of the myxobacteria. Annu Rev Microbiol 20: 75-106.
  47. Reichenbach, H., (1993) Biology of the Myxobacteria: Ecology and Taxonomy. In: Myxobacteria II. Dworkin, M. and Kaiser, A.D. (eds). Washington DC: American Society for Microbilology, pp. 13-62.
  48. Senevirathne, C. and Pflum, M.K., (2013) Biotinylated phosphoproteins from kinase- catalyzed biotinylation are stable to phosphatases: implications for phosphoproteomics. Chembiochem 14: 381-387.
  49. Dubnau, D. and Losick, R., (2006) Bistability in bacteria. Mol Microbiol 61: 564-572.
  50. Kaiser, D., (2001) Building a multicellular organism. Annu Rev Genet 35: 103-123.
  51. Tse, H. and Gill, R.E., (2002) Bypass of A-and B-signaling requirements for Myxococcus xanthus development by mutations in spdR. J Bacteriol 184: 1455-1457.
  52. Gonzalez-Pastor, J.E., (2011) Cannibalism: a social behavior in sporulating Bacillus subtilis. FEMS Microbiol Rev 35: 415-424.
  53. Lopez, D., Vlamakis, H., Losick, R. and Kolter, R., (2009a) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74: 609-618.
  54. Skerker, J.M. and Laub, M.T., (2004) Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2: 325-337.
  55. Rosenberg, E., Keller, K.H. and Dworkin, M., (1977) Cell density-dependent growth of Myxococcus xanthus on casein. J Bacteriol 129: 770-777.
  56. Childers, W.S., Xu, Q., Mann, T.H., Mathews, II, Blair, J.A., Deacon, A.M. and Shapiro, L., (2014) Cell fate regulation governed by a repurposed bacterial histidine kinase. PLoS Biol 12: e1001979.
  57. Kim, S.K. and Kaiser, D., (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.
  58. Sogaard-Andersen, L., (2004) Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. Curr Opin Microbiol 7: 587-593.
  59. Kim, S.K. and Kaiser, D., (1990a) C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell 61: 19-26.
  60. Cusick, J.K., Hager, E. and Gill, R.E., (2002) Characterization of bcsA mutations that bypass two distinct signaling requirements for Myxococcus xanthus development. J Bacteriol 184: 5141-5150.
  61. Boynton, T.O., McMurry, J.L. and Shimkets, L.J., (2013) Characterization of Myxococcus xanthus MazF and implications for a new point of regulation. Mol Microbiol 87: 1267-1276.
  62. Hsu, J.L., Chen, H.C., Peng, H.L. and Chang, H.Y., (2008) Characterization of the histidine-containing phosphotransfer protein B-mediated multistep phosphorelay system in Pseudomonas aeruginosa PAO1. J Biol Chem 283: 9933-9944.
  63. Duclos, B., Marcandier, S. and Cozzone, A.J., (1991) Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis. Methods Enzymol 201: 10-21.
  64. Kirby, J.R. and Zusman, D.R., (2003) Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc Natl Acad Sci U S A 100: 2008- 2013.
  65. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
  66. Nakamura, Y., Gojobori, T. and Ikemura, T., (2000) Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 28: 292.
  67. Mittal, S. and Kroos, L., (2009a) Combinatorial regulation by a novel arrangement of FruA and MrpC2 transcription factors during Myxococcus xanthus development. J Bacteriol 191: 2753-2763.
  68. Son, B., Liu, Y. and 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.
  69. Lee, J.S., Son, B., Viswanathan, P., Luethy, P.M. and Kroos, L., (2011b) Combinatorial regulation of fmgD by MrpC2 and FruA during Myxococcus xanthus development. J Bacteriol 193: 1681-1689.
  70. Campbell, A., Viswanathan, P., Barrett, T., Son, B., Saha, S. and Kroos, L., (2015) Combinatorial regulation of the dev operon by MrpC2 and FruA during Myxococcus xanthus development. J Bacteriol 197: 240-251.
  71. Huntley, S., Hamann, N., Wegener-Feldbrugge, S., Treuner-Lange, A., Kube, M., Reinhardt, R., Klages, S., Muller, R., Ronning, C.M., Nierman, W.C. and Sogaard-Andersen, L., (2011) Comparative genomic analysis of fruiting body formation in Myxococcales. Mol Biol Evol 28: 1083-1097.
  72. Huntley, S., Kneip, S., Treuner-Lange, A. and Sogaard-Andersen, L., (2013) Complete genome sequence of Myxococcus stipitatus strain DSM 14675, a fruiting myxobacterium. Genome Announc 1: e0010013.
  73. Huntley, S., Zhang, Y., Treuner-Lange, A., Kneip, S., Sensen, C.W. and Sogaard- Andersen, L., (2012) Complete genome sequence of the fruiting myxobacterium Corallococcus coralloides DSM 2259. J Bacteriol 194: 3012- 3013.
  74. Huynh, T.N., Noriega, C.E. and Stewart, V., (2010) Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. Proc Natl Acad Sci U S A 107: 21140-21145.
  75. Chao, J.D., Papavinasasundaram, K.G., Zheng, X., Chavez-Steenbock, A., Wang, X., Lee, G.Q. and Av-Gay, Y., (2010) Convergence of Ser/Thr and two- component signaling to coordinate expression of the dormancy regulon in Mycobacterium tuberculosis. J Biol Chem 285: 29239-29246.
  76. Rasmussen, A.A., Porter, S.L., Armitage, J.P. and Sogaard-Andersen, L., (2005) Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol Microbiol 56: 1358-1372.
