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Molecular Recognition by a Polymorphic Cell Surface Receptor Governs Cooperative Behaviors in Bacteria


Cell-cell recognition is a fundamental process that allows cells to coordinate multicellular behaviors. Some microbes, such as myxobacteria, build multicellular fruiting bodies from free-living cells. However, how bacterial cells recognize each other by contact is poorly understood. Here we show that myxobacteria engage in recognition through interactions between TraA cell surface receptors, which leads to the fusion and exchange of outer membrane (OM) components. OM exchange is shown to be selective among 17 environmental isolates, as exchange partners parsed into five major recognition groups. TraA is the determinant of molecular specificity because: (i) exchange partners correlated with sequence conservation within its polymorphic PA14-like domain and (ii) traA allele replacements predictably changed partner specificity. Swapping traA alleles also reprogrammed social interactions among strains, including the regulation of motility and conferred immunity from inter-strain killing. We suggest that TraA helps guide the transition of single cells into a coherent bacterial community, by a proposed mechanism that is analogous to mitochondrial fusion and fission cycling that mixes contents to establish a homogenous population. In evolutionary terms, traA functions as a rare greenbeard gene that recognizes others that bear the same allele to confer beneficial treatment.


Vyšlo v časopise: Molecular Recognition by a Polymorphic Cell Surface Receptor Governs Cooperative Behaviors in Bacteria. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003891
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003891

Souhrn

Cell-cell recognition is a fundamental process that allows cells to coordinate multicellular behaviors. Some microbes, such as myxobacteria, build multicellular fruiting bodies from free-living cells. However, how bacterial cells recognize each other by contact is poorly understood. Here we show that myxobacteria engage in recognition through interactions between TraA cell surface receptors, which leads to the fusion and exchange of outer membrane (OM) components. OM exchange is shown to be selective among 17 environmental isolates, as exchange partners parsed into five major recognition groups. TraA is the determinant of molecular specificity because: (i) exchange partners correlated with sequence conservation within its polymorphic PA14-like domain and (ii) traA allele replacements predictably changed partner specificity. Swapping traA alleles also reprogrammed social interactions among strains, including the regulation of motility and conferred immunity from inter-strain killing. We suggest that TraA helps guide the transition of single cells into a coherent bacterial community, by a proposed mechanism that is analogous to mitochondrial fusion and fission cycling that mixes contents to establish a homogenous population. In evolutionary terms, traA functions as a rare greenbeard gene that recognizes others that bear the same allele to confer beneficial treatment.


Zdroje

1. StrassmannJE, GilbertOM, QuellerDC (2011) Kin discrimination and cooperation in microbes. Annu Rev Microbiol 65: 349–367.

2. BoehmT (2006) Quality control in self/nonself discrimination. Cell 125: 845–858.

3. RosengartenRD, NicotraML (2011) Model systems of invertebrate allorecognition. Curr Biol 21: R82–92.

4. JacobiCA, AssmusB, ReichenbachH, StackebrandtE (1997) Molecular evidence for association between the sphingobacterium-like organism “Candidatus comitans” and the myxobacterium Chondromyces crocatus. Appl Environ Microbiol 63: 719–723.

5. PathakDT, WeiX, WallD (2012) Myxobacterial tools for social interactions. Res Microbiol 163: 579–591.

6. MendesR, KruijtM, de BruijnI, DekkersE, van der VoortM, et al. (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097–1100.

7. PathakDT, WeiX, BucuvalasA, HaftDH, GerloffDL, et al. (2012) Cell contact-dependent outer membrane exchange in myxobacteria: Genetic determinants and mechanism. PLoS Genet 8: e1002626.

8. WeiX, PathakDT, WallD (2011) Heterologous protein transfer within structured myxobacteria biofilms. Mol Microbiol 81: 315–326.

9. NudlemanE, WallD, KaiserD (2005) Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309: 125–127.

10. HodgkinJ, KaiserD (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A 74: 2938–2942.

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

12. WallD, WuSS, KaiserD (1998) Contact stimulation of Tgl and type IV pili in Myxococcus xanthus. J Bacteriol 180: 759–761.

13. GoossensK, WillaertR (2010) Flocculation protein structure and cell-cell adhesion mechanism in Saccharomyces cerevisiae. Biotechnol Lett 32: 1571–1585.

14. WallD, KaiserD (1998) Alignment enhances the cell-to-cell transfer of pilus phenotype. Proc Natl Acad Sci U S A 95: 3054–3058.

15. PathakDT, WallD (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.

16. XiaoY, WeiX, EbrightR, WallD (2011) Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193: 4626–4633.

17. Rosenberg E, Varon M (1984) Antibotics and lytic enzymes. In: Rosenberg E, editor. Myxobacteria: Development and cell interactions. New York: Springer-Verlag. pp. 109–125.

18. SmithDR, DworkinM (1994) Territorial interactions between two Myxococcus species. J Bacteriol 176: 1201–1205.

19. HirschHJ (1977) Bacteriocins from Myxococcus fulvus (Myxobacterales). Arch Microbiol 115: 45–49.

20. RigdenDJ, MelloLV, GalperinMY (2004) The PA14 domain, a conserved all-beta domain in bacterial toxins, enzymes, adhesins and signaling molecules. Trends Biochem Sci 29: 335–339.

21. van der WoudeMW, HendersonIR (2008) Regulation and function of Ag43 (flu). Annual Review of Microbiology 62: 153–169.

22. KolenbranderPE, AndersenRN, BlehertDS, EglandPG, FosterJS, et al. (2002) Communication among oral bacteria. Microbiol Mol Biol Rev 66: 486–505.

23. WenrenLM, SullivanNL, CardarelliL, SepterAN, GibbsKA (2013) Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. MBio 4.

24. RuheZC, WallaceAB, LowDA, HayesCS (2013) Receptor polymorphism restricts contact-dependent growth inhibition to members of the same species. MBio 4.

25. ChanDC (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Ann Rev Genet 46: 265–287.

26. YouleRJ, van der BliekAM (2012) Mitochondrial fission, fusion, and stress. Science 337: 1062–1065.

27. ZhangD, de SouzaRF, AnantharamanV, IyerLM, AravindL (2012) Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7: 18.

28. VosM, VelicerGJ (2006) Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol 72: 3615–3625.

29. VosM, VelicerGJ (2009) Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus. Curr Biol 19: 1763–1767.

30. GillRE, CullMG, FlyS (1988) Genetic identification and cloning of a gene required for developmental cell interactions in Myxococcus xanthus. J Bacteriol 170: 5279–5288.

31. KoskiniemiS, LamoureuxJG, NikolakakisKC, T'Kint de RoodenbekeC, KaplanMD, et al. (2013) Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci U S A 110: 7032–7037.

32. WestSA, GriffinAS, GardnerA, DiggleSP (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4: 597–607.

33. Dawkins R (1976) The Selfish Gene. Oxford, UK: Oxford University Press.

34. HamiltonWD (1964) The genetical evolution of social behaviour. II. J Theor Biol 7: 17–52.

35. HaigD (1996) Gestational drive and the green-bearded placenta. Proc Natl Acad Sci U S A 93: 6547–6551.

36. HiroseS, BenabentosR, HoHI, KuspaA, ShaulskyG (2011) Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333: 467–470.

37. BenabentosR, HiroseS, SucgangR, CurkT, KatohM, et al. (2009) Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19: 567–572.

38. SmukallaS, CaldaraM, PochetN, BeauvaisA, GuadagniniS, et al. (2008) FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135: 726–737.

39. Haig D (1997) The social gene. In: Krebs JR, Davies NB, editors. Behavioural ecology: An evolutionary approach. 4th ed. Cambridge, Great Britain: Wiley-Blackwell pp. 284–304.

40. BoyntonTO, McMurryJL, ShimketsLJ (2013) Characterization of Myxococcus xanthus MazF and implications for a new point of regulation. Mol Microbiol 87: 1267–1276.

41. XiaoY, GerthK, MullerR, WallD (2012) Myxobacterium-produced antibiotic TA (myxovirescin) inhibits type II signal peptidase. Antimicrob Agents Chemother 56: 2014–2021.

42. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.

43. DarribaD, TaboadaGL, DoalloR, PosadaD (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164–1165.

44. HuelsenbeckJP, RonquistF (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.

45. TraulsenA, NowakMA (2006) Evolution of cooperation by multilevel selection. Proc Natl Acad Sci U S A 103: 10952–10955.

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


2013 Číslo 11
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