Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism

English version České info

Biofilms are dense microbial communities. Although widely distributed and medically important, how biofilm cells interact with one another is poorly understood. Recently, we described a novel process whereby myxobacterial biofilm cells exchange their outer membrane (OM) lipoproteins. For the first time we report here the identification of two host proteins, TraAB, required for transfer. These proteins are predicted to localize in the cell envelope; and TraA encodes a distant PA14 lectin-like domain, a cysteine-rich tandem repeat region, and a putative C-terminal protein sorting tag named MYXO-CTERM, while TraB encodes an OmpA-like domain. Importantly, TraAB are required in donors and recipients, suggesting bidirectional transfer. By use of a lipophilic fluorescent dye, we also discovered that OM lipids are exchanged. Similar to lipoproteins, dye transfer requires TraAB function, gliding motility and a structured biofilm. Importantly, OM exchange was found to regulate swarming and development behaviors, suggesting a new role in cell–cell communication. A working model proposes TraA is a cell surface receptor that mediates cell–cell adhesion for OM fusion, in which lipoproteins/lipids are transferred by lateral diffusion. We further hypothesize that cell contact–dependent exchange helps myxobacteria to coordinate their social behaviors.

Vyšlo v časopise: Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002626
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002626

Souhrn

Zdroje

1. DaviesD 2003 Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2 114 122

2. BasslerBLLosickR 2006 Bacterially speaking. Cell 125 237 246

3. NadellCDXavierJBFosterKR 2009 The sociobiology of biofilms. FEMS Microbiol Rev 33 206 224

4. StewartPSFranklinMJ 2008 Physiological heterogeneity in biofilms. Nat Rev Microbiol 6 199 210

5. NudlemanEWallDKaiserD 2005 Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309 125 127

6. WeiXPathakDTWallD 2011 Heterologous protein transfer within structured myxobacteria biofilms. Mol Microbiol 81 315 326

7. HodgkinJKaiserJ 1979 Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): Two gene systems control movement. Mol Gen Genet 171 177 191

8. HodgkinJKaiserD 1977 Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A 74 2938 2942

9. WallDKaiserD 1999 Type IV pili and cell motility. Mol Microbiol 32 1 10

10. NanBZusmanDR 2011 Uncovering the mystery of gliding motility in the myxobacteria. Annu Rev Genet 45 21 39

11. HodgkinJKaiserD 1979 Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): Genes controlling movements of single cells. Mol Gen Genet 171 167 176

12. Rodriguez-SotoJPKaiserD 1997 The tgl gene: social motility and stimulation in Myxococcus xanthus. J Bacteriol 179 4361 4371

13. RodriguezAMSpormannAM 1999 Genetic and molecular analysis of cglB, a gene essential for single-cell gliding in Myxococcus xanthus. J Bacteriol 181 4381 4390

14. PathakDTWallD 2012 Identification of the cglC, cglD, cglE and cglF genes and their role in cell contact-dependent gliding motility in Myxococcus xanthus. J Bacteriol In press

15. WallDKaiserD 1998 Alignment enhances the cell-to-cell transfer of pilus phenotype. Proc Natl Acad Sci U S A 95 3054 3058

16. NudlemanEWallDKaiserD 2006 Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol 60 16 29

17. GoldmanBSNiermanWCKaiserDSlaterSCDurkinAS 2006 Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103 15200 15205

18. WuSSKaiserD 1995 Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18 547 558

19. YouderianPBurkeNWhiteDJHartzellPL 2003 Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49 555 570

20. PetersenTNBrunakSvon HeijneGNielsenH 2011 SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8 785 786

21. RigdenDJMelloLVGalperinMY 2004 The PA14 domain, a conserved all-beta domain in bacterial toxins, enzymes, adhesins and signaling molecules. Trends Biochem Sci 29 335 339

22. ZupancicMLFriemanMSmithDAlvarezRACummingsRD 2008 Glycan microarray analysis of Candida glabrata adhesin ligand specificity. Mol Microbiol 68 547 559

23. BiegertAMayerCRemmertMSodingJLupasAN 2006 The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34 W335 339

24. VeeldersMBrucknerSOttDUnverzagtCMoschHU 2010 Structural basis of flocculin-mediated social behavior in yeast. Proc Natl Acad Sci U S A 107 22511 22516

25. KurowskiMABujnickiJM 2003 GeneSilico protein structure prediction meta-server. Nucleic Acids Res 31 3305 3307

26. GoossensKWillaertR 2010 Flocculation protein structure and cell-cell adhesion mechanism in Saccharomyces cerevisiae. Biotechnol Lett 32 1571 1585

27. KolbingerAGaoTBrockDAmmannRKistersA 2005 A cysteine-rich extracellular protein containing a PA14 domain mediates quorum sensing in Dictyostelium discoideum. Eukaryot Cell 4 991 998

28. PatersonGKMitchellTJ 2004 The biology of Gram-positive sortase enzymes. Trends Microbiol 12 89 95

29. HaftDHPaulsenITWardNSelengutJD 2006 Exopolysaccharide-associated protein sorting in environmental organisms: the PEP-CTERM/EpsH system. Application of a novel phylogenetic profiling heuristic. BMC Biol 4 29

30. HaftDHVargheseN 2011 GlyGly-CTERM and rhombosortase: a C-terminal protein processing signal in a many-to-one pairing with a rhomboid family intramembrane serine protease. PLoS ONE 6 e28886 doi:10.1371/journal.pone.0028886

31. HaftDHPayneSHSelengutJD 2012 Archaeosortases and exosortases are widely distributed systems linking membrane transit with posttranslational modification. J Bacteriol 194 36 48

32. KonovalovaAPettersTSogaard-AndersenL 2010 Extracellular biology of Myxococcus xanthus. FEMS Microbiol Rev 34 89 106

33. KraemerSAVelicerGJ 2011 Endemic social diversity within natural kin groups of a cooperative bacterium. Proc Natl Acad Sci U S A 108 Suppl 2 10823 10830

34. WallDKolenbranderPEKaiserD 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

35. KimSKKaiserD 1990 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

36. HayesCSAokiSKLowDA 2010 Bacterial contact-dependent delivery systems. Annu Rev Genet 44 71 90

37. KonovalovaASogaard-AndersenL 2011 Close encounters: Contact-dependent interactions in bacteria. Mol Microbiol 81 297 301

38. KudryashevMCyrklaffMAlexBLemgruberLBaumeisterW 2011 Evidence of direct cell-cell fusion in Borrelia by cryogenic electron tomography. Cell Microbiol 13 731 741

39. DubeyGPBen-YehudaS 2011 Intercellular nanotubes mediate bacterial communication. Cell 144 590 600

40. SmukallaSCaldaraMPochetNBeauvaisAGuadagniniS 2008 FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135 726 737

41. DaoDNKessinRHEnnisHL 2000 Developmental cheating and the evolutionary biology of Dictyostelium and Myxococcus. Microbiology 146 1505 1512

42. YamadaYMinamisawaHFukuzawaMKawataTOohataAA 2010 Prespore cell inducing factor, psi factor, controls both prestalk and prespore gene expression in Dictyostelium development. Dev Growth Differ 52 377 383

43. KawataTNakagawaMShimadaNFujiiSOohataAA 2004 A gene encoding, prespore-cell-inducing factor in Dictyostelium discoideum. Dev Growth Differ 46 383 392

44. TokudaHMatsuyamaS 2004 Sorting of lipoproteins to the outer membrane in E. coli. Biochim Biophys Acta 1694 IN1 9

45. MartensSMcMahonHT 2008 Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol 9 543 556

46. VosMVelicerGJ 2006 Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol 72 3615 3625

47. KimSKKaiserD 1990 Cell alignment required in differentiation of Myxococcus xanthus. Science 249 926 928

48. TravisanoMVelicerGJ 2004 Strategies of microbial cheater control. Trends Microbiol 12 72 78

49. WestSAGardnerA 2010 Altruism, spite, and greenbeards. Science 327 1341 1344

50. GardnerAWestSA 2010 Greenbeards. Evolution 64 25 38

51. QuellerDCPonteEBozzaroSStrassmannJE 2003 Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299 105 106

52. FontesMKaiserD 1999 Myxococcus cells respond to elastic forces in their substrate. Proc Natl Acad Sci U S A 96 8052 8057

53. MillerNAKingsmoreSFFarmerALangleyRJMudgeJ 2008 Management of high-throughput DNA sequencing projects: Alpheus. J Comput Sci Syst Biol 1 132

54. SambrookJRusselDW 2001 Molecular cloning: A laboratory manual Cold Sring Harbor, NY Cold Spring Harbor Press

55. SalisHMMirskyEAVoigtCA 2009 Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27 946 950

56. HartzellPKaiserD 1991 Upstream gene of the mgl operon controls the level of MglA protein in Myxococcus xanthus. J Bacteriol 173 7625 7635

57. JohnsonLSEddySRPortugalyE 2010 Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11 431

58. SelengutJDHaftDHDavidsenTGanapathyAGwinn-GiglioM 2007 TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res 35 D260 264

59. EswarNEramianDWebbBShenMYSaliA 2008 Protein structure modeling with MODELLER. Methods Mol Biol 426 145 159

60. KrivovGGShapovalovMVDunbrackRLJr 2009 Improved prediction of protein side-chain conformations with SCWRL4. Proteins 77 778 795

61. LernerMGCarlsonHA 2006 APBS plugin for PyMOL Ann Arbor, MI University of Michigan

62. CrooksGEHonGChandoniaJMBrennerSE 2004 WebLogo: a sequence logo generator. Genome Res 14 1188 1190