  77. Leonardy, S., Freymark, G., Hebener, S., Ellehauge, E. and Sogaard-Andersen, L., (2007) Coupling of protein localization and cell movements by a dynamically localized response regulator in Myxococcus xanthus. EMBO J 26: 4433-4444.
  78. Blethrow, J.D., Glavy, J.S., Morgan, D.O. and Shokat, K.M., (2008) Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci U S A 105: 1442-1447.
  79. Ninfa, A.J. and Magasanik, B., (1986) Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A 83: 5909-5913.
  80. Madhusudan, Akamine, P., Xuong, N.H. and Taylor, S.S., (2002) Crystal structure of a transition state mimic of the catalytic subunit of cAMP-dependent protein kinase. Nat Struct Biol 9: 273-277.
  81. Ortiz-Lombardia, M., Pompeo, F., Boitel, B. and Alzari, P.M., (2003) Crystal structure of the catalytic domain of the PknB serine/threonine kinase from Mycobacterium tuberculosis. J Biol Chem 278: 13094-13100.
  82. Kornev, A.P. and Taylor, S.S., (2010) Defining the conserved internal architecture of a protein kinase. Biochim Biophys Acta 1804: 440-444.
  83. Hidaka, Y., Park, H. and Inouye, M., (1997) Demonstration of dimer formation of the cytoplasmic domain of a transmembrane osmosensor protein, EnvZ, of Escherichia coli using Ni-histidine tag affinity chromatography. FEBS Lett 400: 238-242.
  84. Moglich, A., Ayers, R.A. and Moffat, K., (2009a) Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385: 1433-1444.
  85. Lux, R., Li, Y., Lu, A. and Shi, W., (2004) Detailed three-dimensional analysis of structural features of Myxococcus xanthus fruiting bodies using confocal laser scanning microscopy. Biofilms 1: 293-303.
  86. Besant, P.G. and Attwood, P.V., (2009) Detection and analysis of protein histidine phosphorylation. Mol Cell Biochem 329: 93-106.
  87. Rhie, H.G. and Shimkets, L.J., (1989) Developmental bypass suppression of Myxococcus xanthus csgA mutations. J Bacteriol 171: 3268-3276.
  88. Wireman, J.W. and Dworkin, M., (1977) Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J Bacteriol 129: 798-802.
  89. O'Connor, K.A. and Zusman, D.R., (1991a) Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J Bacteriol 173: 3318-3333.
  90. Lan, C.Y. and Igo, M.M., (1998) Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J Bacteriol 180: 171-174.
  91. Goodman, A.L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A. and Lory, S., (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249-259.
  92. Gilbert, D.G., (1980) Dispersal of yeasts and bacteria by Drosophila in a temperate forest. Oecologia 46: 135-137.
  93. Szurmant, H. and Ordal, G.W., (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68: 301-319.
  94. Galperin, M.Y., (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13: 150-159.
  95. van Gestel, J., Vlamakis, H. and Kolter, R., (2015) Division of Labor in Biofilms: the Ecology of Cell Differentiation. Microbiol Spectr 3: MB-0002-2014.
  96. Tzeng, L., Ellis, T.N. and Singer, M., (2006) DNA replication during aggregation phase is essential for Myxococcus xanthus development. J Bacteriol 188: 2774- 2779.
  97. Tzeng, L. and Singer, M., (2005) DNA replication during sporulation in Myxococcus xanthus fruiting bodies. Proc Natl Acad Sci U S A 102: 14428-14433.
  98. Inouye, S. and Nariya, H., (2008) Dual regulation with Ser/Thr kinase cascade and a His/Asp TCS in Myxococcus xanthus. Adv Exp Med Biol 631: 111-121.
  99. Horstmann, N., Saldana, M., Sahasrabhojane, P., Yao, H., Su, X., Thompson, E., Koller, A. and Shelburne, S.A., 3rd, (2014) Dual-site phosphorylation of the control of virulence regulator impacts group a streptococcal global gene expression and pathogenesis. PLoS Pathog 10: e1004088.
  100. Chen, Y.E., Tsokos, C.G., Biondi, E.G., Perchuk, B.S. and Laub, M.T., (2009) Dynamics of two Phosphorelays controlling cell cycle progression in Caulobacter crescentus. J Bacteriol 191: 7417-7429.
  101. Singer, M. and Kaiser, D., (1995) Ectopic production of guanosine penta-and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes Dev 9: 1633-1644.
  102. Welch, M., Oosawa, K., Aizawa, S.I. and Eisenbach, M., (1994) Effects of phosphorylation, Mg2+, and conformation of the chemotaxis protein CheY on its binding to the flagellar switch protein FliM. Biochemistry 33: 10470-10476.
  103. Russo, F.D. and Silhavy, T.J., (1991) EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222: 567-580.
  104. Kimura, Y., Mori, Y., Ina, Y. and Takegawa, K., (2011) Enzymatic and functional analysis of a protein phosphatase, Pph3, from Myxococcus xanthus. J Bacteriol 193: 2657-2661.
  105. Higgs, P.I., Jagadeesan, S., Mann, P. and Zusman, D.R., (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.
  106. Lee, B., Higgs, P.I., Zusman, D.R. and Cho, K., (2005) EspC is involved in controlling the timing of development in Myxococcus xanthus. J Bacteriol 187: 5029- 5031.
  107. Pereira, S.F., Goss, L. and Dworkin, J., (2011) Eukaryote-like serine/threonine kinases and phosphatases in bacteria. Microbiol Mol Biol Rev 75: 192-212.
  108. Perez, J., Castaneda-Garcia, A., Jenke-Kodama, H., Muller, R. and Munoz-Dorado, J., (2008) Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc Natl Acad Sci U S A 105: 15950-15955.
  109. Wuichet, K., Cantwell, B.J. and Zhulin, I.B., (2010) Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 13: 219- 225.
  110. Hillesland, K.L., Velicer, G.J. and Lenski, R.E., (2009) Experimental evolution of a microbial predator's ability to find prey. Proc Biol Sci 276: 459-467.
  111. Velicer, G.J. and Stredwick, K.L., (2002) Experimental social evolution with Myxococcus xanthus. Antonie Van Leeuwenhoek 81: 155-164.
  112. Li, Y., Sun, H., Ma, X., Lu, A., Lux, R., Zusman, D. and Shi, W., (2003) Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc Natl Acad Sci U S A 100: 5443-5448.
  113. Shank, E.A. and Kolter, R., (2011) Extracellular signaling and multicellularity in Bacillus subtilis. Curr Opin Microbiol 14: 741-747.
  114. Lopez, D. and Kolter, R., (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34: 134-149.
  115. Nariya, H. and Inouye, S., (2005b) Factors that modulate the Pkn4 kinase cascade in Myxococcus xanthus. J Mol Microbiol Biotechnol 9: 147-153.
  116. Rasmussen, A.A., Wegener-Feldbrugge, S., Porter, S.L., Armitage, J.P. and Sogaard-Andersen, L., (2006) Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol Microbiol 60: 525-534.
  117. Higgs, P.I., Cho, K., Whitworth, D.E., Evans, L.S. and Zusman, D.R., (2005) Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus. J Bacteriol 187: 8191-8195.
  118. Smith, J., Queller, D.C. and Strassmann, J.E., (2014) Fruiting bodies of the social amoeba Dictyostelium discoideum increase spore transport by Drosophila. BMC Evol Biol 14: 105.
  119. Berleman, J.E., Vicente, J.J., Davis, A.E., Jiang, S.Y., Seo, Y.E. and Zusman, D.R., (2011) FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS One 6: e23920.
  120. Jiang, P., Atkinson, M.R., Srisawat, C., Sun, Q. and Ninfa, A.J., (2000) Functional dissection of the dimerization and enzymatic activities of Escherichia coli nitrogen regulator II and their regulation by the PII protein. Biochemistry 39: 13433-13449.
  121. Hsing, W. and Silhavy, T.J., (1997) Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J Bacteriol 179: 3729-3735.
  122. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J., (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
  123. Lopez, D., Vlamakis, H. and Kolter, R., (2009b) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33: 152-163.
  124. Willett, J.W. and Kirby, J.R., (2012) Genetic and biochemical dissection of a HisKA domain identifies residues required exclusively for kinase and phosphatase activities. PLoS Genet 8: e1003084.
  125. Rhodenizer, D., Martin, I., Bhandari, P., Pletcher, S.D. and Grotewiel, M., (2008) Genetic and environmental factors impact age-related impairment of negative geotaxis in Drosophila by altering age-dependent climbing speed. Exp Gerontol 43: 739-748.
  126. Wu, S.S. and Kaiser, D., (1995) Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18: 547-558.
  127. Vos, M. and Velicer, G.J., (2006) Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol 72: 3615- 3625.
  128. Sun, H. and Shi, W., (2001b) Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J Bacteriol 183: 4786- 4795.
  129. Dunmire, V., Tatar, L.D. and Plamann, L., (1999) Genetic suppression analysis of an asgA missense mutation in Myxococcus xanthus. Microbiology 145 ( Pt 6): 1299-1306.
  130. Li, Z.F., Li, X., Liu, H., Liu, X., Han, K., Wu, Z.H., Hu, W., Li, F.F. and Li, Y.Z., (2011) Genome sequence of the halotolerant marine bacterium Myxococcus fulvus HW-1. J Bacteriol 193: 5015-5016.
  131. Furusawa, G., Dziewanowska, K., Stone, H., Settles, M. and Hartzell, P., (2011) Global analysis of phase variation in Myxococcus xanthus. Mol Microbiol 81: 784-804.
  132. Muller, F.D., Treuner-Lange, A., Heider, J., Huntley, S.M. and Higgs, P.I., (2010) Global transcriptome analysis of spore formation in Myxococcus xanthus reveals a locus necessary for cell differentiation. BMC Genomics 11: 264.
  133. Klose, K.E., Weiss, D.S. and Kustu, S., (1993) Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl- phosphate and activates the protein. J Mol Biol 232: 67-78.
  134. Smaldone, G.T., Jin, Y., Whitfield, D.L., Mu, A.Y., Wong, E.C., Wuertz, S. and Singer, M., (2014) Growth of Myxococcus xanthus in continuous-flow-cell bioreactors as a method for studying development. Appl Environ Microbiol 80: 2461-2467.
  135. Gao, Z., Wen, C.K., Binder, B.M., Chen, Y.F., Chang, J., Chiang, Y.H., Kerris, R.J., 3rd, Chang, C. and Schaller, G.E., (2008) Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. J Biol Chem 283: 23801- 23810.
  136. Inoue, H., Nojima, H. and Okayama, H., (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96: 23-28.
  137. Kroos, L., (2017) Highly Signal-Responsive Gene Regulatory Network Governing Myxococcus Development. Trends Genet 33: 3-15.
  138. Gamble, R.L., Coonfield, M.L. and Schaller, G.E., (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci U S A 95: 7825-7829.
  139. West, A.H. and Stock, A.M., (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
  140. Wolanin, P.M., Thomason, P.A. and Stock, J.B., (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3: REVIEWS3013.
  141. Kessin, R.H., Gundersen, G.G., Zaydfudim, V. and Grimson, M., (1996) How cellular slime molds evade nematodes. Proc Natl Acad Sci U S A 93: 4857-4861.
  142. Kenney, L.J., (2010) How important is the phosphatase activity of sensor kinases? Curr Opin Microbiol 13: 168-176.
  143. Cao, P., Dey, A., Vassallo, C.N. and Wall, D., (2015) How Myxobacteria Cooperate. J Mol Biol 427: 3709-3721.
  144. Hager, E., Tse, H. and Gill, R.E., (2001) Identification and characterization of spdR mutations that bypass the BsgA protease-dependent regulation of developmental gene expression in Myxococcus xanthus. Mol Microbiol 39: 765-780.
  145. Cusick, J.K., Hager, E. and Gill, R.E., (2015) Identification of a mutant locus that bypasses the BsgA protease requirement for social development in Myxococcus xanthus. FEMS Microbiol Lett 362: 1-8.
  146. Ueki, T. and 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.
  147. Nariya, H. and Inouye, S., (2005c) Identification of a protein Ser/Thr kinase cascade that regulates essential transcriptional activators in Myxococcus xanthus development. Mol Microbiol 58: 367-379.
  148. Udo, H., Lam, C.K., Mori, S., Inouye, M. and Inouye, S., (2000) Identification of a substrate for Pkn2, a protein Ser/Thr kinase from Myxococcus xanthus by a novel method for substrate identification. J Mol Microbiol Biotechnol 2: 557- 563.
  149. Lobedanz, S. and 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.
  150. Schaffer, A.A., Aravind, L., Madden, T.L., Shavirin, S., Spouge, J.L., Wolf, Y.I., Koonin, E.V. and Altschul, S.F., (2001) Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res 29: 2994-3005.
  151. Dworkin, M. and Sadler, W., (1966) Induction of cellular morphogenesis in Myxococcus xanthus. I. General description. J Bacteriol 91: 1516-1519.
  152. Diodati, M.E., Gill, R.E., Plamann, L. and Singer, M., (2008) Initiation and early developmental events. In: Myxobacteria: Multicellularity and Differentiation. Whitworth, D.E. (ed). Washington DC: ASM Press, pp. 43-76.
  153. Burbulys, D., Trach, K.A. and Hoch, J.A., (1991) Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64: 545-552.
  154. Uhl, M.A. and Miller, J.F., (1996) Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J 15: 1028-1036.
  155. Shimkets, L.J., (1999) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53: 525-549.
  156. Galperin, M.Y., Higdon, R. and Kolker, E., (2010) Interplay of heritage and habitat in the distribution of bacterial signal transduction systems. Mol Biosyst 6: 721- 728.
  157. Schramm, A., Lee, B. and Higgs, P.I., (2012) Intra-and interprotein phosphorylation between two-hybrid histidine kinases controls Myxococcus xanthus developmental progression. J Biol Chem 287: 25060-25072.
  158. Seidman, C.E., Struhl, K., Sheen, J. and Jessen, T., (2001) Introduction of Plasmid DNA into Cells. Current Protocols in Molecular Biology: 37:II:31.38:31.38.31- 31.38.10.
  159. Silversmith, R.E., Levin, M.D., Schilling, E. and Bourret, R.B., (2008) Kinetic characterization of catalysis by the chemotaxis phosphatase CheZ. Modulation of activity by the phosphorylated CheY substrate. J Biol Chem 283: 756-765.
  160. Gutu, A.D., Wayne, K.J., Sham, L.T. and Winkler, M.E., (2010) Kinetic characterization of the WalRKSpn (VicRK) two-component system of Streptococcus pneumoniae: dependence of WalKSpn (VicK) phosphatase activity on its PAS domain. J Bacteriol 192: 2346-2358.
  161. Henry, J.T. and Crosson, S., (2011) Ligand-binding PAS domains in a genomic, cellular, and structural context. Annu Rev Microbiol 65: 261-286.
  162. Hoiczyk, E., Ring, M.W., McHugh, C.A., Schwar, G., Bode, E., Krug, D., Altmeyer, M.O., Lu, J.Z. and Bode, H.B., (2009) Lipid body formation plays a central role in cell fate determination during developmental differentiation of Myxococcus xanthus. Mol Microbiol 74: 497-517.
  163. Velicer, G.J., Kroos, L. and Lenski, R.E., (1998) Loss of social behaviors by myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci U S A 95: 12376-12380.
  164. Wadhams, G.H. and Armitage, J.P., (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
  165. Nariya, H. and Inouye, M., (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132: 55-66.
  166. Bourret, R.B., Thomas, S.A., Page, S.C., Creager-Allen, R.L., Moore, A.M. and Silversmith, R.E., (2010) Measurement of response regulator autodephosphorylation rates spanning six orders of magnitude. Methods Enzymol 471: 89-114.
  167. Weiss, V., Kramer, G., Dunnebier, T. and Flotho, A., (2002) Mechanism of regulation of the bifunctional histidine kinase NtrB in Escherichia coli. J Mol Microbiol Biotechnol 4: 229-233.
  168. Thomasson, B., Link, J., Stassinopoulos, A.G., Burke, N., Plamann, L. and Hartzell, P.L., (2002) MglA, a small GTPase, interacts with a tyrosine kinase to control type IV pili-mediated motility and development of Myxococcus xanthus. Mol Microbiol 46: 1399-1413.
  169. Nariya, H. and Inouye, S., (2005a) Modulating factors for the Pkn4 kinase cascade in regulating 6-phosphofructokinase in Myxococcus xanthus. Mol Microbiol 56: 1314-1328.
  170. Bretl, D.J. and Kirby, J.R., (2016) Molecular Mechanisms of Signaling in Myxococcus xanthus Development. J Mol Biol 428: 3805-3830.
