#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Phage-mediated Dispersal of Biofilm and Distribution of Bacterial Virulence Genes Is Induced by Quorum Sensing


All higher organisms live in intimate contact with bacteria and viruses in their direct environment. Some of these bacteria in our gut can switch between being harmless commensals and causing severe and sometimes lethal infections. This involves a tight regulation of the mechanisms needed to initially colonize and later to harm the host. Here we describe a novel mechanism by which phages (i.e. viruses that infect bacteria) contribute to virulence in commensal gut bacteria. Our results show that bacteria "sense" the number of bacteria present at any given moment through a process called quorum sensing and this provides them with the information needed to assess the specific step during the infectious process. At late stages of infection bacteria are usually present in high numbers, and at this point release viruses that can infect nearby bacteria and transfer genes that are needed to cause infection, thereby enabling previously harmless bacteria to become dangerous pathogens.


Vyšlo v časopise: Phage-mediated Dispersal of Biofilm and Distribution of Bacterial Virulence Genes Is Induced by Quorum Sensing. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004653
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004653

Souhrn

All higher organisms live in intimate contact with bacteria and viruses in their direct environment. Some of these bacteria in our gut can switch between being harmless commensals and causing severe and sometimes lethal infections. This involves a tight regulation of the mechanisms needed to initially colonize and later to harm the host. Here we describe a novel mechanism by which phages (i.e. viruses that infect bacteria) contribute to virulence in commensal gut bacteria. Our results show that bacteria "sense" the number of bacteria present at any given moment through a process called quorum sensing and this provides them with the information needed to assess the specific step during the infectious process. At late stages of infection bacteria are usually present in high numbers, and at this point release viruses that can infect nearby bacteria and transfer genes that are needed to cause infection, thereby enabling previously harmless bacteria to become dangerous pathogens.


Zdroje

1. Rodriguez-Valera F, Martin-Cuadrado A-B, Rodriguez-Brito B, Pasić L, Thingstad TF, et al. (2009) Explaining microbial population genomics through phage predation. 7: 828–836. doi: 10.1038/nrmicro2235 19834481

2. Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499: 219–222. doi: 10.1038/nature12212 23748443

3. Matos RC, Lapaque N, Rigottier-Gois L, Debarbieux L, Meylheuc T, et al. (2013) Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits. PLoS Genet 9: e1003539. doi: 10.1371/journal.pgen.1003539.s007 23754962

4. Bae T, Baba T, Hiramatsu K, Schneewind O (2006) Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62: 1035–1047. doi: 10.1111/j.1365-2958.2006.05441.x 17078814

5. Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI (2012) Going viral: next-generationsequencing applied to phagepopulations in the human gut. 10: 607–617. doi: 10.1038/nrmicro2853 22864264

6. Palmer KL, Gilmore MS (2010) Multidrug-resistant enterococci lack CRISPR-cas. mBio 1. doi: 10.1128/mBio.00227-10 21179522

7. Sampson TR, Saroj SD, Llewellyn AC, Tzeng Y-L, Weiss DS (2013) A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497: 254–257. doi: 10.1038/nature12048 23584588

8. Seed KD, Lazinski DW, Calderwood SB, Camilli A (2013) A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494: 489–491. doi: 10.1038/nature11927 23446421

9. Zhu J, Kaufmann GF (2013) Quo vadis quorum quenching? Current Opinion in Pharmacology 13: 688–698. doi: 10.1016/j.coph.2013.07.003 23876839

10. Rickard AH, Palmer RJ, Blehert DS, Campagna SR, Semmelhack MF, et al. (2006) Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60: 1446–1456. doi: 10.1111/j.1365-2958.2006.05202.x 16796680

11. Otto M (2013) Staphylococcal Infections: Mechanisms of Biofilm Maturation and Detachment as Critical Determinants of Pathogenicity*. Annu Rev Med 64: 175–188. doi: 10.1146/annurev-med-042711-140023 22906361

12. Creti R, Koch S, Fabretti F, Baldassarri L, Huebner J (2006) Enterococcal colonization of the gastro-intestinal tract: role of biofilm and environmental oligosaccharides. BMC Microbiol 6: 60. doi: 10.1186/1471-2180-6-60 16834772

13. Nallapareddy SR, Singh KV, Sillanpää J, Garsin DA, Höök M, et al. (2006) Endocarditis and biofilm-associated pili of Enterococcus faecalis. 116: 2799–2807. doi: 10.1172/JCI29021 17016560

14. Kristich CJ, Li Y-H, Cvitkovitch DG, Dunny GM (2004) Esp-independent biofilm formation by Enterococcus faecalis. J Bacteriol 186: 154–163. 14679235

15. Tendolkar PM, Baghdayan AS, Gilmore MS, Shankar N (2004) Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect Immun 72: 6032–6039. doi: 10.1128/IAI.72.10.6032-6039.2004 15385507

16. Hufnagel M, Koch S, Creti R, Baldassarri L, Huebner J (2004) A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J INFECT DIS 189: 420–430. doi: 10.1086/381150 14745699

17. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, et al. (2010) Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 120: 4332–4341. doi: 10.1172/JCI43918 21099116

18. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R, et al. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299: 2071–2074. doi: 10.1126/science.1080613 12663927

19. Fritzenwanker M, Kuenne C, Billion A, Hain T, Zimmermann K, et al. (2013) Complete Genome Sequence of the Probiotic Enterococcus faecalis Symbioflor 1 Clone DSM 16431. Genome Announcements 1: e00165-12–e00165-12. doi: 10.1128/genomeA.00165-12 24371207

20. Wagner PL, Waldor MK (2002) Bacteriophage control of bacterial virulence. Infect Immun 70: 3985–3993. 12117903

21. Vendeville A, Winzer K, Heurlier K, Tang CM, Hardie KR (2005) Making “sense” of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Micro 3: 383–396. doi: 10.1038/nrmicro1146

22. Winzer K, Hardie KR, Williams P (2002) Bacterial cell-to-cell communication: sorry, can't talk now—gone to lunch! Curr Opin Microbiol 5: 216–222. 11934621

23. Doherty N, Holden MTG, Qazi SN, Williams P, Winzer K (2006) Functional Analysis of luxS in Staphylococcus aureus Reveals a Role in Metabolism but Not Quorum Sensing. J Bacteriol 188: 2885–2897. doi: 10.1128/JB.188.8.2885-2897.2006 16585750

24. Shao C, Shang W, Yang Z, Sun Z, Li Y, et al. (2012) LuxS-dependent AI-2 regulates versatile functions in Enterococcus faecalis V583. J Proteome Res 11: 4465–4475. doi: 10.1021/pr3002244 22856334

25. Cuadra-Saenz G, Rao DL, Underwood AJ, Belapure SA, Campagna SR, et al. (2012) Autoinducer-2 influences interactions amongst pioneer colonizing streptococci in oral biofilms. Microbiology 158: 1783–1795. doi: 10.1099/mic.0.057182-0 22493304

26. Yasmin A, Kenny JG, Shankar J, Darby AC, Hall N, et al. (2010) Comparative Genomics and Transduction Potential of Enterococcus faecalis Temperate Bacteriophages. J Bacteriol 192: 1122–1130. doi: 10.1128/JB.01293-09 20008075

27. Duerkop BA, Clements CV, Rollins D, Rodrigues JLM, Hooper LV (2012) A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc Natl Acad Sci USA 109: 17621–17626. doi: 10.1073/pnas.1206136109 23045666

28. Theilacker C, Sanchez-Carballo P, Toma I, Fabretti F, Sava I, et al. (2009) Glycolipids are involved in biofilm accumulation and prolonged bacteraemia in Enterococcus faecalis. Mol Microbiol 71: 1055–1069. doi: 10.1111/j.1365-2958.2009.06587.x 19170884

29. Gödeke J, Paul K, Lassak J, Thormann KM (2011) Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. ISME J 5: 613–626. doi: 10.1038/ismej.2010.153 20962878

30. Teng F, Nannini EC, Murray BE (2005) Importance of gls24 in virulence and stress response of Enterococcus faecalis and use of the Gls24 protein as a possible immunotherapy target. J INFECT DIS 191: 472–480. doi: 10.1086/427191 15633107

31. Anetzberger C, Reiger M, Fekete A, Schell U, Stambrau N, et al. (2012) Autoinducers act as biological timers in Vibrio harveyi. PLoS ONE 7: e48310. doi: 10.1371/journal.pone.0048310 23110227

32. Rajamani S, Zhu J, Pei D, Sayre R (2007) A LuxP-FRET-based reporter for the detection and quantification of AI-2 bacterial quorum-sensing signal compounds. Biochemistry 46: 3990–3997. doi: 10.1021/bi602479e 17352493

33. Taga ME, Xavier KB (2011) Methods for analysis of bacterial autoinducer-2 production. Current Protocols in Microbiology Chapter 1: Unit1C.1. doi: 10.1002/9780471729259.mc01c01s23

34. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174

35. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

36. Rigottier-Gois L, Alberti A, Houel A, Taly J-F, Palcy P, et al. (2011) Large-Scale Screening of a Targeted Enterococcus faecalis Mutant Library Identifies Envelope Fitness Factors. PLoS ONE 6: e29023. doi: 10.1371/journal.pone.0029023.t001 22194979

37. Haller C, Berthold M, Wobser D, Kropec A, Lauriola M, et al. (2014) Cell-Wall Glycolipid Mutations and Their Effects on Virulence of E. faecalis in a Rat Model of Infective Endocarditis. PLoS ONE 9: e91863. doi: 10.1371/journal.pone.0091863 24637922

38. Hendrickx APA, Bonten MJM, van Luit-Asbroek M, Schapendonk CME, Kragten AHM, et al. (2008) Expression of two distinct types of pili by a hospital-acquired Enterococcus faecium isolate. Microbiology (Reading, Engl) 154: 3212–3223. doi: 10.1099/mic.0.2008/020891-0 18832326

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#