Kind Discrimination and Competitive Exclusion Mediated by Contact-Dependent Growth Inhibition Systems Shape Biofilm Community Structure

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Contact-Dependent Growth Inhibition (CDI) systems are highly diverse interbacterial competition systems that bacteria use to kill neighboring bacteria upon cell-cell contact. In Burkholderia species, BcpA is the large exoprotein responsible for mediating CDI. BcpI proteins provide immunity against auto-inhibition. Diversity of CDI systems exists within the toxic C-terminus of BcpA proteins (called the BcpA-CT) and BcpI proteins. In addition to mediating interbacterial competition in Burkholderia thailandensis, BcpA also mediates biofilm formation, suggesting CDI system proteins play a cooperative role in nature. However, the roles of CDI system-mediated interbacterial competition and of CDI system diversity in nature are unclear. We constructed B. thailandensis strains that produced different BcpA-CT and BcpI proteins. Bacteria participated in CDI during biofilm formation, resulting in biofilm structures that were segregated by CDI system protein types. Furthermore, competition via CDI allowed bacteria in a pre-established biofilm community producing one set of CDI system proteins to exclude bacteria producing a different set of CDI system proteins from entering the community. Our data imply, therefore, that CDI-mediated competition and CDI system diversity function as a mechanism for self-recognition during the development of microbial communities.

Vyšlo v časopise: Kind Discrimination and Competitive Exclusion Mediated by Contact-Dependent Growth Inhibition Systems Shape Biofilm Community Structure. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004076
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004076

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Zdroje

1. AokiSK, PammaR, HerndayAD, BickhamJE, BraatenBA, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245–1248 doi:10.1126/science.1115109

2. AokiSK, DinerEJ, de RoodenbekeCT, BurgessBR, PooleSJ, et al. (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468: 439–442 doi:10.1038/nature09490

3. WebbJS, NikolakakisKC, WillettJLE, AokiSK, HayesCS, et al. (2013) Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLoS ONE 8: e57609 doi:10.1371/journal.pone.0057609

4. PooleSJ, DinerEJ, AokiSK, BraatenBA, t'Kint de RoodenbekeC, et al. (2011) Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7: e1002217 doi:10.1371/journal.pgen.1002217

5. NikolakakisK, AmberS, WilburJS, DinerEJ, AokiSK, et al. (2012) The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems. Mol Microbiol 84: 516–529 doi:10.1111/j.1365-2958.2012.08039.x

6. AndersonMS, GarciaEC, CotterPA (2012) The Burkholderia bcpAIOB genes define unique classes of two-partner secretion and contact dependent growth inhibition systems. PLoS Genet 8: e1002877 doi:10.1371/journal.pgen.1002877

7. LipumaJJ (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23: 299–323 doi:10.1128/CMR.00068-09

8. DanceDA (2000) Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Trop 74: 159–168.

9. GlassMB, GeeJE, SteigerwaltAG, CavuotiD, BartonT, et al. (2006) Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. J Clin Microbiol 44: 4601–4604 doi:10.1128/JCM.01585-06

10. WiersingaWJ, CurrieBJ, PeacockSJ (2012) Melioidosis. N Engl J Med 367: 1035–1044 doi:10.1056/NEJMra1204699

11. WiersingaWJ, van der PollT, WhiteNJ, DayNP, PeacockSJ (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272–282 doi:10.1038/nrmicro1385

12. ChengAC, CurrieBJ (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416 doi:10.1128/CMR.18.2.383-416.2005

13. GarciaEC, AndersonMS, HagarJA, CotterPA (2013) Burkholderia BcpA mediates biofilm formation independently of interbacterial contact dependent growth inhibition. Mol Microbiol 89(6): 1213–25 doi:10.1111/mmi.12339

14. TuanyokA, LeademBR, AuerbachRK, Beckstrom-SternbergSM, Beckstrom-SternbergJS, et al. (2008) Genomic islands from five strains of Burkholderia pseudomallei. BMC Genomics 9: 566 doi:10.1186/1471-2164-9-566

15. LiguoriAP, WarringtonSD, GintherJL, PearsonT, BowersJ, et al. (2011) Diversity of 16S-23S rDNA internal transcribed spacer (ITS) reveals phylogenetic relationships in Burkholderia pseudomallei and its near-neighbors. PLoS ONE 6: e29323 doi:10.1371/journal.pone.0029323

16. XavierJB, FosterKR (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104: 876–881 doi:10.1073/pnas.0607651104

17. AsallyM, KittisopikulM, RuéP, DuY, HuZ, et al. (2012) Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci USA 109: 18891–18896 doi:10.1073/pnas.1212429109

18. LopezD, VlamakisH, LosickR, KolterR (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74: 609–618 doi:10.1111/j.1365-2958.2009.06882.x

19. ThomasVC, HiromasaY, HarmsN, ThurlowL, TomichJ, et al. (2009) A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol Microbiol 72: 1022–1036 doi:10.1111/j.1365-2958.2009.06703.x

20. VlamakisH, ChaiY, BeauregardP, LosickR, KolterR (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11: 157–168 Available: http://www.nature.com/doifinder/10.1038/nrmicro2960.

21. StrassmannJE, GilbertOM, QuellerDC (2011) Kin discrimination and cooperation in microbes. Annu Rev Microbiol 65: 349–367 doi:10.1146/annurev.micro.112408.134109

22. LeRouxM, De LeonJA, KuwadaNJ, RussellAB, Pinto-SantiniD, et al. (2012) Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc Natl Acad Sci USA 109: 19804–19809 doi:10.1073/pnas.1213963109

23. BaslerM, HoBT, MekalanosJJ (2013) Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152: 884–894 doi:10.1016/j.cell.2013.01.042

24. WenrenLM, SullivanNL, CardarelliL, SepterAN, GibbsKA (2013) Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 4 doi:10.1128/mBio.00374-13

25. AlteriCJ, HimpslSD, PickensSR, LindnerJR, ZoraJS, et al. (2013) Multicellular Bacteria Deploy the Type VI Secretion System to Preemptively Strike Neighboring Cells. PLoS Pathog 9: e1003608 doi:10.1371/journal.ppat.1003608

26. BrettPJ, DeShazerD, WoodsDE (1998) Note: Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. International Journal of Systematic Bacteriology 48: 317–320 doi:10.1099/00207713-48-1-317

27. LopezCM, RhollDA, TrunckLA, SchweizerHP (2009) Versatile Dual-Technology System for Markerless Allele Replacement in Burkholderia pseudomallei. Applied and Environmental Microbiology 75: 6496–6503 doi:10.1128/AEM.01669-09

28. ThongdeeM, GallagherLA, SchellM, DharakulT, SongsivilaiS, et al. (2008) Targeted mutagenesis of Burkholderia thailandensis and Burkholderia pseudomallei through natural transformation of PCR fragments. Applied and Environmental Microbiology 74: 2985–2989 Available: http://aem.asm.org/content/74/10/2985.long.

29. ChoiK-H, DeShazerD, SchweizerHP (2006) mini-Tn7 insertion in bacteria with multiple glmS-linked attTn7 sites: example Burkholderia mallei ATCC 23344. Nat Protoc 1: 162–169 doi:10.1038/nprot.2006.25

30. NorrisMH, KangY, WilcoxB, HoangTT (2010) Stable, Site-Specific Fluorescent Tagging Constructs Optimized for Burkholderia Species. Applied and Environmental Microbiology 76: 7635–7640 doi:10.1128/AEM.01188-10

31. HeydornA, NielsenAT, HentzerM, SternbergC, GivskovM, et al. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology (Reading, Engl.) 146(Pt 10): 2395–2407.