Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population

English version

Autoři: Sarah M. Cossey ^aff001; Yuen-Tsu Nicco Yu ^aff001; Laura Cossu ^aff002; Gregory J. Velicer ^aff001
Působiště autorů: Institute for Integrative Biology, Department of Environmental Systems Science, ETH Zürich, Switzerland ^aff001; Department of Environmental Microbiology, Eawag, Switzerland ^aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224817

Souhrn

In some species of myxobacteria, adjacent cells sufficiently similar at the adhesin protein TraA can exchange components of their outer membranes. The primary benefits of such outer membrane exchange (OME) in natural populations are unclear, but in some OME interactions, transferred OM content can include SitA toxins that kill OME participants lacking an appropriate immunity gene. Such OME-dependent toxin transfer across Myxococcus xanthus strains that differ only in their sitBAI toxin/antitoxin cassette can mediate inter-strain killing and generate colony-merger incompatibilities (CMIs)–inter-colony border phenotypes between distinct genotypes that differ from respective self-self colony interfaces. Here we ask whether OME-dependent toxin transfer is a common cause of prevalent CMIs and antagonisms between M. xanthus natural isolates identical at TraA. We disrupted traA in eleven isolates from a cm-scale soil population and assayed whether traA disruption eliminated or reduced CMIs between swarming colonies or antagonisms between strains in mixed cultures. Among 33 isolate pairs identical at traA that form clear CMIs, in no case did functional disruption of traA in one partner detectably alter CMI phenotypes. Further, traA disruption did not alleviate strong antagonisms observed during starvation-induced fruiting-body development in seven pairs of strains identical at traA. Collectively, our results suggest that most mechanisms of interference competition and inter-colony kin discrimination in natural populations of myxobacteria do not require OME. Finally, our experiments also indicate that several closely related laboratory reference strains kill some natural isolates by toxins delivered by a shared, OME-independent type VI secretion system (T6SS), suggesting that some antagonisms between sympatric natural isolates may also involve T6SS toxins.

Klíčová slova:

Phenotypes – Secretion systems – Outer membrane proteins – Plasmid construction – Toxins – Gene amplification – Animal sociality – Pure culture

Zdroje

1. Rendueles O, Zee PC, Dinkelacker I, Amherd M, Wielgoss S, Velicer GJ. Rapid and widespread de novo evolution of kin discrimination. Proc Natl Acad Sci USA. 2015;112(29):9076–81. doi: 10.1073/pnas.1502251112 26150498

2. Strassmann JE, Gilbert OM, Queller DC. Kin Discrimination and Cooperation in Microbes. Annu Rev Microbiol. 2011;65:349–67. doi: 10.1146/annurev.micro.112408.134109 21682642

3. Wielgoss S, Fiegna F, Rendueles O, Yu YN, Velicer GJ. Kin discrimination and outer membrane exchange in Myxococcus xanthus: A comparative analysis among natural isolates. Mol Ecol. 2018;27(15):3146–58. doi: 10.1111/mec.14773 29924883

4. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA. Contact-dependent inhibition of growth in Escherichia coli. Science. 2005;309(5738):1245–8. doi: 10.1126/science.1115109 16109881

5. Hawlena H, Bashey F, Mendes-Soares H, Lively CM. Spiteful Interactions in a natural population of the bacterium Xenorhabdus bovienii. Am Nat. 2010;175(3):374–81. doi: 10.1086/650375 20095826

6. Gilbert OM, Foster KR, Mehdiabadi NJ, Strassmann JE, Queller DC. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc Natl Acad Sci USA. 2007;104(21):8913–7. doi: 10.1073/pnas.0702723104 17496139

7. Hamilton WD. The genetical evolution of social behaviour. I. J Theor Biol. 1964;7(1):1–16. doi: 10.1016/0022-5193(64)90038-4 5875341

8. West SA, Griffin AS, Gardner A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol. 2007;20(2):415–32. doi: 10.1111/j.1420-9101.2006.01258.x 17305808

9. Gardner A, West SA, Buckling A. Bacteriocins, spite and virulence. Proc Biol Sci. 2004;271(1547):1529–35. doi: 10.1098/rspb.2004.2756 15306326

10. Ho HI, Hirose S, Kuspa A, Shaulsky G. Kin Recognition Protects Cooperators against Cheaters. Curr Biol. 2013;23(16):1590–5. doi: 10.1016/j.cub.2013.06.049 23910661

11. Mehdiabadi NJ, Jack CN, Farnham TT, Platt TG, Kalla SE, Shaulsky G, et al. Social evolution: kin preference in a social microbe. Nature. 2006;442(7105):881–2. doi: 10.1038/442881a 16929288

12. Beecher MD, Beecher IM, Hahn S. Parent-Offspring Recognition in Bank Swallows (Riparia-Riparia) .2. Development and Acoustic Basis. Anim Beh. 1981;29(Feb):95–&.

13. Breed MD, Williams KR, Fewell JH. Comb wax mediates the acquisition of nest-mate recognition cues in honey bees. Proc Natl Acad Sci USA. 1988;85(22):8766–9. doi: 10.1073/pnas.85.22.8766 16593995

14. Dietemann V, Liebig J, Holldobler B, Peeters C. Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant Myrmecia gulosa. Behav Ecol Sociobiol. 2005;58(5):486–96.

15. Komdeur J, Hatchwell BJ. Kin recognition: function and mechanism in avian societies. Trends Ecol Evol. 1999;14(6):237–41. doi: 10.1016/s0169-5347(98)01573-0 10354628

16. Peeters C, Monnin T, Malosse C. Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B. 1999;266(1426):1323–7.

17. Nair RR, Fiegna F, Velicer GJ. Indirect evolution of social fitness inequalities and facultative social exploitation. Proc R Soc B. 2018;285(1875).

18. Dienes L. Reproductive Processes in Proteus Cultures. Proc Soc Exp Biol Med. 1946;63(2):265–70. doi: 10.3181/00379727-63-15570 20277719

19. Vos M, Velicer GJ. Social Conflict in Centimeter and Global-Scale Populations of the Bacterium Myxococcus xanthus. Curr Biol. 2009;19(20):1763–7. doi: 10.1016/j.cub.2009.08.061 19879146

20. Stefanic P, Kraigher B, Lyons NA, Kolter R, Mandic-Mulec I. Kin discrimination between sympatric Bacillus subtilis isolates. Proc Natl Acad Sci USA. 2015;112(45):14042–7. doi: 10.1073/pnas.1512671112 26438858

21. Munson EL, Pfaller MA, Doern GV. Modification of dienes mutual inhibition test for epidemiological characterization of Pseudomonas aeruginosa isolates. J Clin Microbiol. 2002;40(11):4285–8. doi: 10.1128/JCM.40.11.4285-4288.2002 12409411

22. Alteri CJ, Himpsl SD, Pickens SR, Lindner JR, Zora JS, Miller JE, et al. Multicellular Bacteria Deploy the Type VI Secretion System to Preemptively Strike Neighboring Cells. PLoS Pathog. 2013;9(9).

23. Gibbs KA, Urbanowski ML, Greenberg EP. Genetic determinants of self identity and social recognition in bacteria. Science. 2008;321(5886):256–9. doi: 10.1126/science.1160033 18621670

24. Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. MBio. 2013;4(4).

25. Lyons NA, Kraigher B, Stefanic P, Mandic-Mulec I, Kolter R. A Combinatorial Kin Discrimination System in Bacillus subtilis. Curr Biol. 2016;26(6):733–42. doi: 10.1016/j.cub.2016.01.032 26923784

26. Vassallo CN, Cao PB, Conklin A, Finkelstein H, Heyer CS, Wall D. Infectious polymorphic toxins delivered by outer membrane exchange discriminate kin in myxobacteria. Elife. 2017;6.

27. Patra P, Vassallo CN, Wall D, Igoshin OA. Mechanism of Kin-Discriminatory Demarcation Line Formation between Colonies of Swarming Bacteria. Biophys J. 2017;113(11):2477–2486. doi: 10.1016/j.bpj.2017.09.020 29212001

28. Gong Y, Zhang Z, Liu Y, Zhou XW, Anwar MN, Li ZS, et al. A nuclease-toxin and immunity system for kin discrimination in Myxococcus xanthus. Environ Microbiol. 2018;20(7):2552–67. doi: 10.1111/1462-2920.14282 29806725

29. Hodgkin J, Kaiser D. Genetics of Gliding Motility in Myxococcus xanthus (Myxobacterales) - 2 Gene Systems Control Movement. Mol Gen Genet. 1979;171(2):177–91.

30. Kaiser D. Signaling in myxobacteria. Annu Rev Microbiol. 2004;58:75–98. doi: 10.1146/annurev.micro.58.030603.123620 15487930

31. Berleman JE, Kirby JR. Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev. 2009;33(5):942–57. doi: 10.1111/j.1574-6976.2009.00185.x 19519767

32. Wireman JW, Dworkin M. Developmentally Induced Autolysis during Fruiting Body Formation by Myxococcus xanthus. J Bacteriol. 1977;129(2):796–802.

33. Nudleman E, Wall D, Kaiser D. Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science. 2005;309(5731):125–7. doi: 10.1126/science.1112440 15994555

34. Pathak DT, Wei XM, Bucuvalas A, Haft DH, Gerloff DL, Wall D. Cell Contact-Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism. PLoS Genet. 2012;8(4):160–71.

35. Nudleman E, Wall D, Kaiser D. Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol. 2006;60(1):16–29. doi: 10.1111/j.1365-2958.2006.05095.x 16556217

36. Pathak DT, Wei XM, Dey A, Wall D. Molecular Recognition by a Polymorphic Cell Surface Receptor Governs Cooperative Behaviors in Bacteria. PLoS Genet. 2013;9(11).

37. Wei X, Pathak DT, Wall D. Heterologous protein transfer within structured myxobacteria biofilms. Mol Microbiol. 2011;81(2):315–26. doi: 10.1111/j.1365-2958.2011.07710.x 21635581

38. Cao P, Wei X, Awal RP, Muller R, Wall D. A Highly Polymorphic Receptor Governs Many Distinct Self-Recognition Types within the Myxococcales Order. MBio. 2019;10(1).

39. Vassallo C, Pathak DT, Cao PB, Zuckerman DM, Hoiczyk E, Wall D. Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria. Proc Natl Acad Sci USA. 2015;112(22):E2939–E46. doi: 10.1073/pnas.1503553112 26038568

40. Cao P, Wall D. Self-identity reprogrammed by a single residue switch in a cell surface receptor of a social bacterium. Proc Natl Acad Sci USA. 2017;114(14):3732–7. doi: 10.1073/pnas.1700315114 28320967

41. Cao PB, Dey A, Vassallo CN, Wall D. How Myxobacteria Cooperate. J Mol Biol. 2015;427(23):3709–21. doi: 10.1016/j.jmb.2015.07.022 26254571

42. Vassallo CN, Wall D. Tissue repair in myxobacteria: A cooperative strategy to heal cellular damage. Bioessays. 2016;38(4):306–15. doi: 10.1002/bies.201500132 26898360

43. Wall D. Molecular recognition in myxobacterial outer membrane exchange: functional, social and evolutionary implications. Mol Microbiol. 2014;91(2):209–20. doi: 10.1111/mmi.12450 24261719

44. Wall D. Kin Recognition in Bacteria. Annu Rev Microbiol. 2016;70:143–60. doi: 10.1146/annurev-micro-102215-095325 27359217

45. Ruhe ZC, Low DA, Hayes CS. Bacterial contact-dependent growth inhibition. Trends Microbiol. 2013;21(5):230–7. doi: 10.1016/j.tim.2013.02.003 23473845

46. Dey A, Vassallo CN, Conklin AC, Pathak DT, Troselj V, Wall D. Sibling Rivalry in Myxococcus xanthus Is Mediated by Kin Recognition and a Polyploid Prophage. J Bacteriol. 2016;198(6):994–1004. doi: 10.1128/JB.00964-15 26787762

47. Wielgoss S, Didelot X, Chaudhuri RR, Liu X, Weedall GD, Velicer GJ, et al. A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. ISME J. 2016;10(10):2468–77. doi: 10.1038/ismej.2016.34 27046334

48. Rendueles O, Amherd M, Velicer GJ. Positively Frequency-Dependent Interference Competition Maintains Diversity and Pervades a Natural Population of Cooperative Microbes. Curr Biol. 2015;25(13):1673–81. doi: 10.1016/j.cub.2015.04.057 26051889

49. Vos M, Velicer GJ. Isolation by distance in the spore-forming soil bacterium Myxococcus xanthus. Curr Biol. 2008;18(5):386–391. doi: 10.1016/j.cub.2008.02.050 18328701

50. Kaiser D. Social Gliding Is Correlated with the Presence of Pili in Myxococcus xanthus. Proc Natl Acad Sci USA. 1979;76(11):5952–6. doi: 10.1073/pnas.76.11.5952 42906

51. Velicer GJ, Raddatz G, Keller H, Deiss S, Lanz C, Dinkelacker I, et al. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc Natl Acad Sci USA. 2006;103(21):8107–12. doi: 10.1073/pnas.0510740103 16707573

52. Velicer GJ, Kroos L, Lenski RE. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci USA. 1998;95(21):12376–80. doi: 10.1073/pnas.95.21.12376 9770494

53. Wall D, Kolenbrander PE, Kaiser D. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J Bacteriol. 1999;181(1):24–33. 9864308

54. Vos M, Velicer GJ. Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl Environ Microbiol. 2006;72(5):3615–25. doi: 10.1128/AEM.72.5.3615-3625.2006 16672510

55. Troselj V, Treuner-Lange A, Sogaard-Andersen L, Wall D. Physiological Heterogeneity Triggers Sibling Conflict Mediated by the Type VI Secretion System in an Aggregative Multicellular Bacterium. MBio. 2018;9(1).

56. Rodriguez AM, Spormann AM. Genetic and molecular analysis of cglB, a gene essential for single-cell gliding in Myxococcus xanthus. J Bacteriol. 1999;181(14):4381–90. 10400597

57. Bretscher AP, Kaiser D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J Bacteriol. 1978;133(2):763–8. 415048

58. Muller S, Willett JW, Bahr SM, Scott JC, Wilson JM, Darnell CL, et al. Draft Genome of a Type 4 Pilus Defective Myxococcus xanthus Strain, DZF1. Genome Announc. 2013;1(3).

59. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, Trinidad RR, et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe. 2010;7(1):25–37. doi: 10.1016/j.chom.2009.12.007 20114026

60. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature. 2011;475(7356):343–7. doi: 10.1038/nature10244 21776080

61. Russell AB, Peterson SB, Mougous JD. Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol. 2014;12(2):137–48. doi: 10.1038/nrmicro3185 24384601

62. Konovalova A, Petters T, Sogaard-Andersen L. Extracellular biology of Myxococcus xanthus. FEMS Microbiol Rev. 2010;34(2):89–106. doi: 10.1111/j.1574-6976.2009.00194.x 19895646

63. Cianfanelli FR, Monlezun L, Coulthurst SJ. Aim, load, fire: The Type VI secretion system, a bacterial nanoweapon. Trends Microbiol. 2016;24(1):51–62. doi: 10.1016/j.tim.2015.10.005 26549582

64. Zoued A, Brunet YR, Durand E, Aschtgen MS, Logger L, Douzi B, et al. Architecture and assembly of the Type VI secretion system. Biochim Biophys Acta. 2014;1843(8):1664–73. doi: 10.1016/j.bbamcr.2014.03.018 24681160

65. Kraemer SA, Wielgoss S, Fiegna F, Velicer GJ. The biogeography of kin discrimination across microbial neighbourhoods. Mol Ecol. 2016;25(19):4875–88. doi: 10.1111/mec.13803 27540705

66. Krug D, Zurek G, Revermann O, Vos M, Velicer GJ, Muller R. Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity. Appl Environ Microbiol. 2008;74(10):3058–68. doi: 10.1128/AEM.02863-07 18378661

67. McCurdy HD Jr., MacRae TH. Xanthacin. A bacteriocin of Myxococcus xanthus fb. Can J Microbiol. 1974;20(2):131–5. doi: 10.1139/m74-021 4132608

68. Sudo S, Dworkin M. Bacteriolytic Enzymes Produced by Myxococcus xanthus. J Bacteriol. 1972;110(1):236–245. 4622898

69. Davies J, Spiegelman GB, Yim G. The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol. 2006;9(5):445–53. doi: 10.1016/j.mib.2006.08.006 16942902

70. Keane R, Berleman J. The predatory life cycle of Myxococcus xanthus. Microbiology. 2016;162(1):1–11. doi: 10.1099/mic.0.000208 26518442

71. Smith DR, Dworkin M. Territorial interactions between two Myxococcus Species. J Bacteriol. 1994;176(4):1201–5. doi: 10.1128/jb.176.4.1201-1205.1994 8106334

72. Evans AGL, Davey HM, Cookson A, Currinn H, Cooke-Fox G, Stanczyk PJ, et al. Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo. Microbiology. 2012;158:2742–52. doi: 10.1099/mic.0.060343-0 22977088

73. Berleman JE, Allen S, Danielewicz MA, Remis JP, Gorur A, Cunha J, et al. The lethal cargo of Myxococcus xanthus outer membrane vesicles. Front Microbiol. 2014;5:474. doi: 10.3389/fmicb.2014.00474 25250022

74. Kahnt J, Aguiluz K, Koch J, Treuner-Lange A, Konovalova A, Huntley S, et al. 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. 2010;9(10):5197–208. doi: 10.1021/pr1004983 20687614

75. Kadurugamuwa JL, Beveridge TJ. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: Conceptually new antibiotics. J Bacteriol. 1996;178(10):2767–74. doi: 10.1128/jb.178.10.2767-2774.1996 8631663

76. Kulp A, Kuehn MJ. Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles. Ann Rev Microbiol. 2010;64:163–84.

77. Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T, Kostiuk B, et al. The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nat Commun. 2014;5:3549. doi: 10.1038/ncomms4549 24686479

78. Jamet A, Nassif X. New Players in the Toxin Field: Polymorphic Toxin Systems in Bacteria. MBio. 2015;6(3).

79. Makarova K, Wolf Y, Karamycheva S, Zhang D, Aravind L, Koonin E. Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts. MBio. 2019;10(3).

Kin discrimination and outer membrane exchange in Myxococcus xanthus: Experimental analysis of a natural population

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz