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Lectin-Like Bacteriocins from spp. Utilise D-Rhamnose Containing Lipopolysaccharide as a Cellular Receptor


Lectin-like bacteriocins consist of tandem monocot mannose-binding domains and display a genus-specific killing activity. Here we show that pyocin L1, a novel member of this family from Pseudomonas aeruginosa, targets susceptible strains of this species through recognition of the common polysaccharide antigen (CPA) of P. aeruginosa lipopolysaccharide that is predominantly a homopolymer of d-rhamnose. Structural and biophysical analyses show that recognition of CPA occurs through the C-terminal carbohydrate-binding domain of pyocin L1 and that this interaction is a prerequisite for bactericidal activity. Further to this, we show that the previously described lectin-like bacteriocin putidacin L1 shows a similar carbohydrate-binding specificity, indicating that oligosaccharides containing d-rhamnose and not d-mannose, as was previously thought, are the physiologically relevant ligands for this group of bacteriocins. The widespread inclusion of d-rhamnose in the lipopolysaccharide of members of the genus Pseudomonas explains the unusual genus-specific activity of the lectin-like bacteriocins.


Vyšlo v časopise: Lectin-Like Bacteriocins from spp. Utilise D-Rhamnose Containing Lipopolysaccharide as a Cellular Receptor. PLoS Pathog 10(2): e32767. doi:10.1371/journal.ppat.1003898
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003898

Souhrn

Lectin-like bacteriocins consist of tandem monocot mannose-binding domains and display a genus-specific killing activity. Here we show that pyocin L1, a novel member of this family from Pseudomonas aeruginosa, targets susceptible strains of this species through recognition of the common polysaccharide antigen (CPA) of P. aeruginosa lipopolysaccharide that is predominantly a homopolymer of d-rhamnose. Structural and biophysical analyses show that recognition of CPA occurs through the C-terminal carbohydrate-binding domain of pyocin L1 and that this interaction is a prerequisite for bactericidal activity. Further to this, we show that the previously described lectin-like bacteriocin putidacin L1 shows a similar carbohydrate-binding specificity, indicating that oligosaccharides containing d-rhamnose and not d-mannose, as was previously thought, are the physiologically relevant ligands for this group of bacteriocins. The widespread inclusion of d-rhamnose in the lipopolysaccharide of members of the genus Pseudomonas explains the unusual genus-specific activity of the lectin-like bacteriocins.


Zdroje

1. GorkiewiczG (2009) Nosocomial and antibiotic-associated diarrhoea caused by organisms other than Clostridium difficile. International Journal of Antimicrobial Agents 33: S37–S41.

2. CarrollKC, BartlettJG (2011) Biology of Clostridium difficile: Implications for Epidemiology and Diagnosis. Annual Review of Microbiology 65: 501–521.

3. ManichanhC, BorruelN, CasellasF, GuarnerF (2012) The gut microbiota in IBD. Nature Reviews Gastroenterology & Hepatology 9: 599–608.

4. QinJ, LiY, CaiZ, LiS, ZhuJ, et al. (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55–60.

5. Henao-MejiaJ, ElinavE, JinC, HaoL, MehalWZ, et al. (2012) Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482: 179–U167.

6. ScherJU, AbramsonSB (2011) The microbiome and rheumatoid arthritis. Nature Reviews Rheumatology 7: 569–578.

7. HviidA, SvanstromH, FrischM (2011) Antibiotic use and inflammatory bowel diseases in childhood. Gut 60: 49–54.

8. ShawSY, BlanchardJF, BernsteinCN (2011) Association Between the Use of Antibiotics and New Diagnoses of Crohn's Disease and Ulcerative Colitis. American Journal of Gastroenterology 106: 2133–2142.

9. SpehlmannME, BegunAZ, SaroglouE, HinrichsF, TiemannU, et al. (2012) Risk factors in German twins with inflammatory bowel disease: Results of a questionnaire-based survey. Journal of Crohns & Colitis 6: 29–42.

10. GrinterR, MilnerJ, WalkerD (2012) Ferredoxin containing bacteriocins suggest a novel mechanism of iron uptake in Pectobacterium spp. PLoS ONE 7: e33033.

11. GrinterR, RoszakAW, CogdellRJ, MilnerJJ, WalkerD (2012) The Crystal Structure of the Lipid II-degrading Bacteriocin Syringacin M Suggests Unexpected Evolutionary Relationships between Colicin M-like Bacteriocins. Journal of Biological Chemistry 287: 38876–38888.

12. CascalesE, BuchananSK, DuchéD, KleanthousC, LloubèsR, et al. (2007) Colicin biology. Microbiology and Molecular Biology Reviews 71: 158–229.

13. Michel-BriandY, BaysseC (2002) The pyocins of Pseudomonas aeruginosa. Biochimie 84: 499–510.

14. WalkerD, MoshbahiK, VankemmelbekeM, JamesR, KleanthousC (2007) The role of electrostatics in colicin nuclease domain translocation into bacterial cells. Journal of Biological Chemistry 282: 31389–31397.

15. OgawaT, TomitaK, UedaT, WatanabeK, UozumiT, et al. (1999) A cytotoxic ribonuclease targeting specific transfer RNA anticodons. Science 283: 2097–2100.

16. NgCL, LangK, MeenanNAG, SharmaA, KelleyAC, et al. (2010) Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3. Nature Structural & Molecular Biology 17: 1241–+.

17. ZethK, RoemerC, PatzerSI, BraunV (2008) Crystal structure of colicin M, a novel phosphatase specifically imported by Escherichia coli. Journal of Biological Chemistry 283: 25324–25331.

18. GrahamAC, StockerBAD (1977) GENETICS OF SENSITIVITY OF SALMONELLA SPECIES TO COLICIN-M AND BACTERIOPHAGES T5 T1, AND ES18. Journal of Bacteriology 130: 1214–1223.

19. KurisuG, ZakharovSD, ZhalninaMV, BanoS, EroukovaVY, et al. (2003) The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nature Structural Biology 10: 948–954.

20. SmithK, MartinL, RinaldiA, RajendranR, RamageG, et al. (2012) Activity of Pyocin S2 against Pseudomonas aeruginosa Biofilms. Antimicrobial Agents and Chemotherapy 56: 1599–1601.

21. BrownCL, SmithK, McCaugheyL, WalkerD (2012) Colicin-like bacteriocins as novel therapeutic agents for the treatment of chronic biofilm-mediated infection. Biochemical Society Transactions 40: 1549–1552.

22. LyczakJB, CannonCL, PierGB (2002) Lung Infections Associated with Cystic Fibrosis. Clinical Microbiology Reviews 15: 194–222.

23. GhequireMGK, Garcia-PinoA, LebbeEKM, SpaepenS, LorisR, et al. (2013) Structural Determinants for Activity and Specificity of the Bacterial Toxin LlpA. PLoS pathogens 9: e1003199–e1003199.

24. GhequireMGK, LiW, ProostP, LorisR, De MotR (2012) Plant lectin-like antibacterial proteins from phytopathogens Pseudomonas syringae and Xanthomonas citri. Environmental Microbiology Reports 4: 373–380.

25. GhequireMGK, LorisR, De MotR (2012) MMBL proteins: from lectin to bacteriocin. Biochemical Society Transactions 40: 1553–U1433.

26. ParretAHA, SchoofsG, ProostP, De MotR (2003) Plant lectin-like bacteriocin from a rhizosphere-colonizing Pseudomonas isolate. Journal of Bacteriology 185: 897–908.

27. ParretAHA, TemmermanK, De MotR (2005) Novel lectin-like bacteriocins of biocontrol strain Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology 71: 5197–5207.

28. Sharon N (2001) Lectins. eLS: John Wiley & Sons, Ltd.

29. SharonN, LisH (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14: 53R–62R.

30. Van DammeEJM, Nakamura-TsurutaS, SmithDF, OngenaertM, WinterHC, et al. (2007) Phylogenetic and specificity studies of two-domain GNA-related lectins: generation of multispecificity through domain duplication and divergent evolution. Biochemical Journal 404: 51–61.

31. ChandraNR, RamachandraiahG, BachhawatK, DamTK, SuroliaA, et al. (1999) Crystal structure of a dimeric mannose-specific agglutinin from garlic: Quaternary association and carbohydrate specificity. Journal of Molecular Biology 285: 1157–1168.

32. VastaGR, Nita-LazarM, GiomarelliB, AhmedH, DuS, et al. (2011) Structural and functional diversity of the lectin repertoire in teleost fish: Relevance to innate and adaptive immunity. Developmental and Comparative Immunology 35: 1388–1399.

33. KurimotoE, SuzukiM, AmemiyaE, YamaguchiY, NirasawaS, et al. (2007) Curculin Exhibits Sweet-tasting and Taste-modifying Activities through Its Distinct Molecular Surfaces. Journal of Biological Chemistry 282: 33252–33256.

34. ShimokawaM, FukudomeA, YamashitaR, MinamiY, YagiF, et al. (2012) Characterization and cloning of GNA-like lectin from the mushroom Marasmius oreades. Glycoconjugate Journal 29: 457–465.

35. HesterG, WrightCS (1996) The Mannose-specific bulb lectin from Galanthus nivalis (snowdrop) binds mono- and dimannosides at distinct sites. Structure analysis of refined complexes at 2.3 angstrom and 3.0 angstrom resolution. Journal of Molecular Biology 262: 516–531.

36. FyfeJAM, HarrisG, GovanJRW (1984) Revised Pyocin Typing Method For Pseudomonas-Aeruginosa. Journal of Clinical Microbiology 20: 47–50.

37. RocchettaHL, BurrowsLL, PacanJC, LamJS (1998) Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Molecular Microbiology 30: 1131–1131.

38. LamJS, TaylorVL, IslamST, HaoY, KocincovaD (2011) Genetic and Functional Diversity of Pseudomonas aeruginosa Lipopolysaccharide. Frontiers in microbiology 2: 118–118.

39. HaoY, KingJD, HuszczynskiS, KocincovaD, LamJS (2013) Five New Genes Are Important for Common Polysaccharide Antigen Biosynthesis in Pseudomonas aeruginosa. Mbio 4.

40. JacobsMA, AlwoodA, ThaipisuttikulI, SpencerD, HaugenE, et al. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America 100: 14339–14344.

41. HolmL, RosenströmP (2010) Dali server: conservation mapping in 3D. Nucleic Acids Research 38: W545–W549.

42. OvodV, RudolphK, KnirelY, KrohnK (1996) Immunochemical characterization of O polysaccharides composing the alpha-D-rhamnose backbone of lipopolysaccharide of Pseudomonas syringae and classification of bacteria into serogroups O1 and O2 with monoclonal antibodies. Journal of Bacteriology 178: 6459–6465.

43. OvodVV, KnirelYA, SamsonR, KrohnKJ (1999) Immunochemical characterization and taxonomic evaluation of the O polysaccharides of the lipopolysaccharides of Pseudomonas syringae serogroup O1 strains. Journal of Bacteriology 181: 6937–6947.

44. KleanthousC (2010) Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nature Reviews Microbiology 8: 843–848.

45. Abdel-MawgoudAM, LepineF, DezielE (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Applied Microbiology and Biotechnology 86: 1323–1336.

46. CaffallKH, MohnenD (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Research 344: 1879–1900.

47. KnirelYA, ShashkovAS, SenchenkovaS, AjikiY, FukuokaS (2002) Structure of the O-polysaccharide of Pseudomonas putida FERM p-18867. Carbohydrate Research 337: 1589–1591.

