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N-acyl homoserine lactone production by bacteria within the sponge Suberites domuncula (Olivi, 1792) (Porifera, Demospongiae)

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Abstract

Many bacteria live in close association with sponges. Within these consortia, molecules of communication such as quorum-sensing and hormone-like molecules may occur in order to regulate the partnership. Of particular interest, bacterial N-acyl-l-homoserine lactones (AHLs) were screened in supernatants from Suberites domuncula-associated bacteria using an E. coli bioluminescent reporter system. These sponge-associated bacteria were beforehand isolated on several media supplemented or not with a sponge extract to attempt to isolate sponge-specific bacteria. Out of 81 AHL-producing bacteria, three strains requiring sponge extract to grow were selected for AHL characterization. The in vitro produced AHLs, that is, in bacterial culture supernatants, were identified as N-(3-butanoyl)-l-homoserine lactone and N-(3-oxododecanoyl)-l-homoserine lactone and quantified using LC–ESI–MS/MS. The in vivo production of AHLs by sponge-associated bacteria has also been demonstrated in a healthy host for the first time: N-(3-oxododecanoyl)-l-homoserine lactone, N-(3-hexanoyl)-l-homoserine lactone, and N-(3-heptanoyl)-l-homoserine lactone. This AHL production in sponges may suggest a potential role of these molecules between sponge-associated bacteria and/or between sponge-associated bacteria and the sponge.

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References

  • Böhn M, Hentschel U, Friedrich AB, Fieseler L, Steffen R, Gamulin V, Müller WE (2001) Molecular response of the sponge Suberites domuncula to bacterial infection. Mar Biol 139:1037–1045

    Article  Google Scholar 

  • Chhabra SR, Stead P, Bainton NJ, Salmond GP, Stewart GS, Williams P, Bycroft BW (1993) Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl)-l-homoserine lactone. J Antibiot 46:441–454

    Article  CAS  Google Scholar 

  • de Bary HA (1879) Die erscheinung der symbiose. Verlag Trubner, Straßburg

    Google Scholar 

  • Dobretsov S, Teplitski M, Paul V (2009) Quorum sensing in the marine environment and its relationship to biofouling. Biofouling 25:413–427

    Article  CAS  Google Scholar 

  • Duperron S, Nadalig T, Caprais JC, Sibuet M, Fiala-Médioni A, Amann R, Dubilier N (2005) Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl Environ Microbiol 71:1694–1700

    Article  CAS  Google Scholar 

  • Ellwanger K, Nickel M (2006) Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera). Front Zool 3:7

    Article  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    CAS  Google Scholar 

  • Horng YT, Deng SC, Daykin M, Soo PC, Wei JR, Luh KT, Ho SW, Swift S, Lai HC, Williams P (2002) The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol Microbiol 45:1655–1671

    Article  CAS  Google Scholar 

  • Jacobi CA, Schiffner F, Henkel M, Waibel M, Stork B, Daubrawa M, Eberl L, Gregor M, Wesselborg S (2009) Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway. Int J Med Microbiol 299:509–519

    Article  CAS  Google Scholar 

  • Joint I, Tait K, Wheeler G (2007) Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos Trans R Soc Lond B Biol Sci 362:1223–1233

    Article  CAS  Google Scholar 

  • Kastbjerg VG, Nielsen KF, Dalsgaard I, Rasch M, Bruhn JB, Givskov M, Gram L (2007) Profiling acylated homoserine lactones in Yersinia ruckeri and influence of exogenous acyl homoserine lactones and known quorum-sensing inhibitors on protease production. J Appl Microbiol 102:363–374

    Article  CAS  Google Scholar 

  • Le Pennec G, Perovic S, Ammar MS, Grebenjuk VA, Steffen R, Brümmer F, Müller WE (2003) Cultivation of primmorphs from the marine sponge Suberites domuncula: morphogenetic potential of silicon and iron. J Biotechnol 100:93–108

    Article  Google Scholar 

  • Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P, Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol Microbiol 37:81–97

    Article  CAS  Google Scholar 

  • Liu X, Jia J, Popat R, Ortori CA, Li J, Diggle SP, Gao K, Cámara M (2011) Characterization of two quorum sensing systems in the endophytic Serratia plymuthica strain G3: differential control of motility and biofilm formation according to life-style. BMC Microbiol 11:26

    Article  CAS  Google Scholar 

  • Mohamed NM, Cicirelli EM, Kan J, Chen F, Fuqua C, Hill RT (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10:75–86

    Article  CAS  Google Scholar 

  • Morin D, Grasland B, Vallée-Réhel K, Dufau C, Haras D (2003) On-line high-performance liquid chromatography-mass spectrometric detection and quantification of N-acylhomoserine lactones, quorum-sensing signal molecules, in the presence of biological matrices. J Chromatogr A 1002:79–92

    Article  CAS  Google Scholar 

  • Morohoshi T, Inaba T, Kato N, Kanai K, Ikeda T (2004) Identification of quorum-sensing signal molecules and the LuxRI homologs in fish pathogen Edwardsiella tarda. J Biosci Bioeng 98:274–281

    CAS  Google Scholar 

  • Morohoshi T, Yokoyama Y, Ouchi M, Kato N, Ikeda T (2009) Motility and the expression of the flagellin protein FliC are negatively regulated by quorum sensing in Edwardsiella tarda. J Biosci Bioeng 108:314–318

    Article  CAS  Google Scholar 

  • Müller WE, Wiens M, Müller IM, Schröder HC (2004) The chemokine networks in sponges: potential roles in morphogenesis, immunity and stem cell formation. Prog Mol Subcell Biol 34:103–143

    Article  Google Scholar 

  • Pontes MH, Babst M, Lochhead R, Oakeson K, Smith K, Dale C (2008) Quorum sensing primes the oxidative stress response in the insect endosymbiont. Sodalis glossinidius. PLoS One 3:e3541

    Article  Google Scholar 

  • Reading NS, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11

    Article  CAS  Google Scholar 

  • Redfield RJ (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365–370

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol

  • Taylor MW, Schupp PJ, Baillie HJ, Charlton TS, de Nys R, Kjelleberg S, Steinberg PD (2004) Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl Environ Microbiol 70:4387–4389

    Article  CAS  Google Scholar 

  • Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  CAS  Google Scholar 

  • Thakur NL, Perovic-Ottstadt S, Batel R, Korzhev M, Diehl-Seifert B, Müller IM, Müller WE (2005) Innate immune defense of the sponge Suberites domuncula against Gram-positive bacteria: induction of lysozyme and AdaPTin. Mar Biol 146:271–282

    Article  CAS  Google Scholar 

  • Vikström E, Tafazoli F, Magnusson KE (2006) Pseudomonas aeruginosa quorum sensing molecule N-(3-oxododecanoyl)-l-homoserine lactone disrupts epithelial barrier integrity of Caco-2 cells. FEBS Lett 580:6921–6928

    Article  Google Scholar 

  • Wagner C, Zimmermann S, Brenner-Weiss G, Hug F, Prior B, Obst U, Hänsch GM (2007) The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone (3OC12-HSL) enhances the host defense by activating human polymorphonuclear neutrophils (PMN). Anal Bioanal Chem 387:481–487

    Article  CAS  Google Scholar 

  • Wiens M, Korzhev M, Krasko A, Thakur NL, Perovic-Ottstadt S, Breter HJ, Ushijima H, Diehl-Seifert B, Müller IM, Müller WE (2005) Innate immune defense of the sponge Suberites domuncula against bacteria involves a MyD88-dependent signaling pathway. Induction of a perforin-like molecule. J Biol Chem 280:27949–27959

    Article  CAS  Google Scholar 

  • Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WE (2007) Toll-like receptors are part of the innate immune defense system of sponges (Demospongiae: Porifera). Mol Biol Evol 24:792–804

    Article  CAS  Google Scholar 

  • Winson MK, Swift S, Fish L, Throup JP, Jørgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GS (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163:185–192

    Article  CAS  Google Scholar 

  • Zan J, Fuqua C, Hill TH (2011) Diversity and functional analysis of luxS genes in vibrios from marine Mycale laxissima and Ircinia strobilina. ISME J 1–12

  • Zhang L, Murphy PJ, Kerr A, Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362:446–448

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Axis 1 “Genomics and blue chemistry” of the GIS Europôle Mer, and European FEDER. JG was the recipient of a doctoral fellowship from the Ministère de l’Enseignement Supérieur et de la Recherche, France.

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Authors and Affiliations

  1. Laboratoire de Biotechnologie et Chimie Marines, Université de Bretagne-Sud (UEB), IUEM, EA 3884, Lorient, France

    Laure Taupin, Jasnizat Bin Saïdin & Alain Dufour

  2. Laboratoire de Biotechnologie et Chimie Marines, Université de Bretagne-Sud, BP 92116, 56321, Lorient Cedex, France

    Johan Gardères & Gaël Le Pennec

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  1. Johan Gardères
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  2. Laure Taupin
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  3. Jasnizat Bin Saïdin
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  4. Alain Dufour
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  5. Gaël Le Pennec
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Correspondence to Johan Gardères or Gaël Le Pennec.

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Communicated by M. Kühl.

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Gardères, J., Taupin, L., Saïdin, J.B. et al. N-acyl homoserine lactone production by bacteria within the sponge Suberites domuncula (Olivi, 1792) (Porifera, Demospongiae). Mar Biol 159, 1685–1692 (2012). https://doi.org/10.1007/s00227-012-1956-z

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  • DOI: https://doi.org/10.1007/s00227-012-1956-z

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