PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2012 | 61 | 4 |

Tytuł artykułu

Edwardsiella ictaluri LuxS: activity, expression, and involvement in pathogenicity

Autorzy

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
Edwardsiella ictaluri is a Gram-negative bacterium and the causative agent of enteric septicemia of catfish. In this study, we examined the expression and function of the LuxS from a pathogenic E. ictaluri strain, J901. J901 was found to produce autoinducer 2 (AI-2) activity that maximized at mid-logarithmic phase and was enhanced by glucose and repressed by high temperature. Consistently, a luxS gene (luxSEi) was identified in J901, whose expression was regulated by cell density, glucose, and temperature in a manner similar to that observed with AI-2 activity. Further analysis showed that LuxSEi is a biologically active AI-2 synthase that was able to complement the luxS-defective phenotype of Escherichia coli DH5. To examine the functional importance of LuxSEi, a genetically modified variant of J901, J901Ri, was constructed, in which luxSEi expression was blocked by RNA interference. Compared to the wild type, J901Ri was (i) reduced in AI-2 activity to a level of 59% of that of the wild type; (ii) impaired in both planktonic and biofilm growth; (iii) significantly attenuated in the ability to infect cultured fish cells and to cause mortality in infected fish; (iv) unable to induce the expression of certain virulence-associated genes. Addition of exogenous AI-2 failed to rescue the growth defect of J901Ri as free-living cells but restored biofilm production and the expression of virulence genes to levels comparable to those of the wild type. Taken together, these results indicate that LuxSEi is a functional AI-2 synthase that is required for optimal cellular growth and host infection.

Wydawca

-

Rocznik

Tom

61

Numer

4

Opis fizyczny

p.263-271,fig.,ref.

Twórcy

autor
  • Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, 266071 Qingdao, China
autor
  • Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, 266071 Qingdao, China

Bibliografia

  • Ahmed N.A., F.C. Petersen and A.A. Scheie. 2007. AI-2 quorum sensing affects antibiotic susceptibility in Streptococcus anginosus. J. Antimicrob. Chemoth. 60: 49–53.
  • Booth N.J., J.B. Beekman and R.L. Thune. 2009. Edwardsiella ictaluri encodes an acid-activated urease that is required for intracellular replication in channel catfish (Ictalurus punctatus) macrophages. Appl. Environ. Microb. 75: 6712–6720.
  • Booth N.J., A. Elkamel and R.L. Thune. 2006. Intracellular replication of Edwardsiella ictaluri in channel catfish macrophages. J. Aquat. Anim. Health 18: 101–108.
  • Cooper R.K., E.B. Shotts and L.K. Nolan. 1996. Use of a minitransposon to study chondroitinase activity associated with Edwardsiella ictaluri. J. Aquat. Anim. Health 8: 319–324.
  • Coulthurst S.J., S. Clare, T.J. Evans, I.J. Foulds, K.J. Roberts, M. Welch, G. Dougan and G.P. Salmond. 2007. Quorum sensing has an unexpected role in virulence in the model pathogen Citrobacter rodentium. EMBO. J. 8: 698–703.
  • Coulthurs T., S.J., C.L. Kurz and G.P.C. Salmond. 2004. luxS mutants of Serratia defective in autoinducer-2-dependent ‘quorum sensing’ show strain-dependent impacts on virulence and production of carbapenem and prodigiosin. Microbiology 150: 1901–1910.
  • De Keersmaecker S.C.J., K. Sonck and J. Vanderleyden. 2006. Let LuxS speak up in AI-2 signaling. Trends Microbiol. 14: 114–119.
  • Doherty N., M.T. Holden, S.N. Qazi, P. Williams and K. Winzer. 2006. Functional analysis of luxS in Staphylococcus aureus reveals a role in metabolism but not quorum sensing. J. Bacteriol. 188: 2885–2897.
  • Eagon R.G. (1962). Pseudomonas natriegens, a marine bacterium with a generation time of less than 10 minutes. J. Bacteriol. 83: 736–737.
  • Gonzalez Barrios A.F., R. Zuo, Y. Hashimoto, L. Yang, W.E. Bentley and T.K. Wood. 2006. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J. Bacteriol. 188: 305–316.
  • Gonzalez J.E. and N.D. Keshavan. 2006. Messing with bacterial quorum sensing. Microbiol. Mol. Biol. R. 70: 859–875.
  • Henke J.M. and B.L. Bassler. 2004. Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J. Bacteriol. 186: 3794–3805.
  • Herzberg M., I.K. Kaye, W. Peti and T.K. Wood. 2006. YdgG (TqsA) controls biofilm formation in Escherichia coli K-12 through autoinducer 2 transport. J. Bacteriol.188: 587–598.
  • Joyce E.A., A. Kawale, S. Censini, C.C. KIM, A. Covacci and S. Falkow. 2004. LuxS is required for persistent pneumococcal carriage and expression of virulence and biosynthesis genes. Infect. Immun. 72: 2964–2975.
  • Karsi A., N. Gülsoy, E. Corb, P.R. Dumpala and M.L. Lawrence. 2009. High-throughput bioluminescence-based mutant screening strategy for identification of bacterial virulence genes. Appl. Environ. Microb. 75: 2166–2175.
  • Kendall M.M., D.A. Rasko and V. Sperandio. 2007. Global e!ects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli. Infect. Immun. 5: 4875–4884.
  • Kong K.F., C. Vuong and M. Otto. 2006. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296: 133–139.
  • Lawrence M.L., M.M. Banes, P. Azadi and B.Y. Reeks. 2003. The Edwardsiella ictaluri O polysaccharide biosynthesis gene cluster and the role of O polysaccharide in resistance to normal catfish serum and catfish neutrophils. Microbiology 149: 1409–1421.
  • Lawrence M.L., M.M. Banes and M.L. Williams. 2001. Phenotype and virulence of an isogenic lipopolysaccharide O side chain mutant strain of Edwardsiella ictaluri. J. Aquat. Anim. Health 13: 291–299.
  • Lyon W.R., J.C. Madden, J.C. Levin, J.L. Stein and M.G. Caparon. 2001. Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol. Microbiol. 42: 145–157.
  • Marouni M.J. and S. Sela. 2003. The luxS gene of Streptococcus pyogenes regulates expression of genes that affect internalization by epithelial cells. Infect. Immun. 71: 5633–5639.
  • Mc Nab R., S.K. Ford, A. EL-Sabaeny, B. Barbieri, G.S. Cook and R.J. Lamont. 2003. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185: 274–284.
  • Menanteau-Ledouble S., A. Karsi and M.L. Lawrence. 2011. Importance of skin abrasion as a primary site of adhesion for Edwardsiella ictaluri and impact on invasion and systematic infection in channel catfish Ictalurus punctatus. Vet. Microbiol. 148: 425–430.
  • Miller M.B. and B.L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165–199.
  • Morrison E.E. and J.A. Plumb. 1994. Olfactory organ of channel catfish as a site of experimental Edwardsiella ictaluri infection. J. Aquat. Anim. Health 6: 101–109.
  • Novak E.A., H. Shao, C.A. Daep and D.R. Demuth. 2010. Autoinducer-2 and QseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans. Infect. Immun. 78: 2919–2926.
  • Parsek M.R. and E.P. Greenberg. 2005. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13: 27–33.
  • Plummer P., O. Sahin, E. Burrough, R. Sippy, K. Mou, J. Raben-old, M. Yaeger and Q. Zhang. 2011. The critical role of LuxS in the virulence of Campylobacter jejuni in a guinea pig model of abortion. Infect. Immun. doi:10.1128/IAI.05766–11.
  • Rickard A.H., R.J. Palmer, D.S. Blehert, S.R. Campagna, M.F. Semmelhack, P.G. Egland, B.L. Bassler and P.E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60: 1446–1456.
  • Schauder S., K. Shokat, M.G. Surette and B.L. Bassler. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorumsensing signal molecule. Mol. Microbiol. 41: 463–476.
  • Sircili M.P., M. Walters, L.R. Trabulsi and V. Sperandio. 2004. Modulation of enteropathogenic Escherichia coli virulence by quorum sensing. Infect. Immun. 72: 2329–2337.
  • Sun K., H. Wang, M. Zhang, Z. Xiao and L. Su. 2009. Genetic mechanisms of multi-antimicrobial resistance in a pathogenic Edwardsiella tarda strain. Aquaculture 289: 134–139.
  • Surette M.G. and B.L. Bassle. 1999. Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31: 585–595.
  • Surette M.G., M.B. Miller and B.L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. P. Natl. Acad. Sci. U.S.A. 96: 1639–1644.
  • Taga M.E., S.T. Miller and B.L. Bassler. 2003. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50: 1411–1427.
  • Taga M.E., J.L. Semmelhack and B.L. Bassler. 2001. The LuxSdependent autoinducer Al-2 controls the expression of an ABC transporter that functions in Al-2 uptake in Salmonella typhimurium. Mol. Microbiol. 42: 777–793.
  • Thune R.L., D.H. Fernandez, J.L. Benoit, M. Kelly-Smith, M.L. Rogge, N.J. Booth, C.A. Landry and R.A. Bologna. 2007. Signature-tagged mutagenesis of Edwardsiella ictaluri identifies virulence-related genes, including a Salmonella pathogenicity island 2 class of type III secretion systems. Appl. Environ. Microb. 73: 7934–7946.
  • Vendeville A., K. Winzer, K. Heurlier, C.M. Tang and K.R. Hardie. 2005. Making ‘sense’ of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3: 383–396.
  • Wagner B.A., D.J. Wise, L.H. Khoo and J.S. Terhune. 2002. The epidemiology of bacterial diseases in food-size channel catfish. J. Aquat. Anim. Health 14: 263–272.
  • Wang L., J. Li, J.C. March, J.J. Valdes and W.E. Bentley. 2005. Cyclic AMP (cAMP) and cAMP receptor protein influence both synthesis and uptake of extracellular autoinducer 2 in Escherichia coli. J. Bacteriol. 187: 2066–2076.
  • Waters C.M. and B.L. Bonnie. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell. Dev. Bi. 21: 319–346.
  • Williams M.L. and M.L. Lawrence. 2005. Identification and characterization of a two-component hemolysin from Edwardsiella ictaluri. Vet. Microbiol.108: 281–289.
  • Williams M.L., A.F. Gillaspy, D.W. Dyer, R.L. Thune, G.C. Waldbieser, S.C. Schuster, J. Gipson, J. Zaitshik, C. Landry, M.M. Banes and others. 2012. Genome sequence of Edwardsiella ictaluri 93–146, a strain associated with a natural channel catfish outbreak of enteric septicemia of catfish. J. Bacteriol. 194: 740–741.
  • Winzer K., K.R. Hardie, N. Burgess, N. Doherty, D. Kirke, M.T. Holden, R. Linforth, K.A. Cornell, A.J. Taylor, P.J. Hill and others. 2002. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909–922.
  • Xavier K.B. and B.L. Bassler. 2005. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187, 238–248.
  • Xu L., H. Li, C. Vuong, V. Vadyvaloo, J. Wang, Y. Yao, M. Otto and Q. Gao. 2006. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect. Immun. 74: 488–496.
  • Zhang M., K. Sun and L. Sun. 2008. Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiol-SGM 154: 2060–2069.
  • Zheng W., Y. Hu and L. Sun. 2010. Cloning and analysis of a ferritin subunit from turbot (Scophthalmus maximus). Fish Shellfish Immun. 28: 829–836.
  • Zheng W. and L. Sun. 2011. Evaluation of housekeeping genes as references for quantitative real time RT-PCR analysis of gene expression in Japanese flounder (Paralichthys olivaceus). Fish Shellfish Immun. 30: 638–645.

Typ dokumentu

Bibliografia

Identyfikatory

Identyfikator YADDA

bwmeta1.element.agro-3ba8ea03-5038-487a-ab22-38df8db1513a
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.