48. MolinaroA, SilipoA, LanzettaR, NewmanMA, DowJM, et al. (2003) Structural elucidation of the O-chain of the lipopolysaccharide from Xanthomonas campestris strain 8004. Carbohydrate Research 338: 277–281.

49. Vinion-DubielAD, GoldbergJB (2003) Lipopolysaccharide of Burkholderia cepacia complex. Journal of Endotoxin Research 9: 201–213.

50. StewartL, FordA, SangalV, JeukensJ, BoyleB, et al. (2013) Draft genomes of twelve host adapted and environmental isolates of Pseudomonas aeruginosa and their position in the core genome phylogeny. Pathogens and Disease [epub ahead of print].

51. ClaessonMJ, WangQ, O'SullivanO, Greene-DinizR, ColeJR, et al. (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Research 38.

52. RammM, LobeM, HamburgerM (2003) A simple method for preparation of D-rhamnose. Carbohydrate Research 338: 109–112.

53. RiveraM, BryanLE, HancockREW, McGroartyEJ (1988) Heterogeneity Of Lipopolysaccharides From Pseudomonas-Aeruginosa - Analysis Of Lipopolysaccharide Chain-Length. Journal of Bacteriology 170: 512–521.

54. MoriS, AbeygunawardanaC, JohnsonMO, vanZijlP (1996) Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation (vol 108, pg 94, 1995). Journal of Magnetic Resonance Series B 110: 321–321.

55. VrankenWF, BoucherW, StevensTJ, FoghRH, PajonA, et al. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins-Structure Function and Bioinformatics 59: 687–696.

56. GorrecF (2009) The MORPHEUS protein crystallization screen. Journal of Applied Crystallography 42: 1035–1042.

57. IncardonaM-F, BourenkovGP, LevikK, PieritzRA, PopovAN, et al. (2009) EDNA: a framework for plugin-based applications applied to X-ray experiment online data analysis. Journal of Synchrotron Radiation 16: 872–879.

58. LongF, VaginAA, YoungP, MurshudovGN (2008) BALBES: a molecular-replacement pipeline. Acta Crystallographica Section D-Biological Crystallography 64: 125–132.

59. AdamsPD, AfoninePV, BunkocziG, ChenVB, DavisIW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D-Biological Crystallography 66: 213–221.

60. EmsleyP, LohkampB, ScottWG, CowtanK (2010) Features and development of Coot. Acta Crystallographica Section D-Biological Crystallography 66: 486–501.

61. MurshudovGN, SkubakP, LebedevAA, PannuNS, SteinerRA, et al. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D-Biological Crystallography 67: 355–367.

62. ChenVB, ArendallWBIII, HeaddJJ, KeedyDA, ImmorminoRM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D-Biological Crystallography 66: 12–21.

63. LaskowskiRA, MacarthurMW, MossDS, ThorntonJM (1993) PROCHECK - A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26: 283–291.

64. McCoyAJ, Grosse-KunstleveRW, AdamsPD, WinnMD, StoroniLC, et al. (2007) Phaser crystallographic software. Journal of Applied Crystallography 40: 658–674.

65. SchuttelkopfAW, van AaltenDMF (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica Section D-Biological Crystallography 60: 1355–1363.

66. KonarevPV, VolkovVV, SokolovaAV, KochMHJ, SvergunDI (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. Journal of Applied Crystallography 36: 1277–1282.

67. SvergunDI (1992) Determination Of The Regularization Parameter In Indirect-Transform Methods Using Perceptual Criteria. Journal of Applied Crystallography 25: 495–503.

68. FrankeD, SvergunDI (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. Journal of Applied Crystallography 42: 342–346.

69. VolkovVV, SvergunDI (2003) Uniqueness of ab initio shape determination in small-angle scattering. Journal of Applied Crystallography 36: 860–864.

70. KozinMB, SvergunDI (2001) Automated matching of high- and low-resolution structural models. Journal of Applied Crystallography 34: 33–41.

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