The Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems
Microbes have evolved many strategies to adapt to changes in environmental conditions and population structures, including cooperation and competition. One apparently competitive mechanism is contact dependent growth inhibition (CDI). Identified in Escherichia coli, CDI is mediated by Two–Partner Secretion (TPS) pathway proteins, CdiA and CdiB. Upon cell contact, the toxic C-terminus of the TpsA family member CdiA, called the CdiA-CT, inhibits the growth of CDI− bacteria. CDI+ bacteria are protected from autoinhibition by an immunity protein, CdiI. Bioinformatic analyses indicate that CDI systems are widespread amongst α, β, and γ proteobacteria and that the CdiA-CTs and CdiI proteins are highly variable. CdiI proteins protect against CDI in an allele-specific manner. Here we identify predicted CDI system-encoding loci in species of Burkholderia, Ralstonia and Cupriavidus, named bcpAIOB, that are distinguished from previously-described CDI systems by gene order and the presence of a small ORF, bcpO, located 5′ to the gene encoding the TpsB family member. A requirement for bcpO in function of BcpA (the TpsA family member) was demonstrated, indicating that bcpAIOB define a novel class of TPS system. Using fluorescence microscopy and flow cytometry, we show that these genes are expressed in a probabilistic manner during culture of Burkholderia thailandensis in liquid medium. The bcpAIOB genes and extracellular DNA were required for autoaggregation and adherence to an abiotic surface, suggesting that CDI is required for biofilm formation, an activity not previously attributed to CDI. By contrast to what has been observed in E. coli, the B. thailandensis bcpAIOB genes only mediated interbacterial competition on a solid surface. Competition occurred in a defined spatiotemporal manner and was abrogated by allele-specific immunity. Our data indicate that the bcpAIOB genes encode distinct classes of CDI and TPS systems that appear to function in sociomicrobiological community development.
Vyšlo v časopise:
The Genes Define Unique Classes of Two-Partner Secretion and Contact Dependent Growth Inhibition Systems. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002877
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002877
Souhrn
Microbes have evolved many strategies to adapt to changes in environmental conditions and population structures, including cooperation and competition. One apparently competitive mechanism is contact dependent growth inhibition (CDI). Identified in Escherichia coli, CDI is mediated by Two–Partner Secretion (TPS) pathway proteins, CdiA and CdiB. Upon cell contact, the toxic C-terminus of the TpsA family member CdiA, called the CdiA-CT, inhibits the growth of CDI− bacteria. CDI+ bacteria are protected from autoinhibition by an immunity protein, CdiI. Bioinformatic analyses indicate that CDI systems are widespread amongst α, β, and γ proteobacteria and that the CdiA-CTs and CdiI proteins are highly variable. CdiI proteins protect against CDI in an allele-specific manner. Here we identify predicted CDI system-encoding loci in species of Burkholderia, Ralstonia and Cupriavidus, named bcpAIOB, that are distinguished from previously-described CDI systems by gene order and the presence of a small ORF, bcpO, located 5′ to the gene encoding the TpsB family member. A requirement for bcpO in function of BcpA (the TpsA family member) was demonstrated, indicating that bcpAIOB define a novel class of TPS system. Using fluorescence microscopy and flow cytometry, we show that these genes are expressed in a probabilistic manner during culture of Burkholderia thailandensis in liquid medium. The bcpAIOB genes and extracellular DNA were required for autoaggregation and adherence to an abiotic surface, suggesting that CDI is required for biofilm formation, an activity not previously attributed to CDI. By contrast to what has been observed in E. coli, the B. thailandensis bcpAIOB genes only mediated interbacterial competition on a solid surface. Competition occurred in a defined spatiotemporal manner and was abrogated by allele-specific immunity. Our data indicate that the bcpAIOB genes encode distinct classes of CDI and TPS systems that appear to function in sociomicrobiological community development.
Zdroje
1. AokiSK, PammaR, HerndayAD, BickhamJE, BraatenBA, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245–1248.
2. MazarJ, CotterPA (2007) New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15: 508–515.
3. HendersonIR, Navarro-GarciaF, DesvauxM, FernandezRC, Ala'AldeenD (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692–744.
4. 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.
5. 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.
6. AokiSK, MalinverniJC, JacobyK, ThomasB, PammaR, et al. (2008) Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70: 323–340.
7. WuthiekanunV, SmithMD, DanceDA, WhiteNJ (1995) Isolation of Pseudomonas pseudomallei from soil in north-eastern Thailand. Trans R Soc Trop Med Hyg 89: 41–43.
8. WuthiekanunV, SmithMD, WhiteNJ (1995) Survival of Burkholderia pseudomallei in the absence of nutrients. Trans R Soc Trop Med Hyg 89: 491.
9. DanceDA (2000) Melioidosis as an emerging global problem. Acta Trop 74: 115–119.
10. DaveJ, SpringbettR, PadmoreH, TurnerP, SmithG (1993) Pseudomonas cepacia pseudobacteraemia. J Hosp Infect 23: 72–73.
11. AronoffSC, QuinnFJJr, SternRC (1991) Longitudinal serum IgG response to Pseudomonas cepacia surface antigens in cystic fibrosis. Pediatr Pulmonol 11: 289–293.
12. DanceDA (2002) Melioidosis. Curr Opin Infect Dis 15: 127–132.
13. ChengAC, CurrieBJ (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383–416.
14. BrettPJ, DeShazerD, WoodsDE (1998) Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 48 Pt 1: 317–320.
15. ChaowagulW, WhiteNJ, DanceDA, WattanagoonY, NaigowitP, et al. (1989) Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J Infect Dis 159: 890–899.
16. CurrieBJ, FisherDA, HowardDM, BurrowJN, SelvanayagamS, et al. (2000) The epidemiology of melioidosis in Australia and Papua New Guinea. Acta Trop 74: 121–127.
17. TuanyokA, LeademBR, AuerbachRK, Beckstrom-SternbergSM, Beckstrom-SternbergJS, et al. (2008) Genomic islands from five strains of Burkholderia pseudomallei. BMC Genomics 9: 566.
18. Jacob-DubuissonF, BuisineC, WilleryE, Renauld-MongenieG, LochtC (1997) Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J Bacteriol 179: 775–783.
19. JulioSM, CotterPA (2005) Characterization of the filamentous hemagglutinin-like protein FhaS in Bordetella bronchiseptica. Infect Immun 73: 4960–4971.
20. MontanaroL, PoggiA, VisaiL, RavaioliS, CampocciaD, et al. (2011) Extracellular DNA in biofilms. Int J Artif Organs 34: 824–831.
21. FanE, FiedlerS, Jacob-DubuissonF, MullerM (2011) Two-partner secretion of gram-negative bacteria: A single beta-barrel protein enables transport across the outer membrane. J Biol Chem
22. HaganCL, SilhavyTJ, KahneD (2011) beta-Barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80: 189–210.
23. DupinE, RealC, Glavieux-PardanaudC, VaigotP, Le DouarinNM (2003) Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci U S A 100: 5229–5233.
24. LeeEJ, RussellT, HurleyL, JamesonJL (2005) Pituitary transcription factor-1 induces transient differentiation of adult hepatic stem cells into prolactin-producing cells in vivo. Mol Endocrinol 19: 964–971.
25. MeeksJC, CampbellEL, SummersML, WongFC (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178: 395–403.
26. GrossmanAD (1995) Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet 29: 477–508.
27. SuelGM, Garcia-OjalvoJ, LibermanLM, ElowitzMB (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440: 545–550.
28. SchwarzS, WestTE, BoyerF, ChiangWC, CarlMA, et al. (2010) Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6: e1001068.
29. ThongdeeM, GallagherLA, SchellM, DharakulT, SongsivilaiS, et al. (2008) Targeted mutagenesis of Burkholderia thailandensis and Burkholderia pseudomallei through natural transformation of PCR fragments. Appl Environ Microbiol 74: 2985–2989.
30. HoldenMT, TitballRW, PeacockSJ, Cerdeno-TarragaAM, AtkinsT, et al. (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101: 14240–14245.
31. NikolakakisK, AmberS, WilburJS, DinerEJ, AokiSK, et al. The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems. Mol Microbiol 84: 516–529.
32. LopezCM, RhollDA, TrunckLA, SchweizerHP (2009) Versatile dual-technology system for markerless allele replacement in Burkholderia pseudomallei. Appl Environ Microbiol 75: 6496–6503.
33. ChoiKH, DeShazerD, SchweizerHP (2006) mini-Tn7 insertion in bacteria with multiple glmS-linked attTn7 sites: example Burkholderia mallei ATCC 23344. Nat Protoc 1: 162–169.
34. NorrisMH, KangY, WilcoxB, HoangTT (2010) Stable, site-specific fluorescent tagging constructs optimized for burkholderia species. Appl Environ Microbiol 76: 7635–7640.
35. WilliamsCL, CotterPA (2007) Autoregulation is essential for precise temporal and steady-state regulation by the Bordetella BvgAS phosphorelay. J Bacteriol 189: 1974–1982.
36. CardonaST, ValvanoMA (2005) An expression vector containing a rhamnose-inducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54: 219–228.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 8
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Dissecting the Gene Network of Dietary Restriction to Identify Evolutionarily Conserved Pathways and New Functional Genes
- It's All in the Timing: Too Much E2F Is a Bad Thing
- Variation of Contributes to Dog Breed Skull Diversity
- The PARN Deadenylase Targets a Discrete Set of mRNAs for Decay and Regulates Cell Motility in Mouse Myoblasts