  171. Singh, B.N., (1947) Myxobacteria in soils and composts; their distribution, number and lytic action on bacteria. J Gen Microbiol 1: 1-10.
  172. Pathak, D.T., Wei, X. and Wall, D., (2012) Myxobacterial tools for social interactions. Res Microbiol 163: 579-591.
  173. Munoz-Dorado, J., Marcos-Torres, F.J., Garcia-Bravo, E., Moraleda-Munoz, A. and Perez, J., (2016) Myxobacteria: Moving, Killing, Feeding, and Surviving Together. Front Microbiol 7: 781.
  174. Lee, B., Holkenbrink, C., Treuner-Lange, A. and Higgs, P.I., (2012) Myxococcus xanthus developmental cell fate production: heterogeneous accumulation of developmental regulatory proteins and reexamination of the role of MazF in developmental lysis. J Bacteriol 194: 3058-3068.
  175. Garcia-Hernandez, R., Moraleda-Munoz, A., Castaneda-Garcia, A., Perez, J. and Munoz-Dorado, J., (2009) Myxococcus xanthus Pph2 is a manganese- dependent protein phosphatase involved in energy metabolism. J Biol Chem 284: 28720-28728.
  176. Higgs, P.I., P.L. Hartzell, C. Holkenbrink and E. Hoiczyk, (2014) Myxococcus xanthus vegetative and developmental cell heterogeneity. In: Myxobacteria: Genomics, Cellular and Molecular Biology. Higgs, Z.Y.a.P.I. (ed). pp. 51-77.
  177. Kraemer, S.A., Toups, M.A. and Velicer, G.J., (2010) Natural variation in developmental life-history traits of the bacterium Myxococcus xanthus. FEMS Microbiol Ecol 73: 226-233.
  178. Vos, M. and Velicer, G.J., (2008) Natural variation of gliding motility in a centimetre- scale population of Myxococcus xanthus. FEMS Microbiol Ecol 64: 343-350.
  179. Akiyama, T., Inouye, S. and Komano, T., (2003) Novel developmental genes, fruCD, of Myxococcus xanthus: involvement of a cell division protein in multicellular development. J Bacteriol 185: 3317-3324.
  180. Rajagopalan, R. and Kroos, L., (2014) Nutrient-regulated proteolysis of MrpC halts expression of genes important for commitment to sporulation during Myxococcus xanthus development. J Bacteriol 196: 2736-2747.
  181. Chung, C.T., Niemela, S.L. and Miller, R.H., (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86: 2172-2175.
  182. Taylor, B.L. and Zhulin, I.B., (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506.
  183. Lewis, K., (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5: 48-56.
  184. Zhou, L., Lei, X.H., Bochner, B.R. and Wanner, B.L., (2003) Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J Bacteriol 185: 4956-4972.
  185. Zhu, Y., Qin, L., Yoshida, T. and Inouye, M., (2000) Phosphatase activity of histidine kinase EnvZ without kinase catalytic domain. Proc Natl Acad Sci U S A 97: 7808-7813.
  186. Lewis, R.J., Brannigan, J.A., Muchova, K., Barak, I. and Wilkinson, A.J., (1999) Phosphorylated aspartate in the structure of a response regulator protein. J Mol Biol 294: 9-15.
  187. Welch, M., Oosawa, K., Aizawa, S. and Eisenbach, M., (1993) Phosphorylation- dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci U S A 90: 8787-8791.
  188. Kaimer, C. and Zusman, D.R., (2013) Phosphorylation-dependent localization of the response regulator FrzZ signals cell reversals in Myxococcus xanthus. Mol Microbiol 88: 740-753.
  189. Berg, H.C. and Purcell, E.M., (1977) Physics of chemoreception. Biophys J 20: 193- 219.
  190. Taylor, S.S., Yang, J., Wu, J., Haste, N.M., Radzio-Andzelm, E. and Anand, G., (2004) PKA: a portrait of protein kinase dynamics. Biochim Biophys Acta 1697: 259- 269.
  191. Ueki, T., Inouye, S. and Inouye, M., (1996) Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183: 153-157.
  192. Treuner-Lange, A., Ward, M.J. and Zusman, D.R., (2001) Pph1 from Myxococcus xanthus is a protein phosphatase involved in vegetative growth and development. Mol Microbiol 40: 126-140.
  193. Appleby, J.L. and Bourret, R.B., (1998) Proposed signal transduction role for conserved CheY residue Thr87, a member of the response regulator active- site quintet. J Bacteriol 180: 3563-3569.
  194. Stewart, R.C., (2010) Protein histidine kinases: assembly of active sites and their regulation in signaling pathways. Curr Opin Microbiol 13: 133-141.
  195. Lasker, M., Bui, C.D., Besant, P.G., Sugawara, K., Thai, P., Medzihradszky, G. and Turck, C.W., (1999) Protein histidine phosphorylation: increased stability of thiophosphohistidine. Protein Sci 8: 2177-2185.
  196. Hanks, S.K. and Hunter, T., (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9: 576-596.
  197. Schreiber, M., Res, I. and Matter, A., (2009) Protein kinases as antibacterial targets. Curr Opin Cell Biol 21: 325-330.
  198. Inouye, S., Nariya, H. and Munoz-Dorado, J., (2008) Protein Ser/Thr Kinases and Phosphatases in Myxococcus xanthus. In: Myxobacteria -Multicellularity and Differentiation. Whitworth, D.E. (ed). Washington, DC: ASM Press, pp. 191- 210.
  199. Kim, S.K. and Kaiser, D., (1990b) Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc Natl Acad Sci U S A 87: 3635- 3639.
  200. Bourret, R.B., (2010) Receiver domain structure and function in response regulator proteins. Curr Opin Microbiol 13: 142-149.
  201. Schumacher, D. and Sogaard-Andersen, L., (2017) Regulation of Cell Polarity in Motility and Cell Division in Myxococcus xanthus. Annu Rev Microbiol 71: 61- 78.
  202. Rajagopal, L., Vo, A., Silvestroni, A. and Rubens, C.E., (2006) Regulation of cytotoxin expression by converging eukaryotic-type and two-component signalling mechanisms in Streptococcus agalactiae. Mol Microbiol 62: 941-957.
  203. Campos, J.M. and Zusman, D.R., (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.
  204. Wu, S.S. and Kaiser, D., (1997) Regulation of expression of the pilA gene in Myxococcus xanthus. J Bacteriol 179: 7748-7758.
  205. Nolen, B., Taylor, S. and Ghosh, G., (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol Cell 15: 661-675.
  206. Gooderham, W.J. and Hancock, R.E., (2009) Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 33: 279-294.
  207. Velicer, G.J., Lenski, R.E. and Kroos, L., (2002) Rescue of social motility lost during evolution of Myxococcus xanthus in an asocial environment. J Bacteriol 184: 2719-2727.
  208. Sudo, S.Z. and Dworkin, M., (1969) Resistance of vegetative cells and microcysts of Myxococcus xanthus. J Bacteriol 98: 883-887.
  209. Dutta, R. and Inouye, M., (1996) Reverse phosphotransfer from OmpR to EnvZ in a kinase-/phosphatase+ mutant of EnvZ (EnvZ.N347D), a bifunctional signal transducer of Escherichia coli. J Biol Chem 271: 1424-1429.
  210. Porter, S.L., Wadhams, G.H. and Armitage, J.P., (2008a) Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol 16: 251-260.
  211. Dahl, J.L., Ulrich, C.H. and Kroft, T.L., (2011) Role of phase variation in the resistance of Myxococcus xanthus fruiting bodies to Caenorhabditis elegans predation. J Bacteriol 193: 5081-5089.
  212. Hutchings, M.I., Hoskisson, P.A., Chandra, G. and Buttner, M.J., (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150: 2795-2806.
  213. Cheung, J. and Hendrickson, W.A., (2010) Sensor domains of two-component regulatory systems. Curr Opin Microbiol 13: 116-123.
  214. Yamada, S., Nakamura, H., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T. and Shiro, Y., (2007) Separation of a phosphorylated histidine protein using phosphate affinity polyacrylamide gel electrophoresis. Anal Biochem 360: 160-162.
  215. Kinoshita, E., Kinoshita-Kikuta, E., Matsubara, M., Yamada, S., Nakamura, H., Shiro, Y., Aoki, Y., Okita, K. and Koike, T., (2008) Separation of phosphoprotein isotypes having the same number of phosphate groups using phosphate- affinity SDS-PAGE. Proteomics 8: 2994-3003.
  216. Blom, N., Gammeltoft, S. and Brunak, S., (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294: 1351- 1362.
  217. Kaiser, D., (2004) Signaling in myxobacteria. Annu Rev Microbiol 58: 75-98.
  218. Psakis, G., Mailliet, J., Lang, C., Teufel, L., Essen, L.O. and Hughes, J., (2011) Signaling kinetics of cyanobacterial phytochrome Cph1, a light regulated histidine kinase. Biochemistry 50: 6178-6188.
  219. Segall, J.E., Manson, M.D. and Berg, H.C., (1982) Signal processing times in bacterial chemotaxis. Nature 296: 855-857.
  220. Stock, J. and Da Re, S., (2000) Signal transduction: response regulators on and off. Curr Biol 10: R420-424.
  221. Appleby, J.L., Parkinson, J.S. and Bourret, R.B., (1996) Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86: 845- 848.
  222. Jenal, U. and Galperin, M.Y., (2009) Single domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr Opin Microbiol 12: 152-160.
  223. Schultz, J., Milpetz, F., Bork, P. and Ponting, C.P., (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95: 5857-5864.
  224. Letunic, I., Doerks, T. and Bork, P., (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43: D257-260.
  225. Shimkets, L.J., (1990) Social and developmental biology of the myxobacteria. Microbiol Rev 54: 473-501.
  226. Velicer, G.J. and Vos, M., (2009) Sociobiology of the myxobacteria. Annu Rev Microbiol 63: 599-623.
  227. Julien, B., Kaiser, A.D. and Garza, A., (2000) Spatial control of cell differentiation in Myxococcus xanthus. Proc Natl Acad Sci U S A 97: 9098-9103.
  228. Curtis, P.D., Taylor, R.G., Welch, R.D. and Shimkets, L.J., (2007) Spatial organization of Myxococcus xanthus during fruiting body formation. J Bacteriol 189: 9126- 9130.
  229. Laub, M.T. and Goulian, M., (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41: 121-145.
  230. Tan, I.S. and Ramamurthi, K.S., (2014) Spore formation in Bacillus subtilis. Environ Microbiol Rep 6: 212-225.
  231. Muller, F.D., Schink, C.W., Hoiczyk, E., Cserti, E. and Higgs, P.I., (2012) Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83: 486-505.
  232. Cho, K. and Zusman, D.R., (1999) Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol Microbiol 34: 714-725.
  233. Xie, C., Zhang, H., Shimkets, L.J. and Igoshin, O.A., (2011) Statistical image analysis reveals features affecting fates of Myxococcus xanthus developmental aggregates. Proc Natl Acad Sci U S A 108: 5915-5920.
  234. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R. and Kolter, R., (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11: 157- 168.
  235. Mascher, T., Helmann, J.D. and Unden, G., (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70: 910-938.
  236. Galperin, M.Y., (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188: 4169- 4182.
  237. Casino, P., Rubio, V. and Marina, A., (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139: 325- 336.
  238. Moglich, A., Ayers, R.A. and Moffat, K., (2009b) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17: 1282-1294.
  239. Greenstein, A.E., Grundner, C., Echols, N., Gay, L.M., Lombana, T.N., Miecskowski, C.A., Pullen, K.E., Sung, P.Y. and Alber, T., (2005) Structure/function studies of Ser/Thr and Tyr protein phosphorylation in Mycobacterium tuberculosis. J Mol Microbiol Biotechnol 9: 167-181.
  240. Young, T.A., Delagoutte, B., Endrizzi, J.A., Falick, A.M. and Alber, T., (2003) Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat Struct Biol 10: 168-174.
  241. Marina, A., Waldburger, C.D. and Hendrickson, W.A., (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24: 4247- 4259.
  242. Grefen, C., Stadele, K., Ruzicka, K., Obrdlik, P., Harter, K. and Horak, J., (2008) Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol Plant 1: 308-320.
  243. Dyer, C.M. and Dahlquist, F.W., (2006) Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM. J Bacteriol 188: 7354-7363.
  244. Holkenbrink, C., Hoiczyk, E., Kahnt, J. and Higgs, P.I., (2014) Synthesis and assembly of a novel glycan layer in Myxococcus xanthus spores. J Biol Chem 289: 32364-32378.
  245. Wegener-Feldbrugge, S. and Sogaard-Andersen, L., (2009) The atypical hybrid histidine protein kinase RodK in Myxococcus xanthus: spatial proximity supersedes kinetic preference in phosphotransfer reactions. J Bacteriol 191: 1765-1776.
  246. Fritsch, F., Mauder, N., Williams, T., Weiser, J., Oberle, M. and Beier, D., (2011) The cell envelope stress response mediated by the LiaFSRLm three-component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaSLm. Microbiology 157: 373-386.
  247. Huse, M. and Kuriyan, J., (2002) The conformational plasticity of protein kinases. Cell 109: 275-282.
  248. Rajagopalan, R. and Kroos, L., (2017) The dev Operon Regulates the Timing of Sporulation during Myxococcus xanthus Development. J Bacteriol 199.
  249. Reichenbach, H., (1999) The ecology of the myxobacteria. Environ Microbiol 1: 15- 21.
  250. Libby, E.A., Goss, L.A. and Dworkin, J., (2015) The Eukaryotic-Like Ser/Thr Kinase PrkC Regulates the Essential WalRK Two-Component System in Bacillus subtilis. PLoS Genet 11: e1005275.
  251. Av-Gay, Y. and Everett, M., (2000) The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol 8: 238-244.
  252. Alm, E., Huang, K. and Arkin, A., (2006) The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol 2: e143.
  253. Li, S.G., Zhou, X.W., Li, P.F., Han, K., Li, W., Li, Z.F., Wu, Z.H. and Li, Y.Z., (2012) The existence and diversity of myxobacteria in lake mud -a previously unexplored myxobacteria habitat. Environ Microbiol Rep 4: 587-595.
  254. Ellehauge, E., Norregaard-Madsen, M. and 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.
  255. Harris, B.Z., Kaiser, D. and Singer, M., (1998) The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev 12: 1022-1035.
  256. Crosson, S., Rajagopal, S. and Moffat, K., (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42: 2-10.
  257. Casino, P., Rubio, V. and Marina, A., (2010) The mechanism of signal transduction by two-component systems. Curr Opin Struct Biol 20: 763-771.
  258. Ulrich, L.E. and Zhulin, I.B., (2010) The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res 38: D401-407.
  259. Durocher, D., Taylor, I.A., Sarbassova, D., Haire, L.F., Westcott, S.L., Jackson, S.P., Smerdon, S.J. and Yaffe, M.B., (2000) The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho- dependent signaling mechanisms. Mol Cell 6: 1169-1182.
  260. Beebe, J.M., (1941) The Morphology and Cytology of Myxococcus xanthus, N. Sp. J Bacteriol 42: 193-223.
  261. Thomas, S.H., Wagner, R.D., Arakaki, A.K., Skolnick, J., Kirby, J.R., Shimkets, L.J., Sanford, R.A. and Loffler, F.E., (2008b) The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria. PLoS One 3: e2103.
  262. Shimkets, L., Reichenbach, H. and Dworkin, M., (2006) The Myxobacteria. . In: The Prokaryotes. Dworkin, M. (ed). New York: Springer, pp. 31-115.
  263. Jagadeesan, S., (2008) The Myxococcus xanhus Red two-component signal transduction system: a novel "four-component" signaling mechanism. In: Max- Planck-Institut für Terrestrische Mikrobiologie. Philipps-Universität Marburg.
  264. Lee, B., Mann, P., Grover, V., Treuner-Lange, A., Kahnt, J. and Higgs, P.I., (2011a) The Myxococcus xanthus spore cuticula protein C is a fragment of FibA, an extracellular metalloprotease produced exclusively in aggregated cells. PLoS One 6: e28968.
  265. Bren, A. and Eisenbach, M., (1998) The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J Mol Biol 278: 507-514.
  266. Treuner-Lange, A., (2010) The phosphatomes of the multicellular myxobacteria Myxococcus xanthus and Sorangium cellulosum in comparison with other prokaryotic genomes. PLoS One 5: e11164.
  267. Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N. and Sternberg, M.J., (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845-858.
  268. Keane, R. and Berleman, J., (2016) The predatory life cycle of Myxococcus xanthus. Microbiology 162: 1-11.
  269. Inclan, Y.F., Laurent, S. and Zusman, D.R., (2008) The receiver domain of FrzE, a CheA-CheY fusion protein, regulates the CheA histidine kinase activity and downstream signalling to the A-and S-motility systems of Myxococcus xanthus. Mol Microbiol 68: 1328-1339.
  270. Lee, B., (2009) The role of negative regulators in coordination of the Myxococcus xanthus developmental program. In: Max-Planck-Institut für Terrestrische Mikrobiologie. Philipps-Universität Marburg.
  271. West, S.A., Diggle, S.P., Buckling, A., Gardner, A. and Griffin, A.S., (2007) The Social Lives of Microbes. Annual Review of Ecology, Evolution and Sysstematics 38: 53-77.
  272. Meiser, P., Bode, H.B. and Muller, R., (2006) The unique DKxanthene secondary metabolite family from the myxobacterium Myxococcus xanthus is required for developmental sporulation. Proc Natl Acad Sci U S A 103: 19128-19133.
  273. Shapiro, J.A., (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52: 81-104.
  274. Lin, W.J., Walthers, D., Connelly, J.E., Burnside, K., Jewell, K.A., Kenney, L.J. and Rajagopal, L., (2009) Threonine phosphorylation prevents promoter DNA binding of the Group B Streptococcus response regulator CovR. Mol Microbiol 71: 1477-1495.
  275. Rasmussen, A.A. and Sogaard-Andersen, L., (2003) TodK, a putative histidine protein kinase, regulates timing of fruiting body morphogenesis in Myxococcus xanthus. J Bacteriol 185: 5452-5464.
  276. Haldimann, A., Fisher, S.L., Daniels, L.L., Walsh, C.T. and Wanner, B.L., (1997) Transcriptional regulation of the Enterococcus faecium BM4147 vancomycin resistance gene cluster by the VanS-VanR two-component regulatory system in Escherichia coli K-12. J Bacteriol 179: 5903-5913.
  277. Robinson, M., Son, B., Kroos, D. and Kroos, L., (2014) Transcription factor MrpC binds to promoter regions of hundreds of developmentally-regulated genes in Myxococcus xanthus. BMC Genomics 15: 1123.
  278. Hoch, J.A., (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3: 165-170.
  279. Goulian, M., (2010) Two-component signaling circuit structure and properties. Curr Opin Microbiol 13: 184-189.
  280. Stock, A.M., Robinson, V.L. and Goudreau, P.N., (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
  281. Lee, B., Schramm, A., Jagadeesan, S. and Higgs, P.I., (2010) Two-component systems and regulation of developmental progression in Myxococcus xanthus. Methods Enzymol 471: 253-278.
  282. Whitworth, D.E. and Cock, P.J., (2008) Two-component systems of the myxobacteria: structure, diversity and evolutionary relationships. Microbiology 154: 360-372.
  283. Stein, E.A., Cho, K., Higgs, P.I. and Zusman, D.R., (2006) Two Ser/Thr protein kinases essential for efficient aggregation and spore morphogenesis in Myxococcus xanthus. Mol Microbiol 60: 1414-1431.
  284. Iniesta, A.A., Garcia-Heras, F., Abellon-Ruiz, J., Gallego-Garcia, A. and Elias-Arnanz, M., (2012) Two systems for conditional gene expression in Myxococcus xanthus inducible by isopropyl-beta-D-thiogalactopyranoside or vanillate. J Bacteriol 194: 5875-5885.
  285. Thomas, S.A., Brewster, J.A. and Bourret, R.B., (2008a) Two variable active site residues modulate response regulator phosphoryl group stability. Mol Microbiol 69: 453-465.
  286. Nan, B. and Zusman, D.R., (2011) Uncovering the mystery of gliding motility in the myxobacteria. Annu Rev Genet 45: 21-39.
  287. Barbieri, C.M. and Stock, A.M., (2008) Universally applicable methods for monitoring response regulator aspartate phosphorylation both in vitro and in vivo using Phos-tag-based reagents. Anal Biochem 376: 73-82.
  288. Carlson, H.K., Plate, L., Price, M.S., Allen, J.J., Shokat, K.M. and Marletta, M.A., (2010) Use of a semisynthetic epitope to probe histidine kinase activity and regulation. Anal Biochem 397: 139-143.
  289. Laue, B.E. and Gill, R.E., (1995) Using a phase-locked mutant of Myxococcus xanthus to study the role of phase variation in development. J Bacteriol 177: 4089- 4096.
  290. Kinoshita-Kikuta, E., Kinoshita, E., Eguchi, Y. and Koike, T., (2016) Validation of Cis and Trans Modes in Multistep Phosphotransfer Signaling of Bacterial Tripartite Sensor Kinases by Using Phos-Tag SDS-PAGE. PLoS One 11: e0148294.
  291. Velicer, G.J., Mendes-Soares, H. and Wielgoss, S., (2014) Whence Comes Social Diversity? Ecological and Evolutionary Analysis of the Myxobacteria. In: Myxobacteria -Genomics, Cellular and Molecular Biology. Yang, Z. and Higgs, P.I. (eds). Norfolk, UK: Caister Academic Press, pp. 1-29.
  292. Velicer, G.J. and Hillesland, K.L., (2008) Why Cooperate? The Ecology and Evolution of Myxobacteria. In: Myxobacteria -Multicellularity and Differentiation. Withworth, D.E. (ed). Washington, D.C.: ASM Press, pp. 17-40.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten