Contact- and Protein Transfer-Dependent Stimulation of Assembly of the Gliding Motility Machinery in

English version České info

Motility facilitates a wide variety of processes such as virulence, biofilm formation and development in bacteria. Bacteria have evolved at least three mechanisms for motility on surfaces: swarming motility, twitching motility and gliding motility. Mechanistically, gliding motility is poorly understood. Here, we focused on four proteins in Myxococcus xanthus that are essential for gliding. We show that CglC is an outer membrane (OM) lipoprotein, GltB and GltA are integral OM β-barrel proteins, and GltC is a soluble periplasmic protein. GltB, GltA and GltC are components of the gliding motility complex, and CglC likely stimulates the integration of GltB and GltA into the OM. Moreover, CglC, in a cell-cell contact-dependent manner, can be transferred from a cglC+ donor to a ΔcglC mutant leading to stimulation of gliding motility in the recipient. We show that upon physical transfer of CglC, CglC stimulates the assembly of the gliding motility complex in the recipient. The data presented here adds to the growing list of cell-cell contact-dependent activities in bacteria by demonstrating that gliding motility can be stimulated in a contact-dependent manner by transfer of a protein that stimulates assembly of the gliding motility complexes.

Vyšlo v časopise: Contact- and Protein Transfer-Dependent Stimulation of Assembly of the Gliding Motility Machinery in. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005341
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005341

Souhrn

Zdroje

1. Bassler BL, Losick R (2006) Bacterially speaking. Cell 125: 237–246. 16630813

2. Konovalova A, Søgaard-Andersen L (2011) Close encounters: contact-dependent interactions in bacteria. Mol Microbiol 81: 297–301. doi: 10.1111/j.1365-2958.2011.07711.x 21651624

3. Hayes CS, Aoki SK, Low DA (2010) Bacterial contact-dependent delivery dystems. Annu Rev Genet 44: 71–90. doi: 10.1146/annurev.genet.42.110807.091449 21047256

4. Ruhe ZC, Low DA, Hayes CS (2013) Bacterial contact-dependent growth inhibition. Trends Microbiol 21: 230–237. doi: 10.1016/j.tim.2013.02.003 23473845

5. Pathak DT, Wei X, Wall D (2012) Myxobacterial tools for social interactions. Res Microbiol 163: 579–591. doi: 10.1016/j.resmic.2012.10.022 23123306

6. Jarrell KF, McBride MJ (2008) The surprisingly diverse ways that prokaryotes move. Nat Rev Micro 6: 466–476.

7. Macnab RM (2003) How bacteria assemble flagella. Ann Rev Microbiol 57: 77–100.

8. Pelicic V (2008) Type IV pili: pluribus unum? Mol Microbiol 68: 827–837. doi: 10.1111/j.1365-2958.2008.06197.x 18399938

9. McBride MJ (2001) Bacterial gliding motility: Multiple mechanisms for cell movement over surfaces. Ann Rev Microbiol 55: 49–75.

10. Hodgkin J, Kaiser D (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): Two gene systems control movement. Mol Gen Genet 171: 177–191.

11. Wu SS, 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. 8748037

12. Sliusarenko O, Zusman DR, Oster G (2007) The motors powering A-motility in Myxococcus xanthus are distributed along the cell body. J Bacteriol 189: 7920–7921. 17704221

13. Sun M, Wartel M, Cascales E, Shaevitz JW, Mignot T (2011) Motor-driven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci U S A 108: 7559–7564. doi: 10.1073/pnas.1101101108 21482768

14. Sun H, Yang Z, Shi W (1999) Effect of cellular filamentation on adventurous and social gliding motility of Myxococcus xanthus. Proc Natl Acad Sci USA 96: 15178–15183. 10611358

15. Nan BY, Mauriello EMF, Sun IH, Wong A, Zusman DR (2010) A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol Microbiol 76: 1539–1554. doi: 10.1111/j.1365-2958.2010.07184.x 20487265

16. Mignot T, Shaevitz JW, Hartzell PL, Zusman DR (2007) Evidence that focal adhesion complexes power bacterial gliding motility. Science 315: 853–856. 17289998

17. Luciano J, Agrebi R, Le Gall AV, Wartel M, Fiegna F, Ducret A, et al. (2011) Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7: e1002268. doi: 10.1371/journal.pgen.1002268 21931562

18. Nan B, Chen J, Neu JC, Berry RM, Oster G, Zusman DR (2011) Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci USA 108: 2498–2503. doi: 10.1073/pnas.1018556108 21248229

19. Ducret A, Valignat M-P, Mouhamar F, Mignot T, Theodoly O (2012) Wet-surface–enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. Proc Natl Acad Sci USA 109: 10036–10041. doi: 10.1073/pnas.1120979109 22665761

20. Pathak DT, Wall D (2012) Identification of the cglC, cglD, cglE, and cglF genes and their role in cell contact-dependent gliding motility in Myxococcus xanthus. J Bacteriol 194: 1940–1949. doi: 10.1128/JB.00055-12 22343295

21. Youderian P, Burke N, White D, Hartzell PL (2003) Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49: 555–570. 12828649

22. Yu R, Kaiser D (2007) Gliding motility and polarized slime secretion. Mol Microbiol 63: 454–467. 17176257

23. Nan BY, Bandaria JN, Moghtaderi A, Sun IH, Yildiz A, Zusman DR (2013) Flagella stator homologs function as motors for myxobacterial gliding motility by moving in helical trajectories. Proc Natl Acad Sci USA 110: E1508–E1513. doi: 10.1073/pnas.1219982110 23576734

24. Müller FD, Schink CW, Hoiczyk E, Cserti E, Higgs PI (2012) Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83: 486–505. doi: 10.1111/j.1365-2958.2011.07944.x 22188356

25. Holkenbrink C, Hoiczyk E, Kahnt J, Higgs PI (2014) Synthesis and assembly of a novel glycan layer in Myxococcus xanthus spores. J Biol Chem 289: 32364–32378. doi: 10.1074/jbc.M114.595504 25271164

26. Agrebi R, Wartel M, Brochier-Armanet C, Mignot T (2015) An evolutionary link between capsular biogenesis and surface motility in bacteria. Nat Rev Micro 13: 318–326.

27. Wartel M, Ducret A, Thutupalli S, Czerwinski F, Le Gall AV, Mauriello EM, et al. (2013) A versatile class of cell surface directional motors gives rise to gliding motility and sporulation in Myxococcus xanthus. PLoS Biol 11: e1001728. doi: 10.1371/journal.pbio.1001728 24339744

28. Balagam R, Litwin DB, Czerwinski F, Sun M, Kaplan HB, Shaevitz JW, et al. (2014) Myxococcus xanthus gliding motors are elastically coupled to the substrate as predicted by the focal adhesion model of gliding motility. PLoS Comput Biol 10: e1003619. doi: 10.1371/journal.pcbi.1003619 24810164

29. Nudleman E, Wall D, Kaiser D (2005) Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309: 125–127. 15994555

30. Whittaker CA, Hynes RO (2002) Distribution and evolution of von Willebrand/Integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere. Mol Biol Cell 13: 3369–3387. 12388743

31. Rodriguez AM, Spormann AM (1999) Genetic and molecular analysis of cglB, a gene essential for single-cell gliding in Myxococcus xanthus. J Bacteriol 181: 4381–4390. 10400597

32. Kahnt J, Aguiluz K, Koch J, Treuner-Lange A, Konovalova A, Huntley S, et al. (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. doi: 10.1021/pr1004983 20687614

33. Hodgkin J, Kaiser D (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci USA 74: 2938–2942. 16592422

34. Wei X, Pathak DT, Wall D (2011) Heterologous protein transfer within structured myxobacteria biofilms. Mol Microbiol 81: 315–326. doi: 10.1111/j.1365-2958.2011.07710.x 21635581

35. Pathak DT, Wei X, Bucuvalas A, Haft DH, Gerloff DL, Wall D (2012) Cell contact-dependent outer membrane exchange in myxobacteria: genetic determinants and mechanism. PLOS Genet 8:: e1002626. doi: 10.1371/journal.pgen.1002626 22511878

36. Ducret A, Fleuchot B, Bergam P, Mignot T (2013) Direct live imaging of cell–cell protein transfer by transient outer membrane fusion in Myxococcus xanthus. eLife 2: e00868. doi: 10.7554/eLife.00868 23898400

37. Wei X, Vassallo CN, Pathak DT, Wall D (2014) Myxobacteria produce outer membrane-enclosed tubes in unstructured environments. J Bacteriol 196: 1807–1814. doi: 10.1128/JB.00850-13 24391054

38. Friedrich C, Bulyha I, Søgaard-Andersen L (2014) Outside-in assembly pathway of the type IV pilus system in Myxococcus xanthus. J Bacteriol 196: 378–390. doi: 10.1128/JB.01094-13 24187092

39. Nudleman E, Wall D, Kaiser D (2006) Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol 60: 16–29. 16556217

40. Keilberg D, Wuichet K, Drescher F, Søgaard-Andersen L (2012) A response regulator interfaces between the Frz chemosensory system and the MglA/MglB GTPase/GAP module to regulate polarity in Myxococcus xanthus. PLoS Genet 8: e1002951. doi: 10.1371/journal.pgen.1002951 23028358

41. Zhang Y, Guzzo M, Ducret A, Li Y-Z, Mignot T (2012) A dynamic response regulator protein modulates G-protein–dependent polarity in the bacterium Myxococcus xanthus. PLoS Genet 8: e1002872. doi: 10.1371/journal.pgen.1002872 22916026

42. Shi W, Zusman DR (1993) The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci USA 90: 3378–3382. 8475084

43. Bulyha I, Schmidt C, Lenz P, Jakovljevic V, Höne A, Maier B, et al. (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74: 691–706. doi: 10.1111/j.1365-2958.2009.06891.x 19775250

44. Jakovljevic V, Leonardy S, Hoppert M, Søgaard-Andersen L (2008) PilB and PilT are ATPases acting antagonistically in type IV pilus function in Myxococcus xanthus. J Bacteriol 190: 2411–2421. doi: 10.1128/JB.01793-07 18223089

45. Dashper SG, Hendtlass A, Slakeski N, Jackson C, Cross KJ, Brownfield L, et al. (2000) Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis. J Bacteriol 182: 6456–6462. 11053391

46. Jin S, Joe A, Lynett J, Hani EK, Sherman P, Chan VL (2001) JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39: 1225–1236. 11251839

47. Leuzzi R, Serino L, Scarselli M, Savino S, Fontana MR, Monaci E, et al. (2005) Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol Microbiol 58: 669–681. 16238618

48. Drummelsmith J, Whitfield C (2000) Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J 19: 57–66. 10619844

49. Bhat S, Zhu X, Patel RP, Orlando R, Shimkets LJ (2011) Identification and localization of Myxococcus xanthus porins and lipoproteins. PLoS ONE 6: e27475. doi: 10.1371/journal.pone.0027475 22132103

50. Martinez-Canamero M, Munoz-Dorado J, Farez-Vidal E, Inouye M, Inouye S (1993) Oar, a 115-Kilodalton membrane protein required for development of Myxococcus xanthus. J Bacteriol 175: 4756–4763. 8335633

51. Rodriguez-Soto JP, Kaiser D (1997) Identification and localization of the Tgl protein, which is required for Myxococcus xanthus social motility. J Bacteriol 179: 4372–4381. 9209056

52. Siewering K, Jain S, Friedrich C, Webber-Birungi MT, Semchonok DA, Binzen I, et al. (2014) Peptidoglycan-binding protein TsaP functions in surface assembly of type IV pili. Proc Natl Acad Sci USA 111: E953–961. doi: 10.1073/pnas.1322889111 24556993

53. Pathak DT, Wei X, Dey A, Wall D (2013) Molecular recognition by a polymorphic cell surface receptor governs cooperative behaviors in bacteria. PLOS Genetics 9: e1003891. doi: 10.1371/journal.pgen.1003891 24244178

54. Shi XQ, Wegener-Feldbrugge S, Huntley S, Hamann N, Hedderich R, Søgaard-Andersen L (2008) Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus. J Bacteriol 190: 613–624. 17993514

55. Konovalova A, Löbach S, Søgaard-Andersen L (2012) A RelA-dependent two-tiered regulated proteolysis cascade controls synthesis of a contact-dependent intercellular signal in Myxococcus xanthus. Mol Microbiol 84: 260–275. doi: 10.1111/j.1365-2958.2012.08020.x 22404381

56. Das S, Noe JC, Paik S, Kitten T (2005) An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites. J Microbiol Methods 63: 89–94. 16157212

57. Pilhofer M, Bauer AP, Schrallhammer M, Richter L, Ludwig W, Schleifer KH, et al. (2007) Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel two-step gene walking method. Nucleic Acids Res 35: e135. 17942428

58. Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215: 403–410. 2231712

59. Overgaard M, Wegener-Feldbrugge S, Søgaard-Andersen L (2006) The orphan response regulator DigR is required for synthesis of extracellular matrix fibrils in Myxcoccus xanthus. J Bacteriol 188: 4384–4394. 16740945

60. Thomasson B, Link J, Stassinopoulos AG, Burke N, Plamann L, Hartzell PL (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. 12453225

61. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.

62. Leonardy S, Freymark G, Hebener S, Ellehauge E, 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. 17932488

63. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786. doi: 10.1038/nmeth.1701 21959131

64. Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652–1662. 12876315

65. Cserzo M, Wallin E, Simon I, vonHeijne G, Elofsson A (1997) Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Engineering 10: 673–676. 9278280

66. Remmert M, Linke D, Lupas AN, Soding J (2009) HHomp--prediction and classification of outer membrane proteins. Nucleic Acids Res 37: W446–451. doi: 10.1093/nar/gkp325 19429691

67. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, et al. (2010) The Pfam protein families database. Nucleic Acids Research 38: D211–222. doi: 10.1093/nar/gkp985 19920124

68. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. (2012) The Pfam protein families database. Nucleic Acids Research 40: D290–301. doi: 10.1093/nar/gkr1065 22127870

69. Hayat S, Elofsson A (2012) BOCTOPUS: improved topology prediction of transmembrane β barrel proteins. Bioinformatics 28: 516–522. doi: 10.1093/bioinformatics/btr710 22247276

70. Kaiser D (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76: 5952–5956. 42906

71. Hodgkin J, Kaiser D (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales)—Genes controlling movement of single cells. Molecular & General Genetics 171: 167–176.

72. Wall D, Kolenbrander PE, Kaiser D (1999) The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol 181: 24–33. 9864308

73. Wu SS, Kaiser D (1997) Regulation of expression of the pilA gene in Myxococcus xanthus. J Bacteriol 179: 7748–7758. 9401034

74. Yang RF, Bartle S, Otto R, Stassinopoulos A, Rogers M, Plamann L, et al. (2004) AglZ is a filament-forming coiled-coil protein required for adventurous gliding motility of Myxococcus xanthus. J Bacteriol 186: 6168–6178. 15342587

75. Leonardy S, Miertzschke M, Bulyha I, Sperling E, Wittinghofer A, Søgaard-Andersen L (2010) Regulation of dynamic polarity switching in bacteria by a Ras-like G-protein and its cognate GAP. EMBO J 29: 2276–2289. doi: 10.1038/emboj.2010.114 20543819