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Molecular/chemical ecology in sponges: evidence for an adaptive antibacterial response in Suberites domuncula

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Abstract

Sponges (Porifera) represent the evolutionary oldest metazoan phylum still extant today. They have developed a complex Bauplan, based on the existence of structural and regulatory molecules; many of these have been cloned and analyzed in the past years. The demosponge Suberites domuncula has been used as a suitable model to demonstrate that these animals not only possess an adaptive immune response on the level of cytokines, but also, as pointed out here, on the level of synthesis of bioactive alkyl-lipid derivatives. From specimens of S. domuncula the two lyso-PAF (platelet-activating factor) compounds, 1-O-hexadecyl-sn-glycero-3-phosphocholine and 1-O-octadecyl-sn-glycero-3-phosphocholine, have been identified and characterized. These two lyso-PAFs showed pronounced anti-bacterial activity. In the central part of this paper it is shown that the level of synthesis of the lyso-PAF congeners increased in response to the model compound, the endotoxin lipopolysaccharide (LPS). Treatment of the tissue with LPS for 72 h substantially increased the synthesis. In order to prove that the lyso-PAFs are really synthesized by the sponge, the key enzyme of the alkyl-dihydroxyacetonephosphate pathway, i.e. alkyl-dihydroxyacetonephosphate synthase (ADS), was cloned from S. domuncula. This sponge enzyme comprises the characteristic features of metazoan ADS enzymes; it is increasingly expressed in the tissue and in the in vitro cell culture system after exposure to LPS. These data are taken as a strong indication that bioactive, low-molecular weight, non-proteinaceous lipid derivatives function in an adaptive manner in response to the endotoxin.

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References

  • Adams MD, and 193 others (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

    Article  PubMed  Google Scholar 

  • Alam N, Bae BH, Hong J, Lee CO, Shin BA, Im KS, Jung JH (2001) Additional bioactive lyso-PAF congeners from the sponge Spirastrella abata. J Nat Prod (Lloydia) 64:533–535

    Google Scholar 

  • Arndt W (1937) Schwämme. In: Pax F, Arndt W (eds) Die Rohstoffe des Tierreichs, vol I/2. Bornträger, Berlin, pp 1577–2000

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidmann JG, Struhl K (1995) Current protocols in molecular biology. Wiley, New York

  • Bergmann W, Feeney RJ (1951) Contribution to the study of marine sponges. 32. The nucleosides of sponges. J Org Chem 16:981–987

    CAS  Google Scholar 

  • Bergquist PR (1978) Sponges. Hutchinson, London

  • Bewley CA, Faulkner DJ (1998) Lithistid sponges: star performance of hosts to the stars? Angew Chem Int Ed 37:2162–2178

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chang L, Karin M (2001) Mammalian MAP kinase signaling cascade. Nature 410:37–40

    CAS  PubMed  Google Scholar 

  • Cimino G, Ghiselin MT (2001) Marine natural products chemistry as an evolutionary narrative. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 115–154

  • Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT (2000) Current protocols in protein science. Wiley, Chichester

  • Custodio MR, Prokic I, Steffen R, Koziol C, Borojevic R, Brümmer F, Nickel M, Müller WEG (1998) Primmorphs generated from dissociated cells of the sponge Suberites domuncula: a model system for studies of cell proliferation and cell death. Mech Ageing Dev 105:45–59

    CAS  PubMed  Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in protein. In: Dayhoff MO (ed) Atlas of protein sequence and structure. National Biomedical Research Foundation, Washington, DC, pp 345–352

  • De Vet EC, van den Bosch H (1998) Nucleotide sequence of alkyl-dihydroxyacetonephosphate synthase cDNA from Dictyostelium discoideum. Biochem Biophys Res Commun 252:629–633

    Article  PubMed  Google Scholar 

  • De Vet EC, Prinsen HC, van den Bosch H (1998) Nucleotide sequence of a cDNA clone encoding a Caenorhabditis elegans homolog of mammalian alkyl-dihydroxyacetonephosphate synthase: evolutionary switching of peroxisomal targeting signals. Biochem Biophys Res Commun 242:277–281

    Article  PubMed  Google Scholar 

  • Dong CD, Yan DD, Tournier C, Whitmarsh AJ, Xu J, Davis RJ, Flavell RA (2000) JNK is required for effector T-cell function but not for T-cell activation. Nature 405:91–94

    Article  CAS  PubMed  Google Scholar 

  • Ebel R, Brenzinger M, Kunze A, Gross H, Proksch P (1997) Wound activation of prototoxins in the marine sponge Aplysina aerophoba. J Chem Ecol 23:1451–1462

    CAS  Google Scholar 

  • Faulkner DJ (2000) Marine natural products. Nat Prod Rep 17:7–55

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1993) PHYLIP, ver 3.5. University of Washington, Seattle

  • Fraaije MW, van den Heuvel RHH, van Berkel WJH, Mattevi A (1999) Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J Biol Chem 274:35514–35520

    Article  CAS  PubMed  Google Scholar 

  • Gonzales JM, Moran MA (1997) Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 63:4237–4242

    PubMed  Google Scholar 

  • Iorizzi M, Minale L, Riccio R, Higa T, Tanaka J (1991) Starfish saponins, part 46. Steroidal glycosides and polyhydroxysteroids from the starfish Culcita novaeguineae. J Nat Prod (Lloydia) 54:1254–1264

    Google Scholar 

  • Kasimir S, Shönfeld W, Alouf JE, König W (1990) Effect of Staphylococcus aureus delta toxin on human granulocyte functions and platelet-activating factor metabolism. Infect Immun 58:1653–1659

    CAS  PubMed  Google Scholar 

  • Kissane JM, Robins E (1958) The fluorometric measurement of deoxyribonucleic acid in animal tissue with special reference to the central nervous system. J Biol Chem 233:184–188

    CAS  Google Scholar 

  • Kruse M, Müller IM, Müller WEG (1997) Early evolution of metazoan serine/threonine- and tyrosine kinases: identification of selected kinases in marine sponges. Mol Biol Evol 14:1326–1334

    CAS  PubMed  Google Scholar 

  • Kruse M, Steffen R, Batel R, Müller IM, Müller WEG (1999) Differential expression of allograft inflammatory factor 1 and of glutathione peroxidase during auto- and allograft response in marine sponges. J Cell Sci 112:4305–4313

    CAS  PubMed  Google Scholar 

  • Lodi T, Ferrero I (1993) Isolation of the DLD gene of Saccharomyces cerevisiae encoding the mitochondrial enzyme D-lactate ferricytochrome c oxidoreductase. Mol Gen Genet 238:315–324

    CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mattevi A, Fraaije MW, Mozzarelli A, Olivi L, Coda A, Berkel WJH (1997a) Crystal structure and inhibitor biding in the octameric flavoenzyme vanillyl-alcohol oxidase: the shape of the active-site cavity controls substrate specificity. Curr Biol 5:907–920

    CAS  Google Scholar 

  • Mattevi A, Fraaije MW, Coda A, Berkel WJH (1997b) Crystallization and preliminary X-ray analysis of the flavoenzyme vanillyl-alcohol oxidase from Penicillium simplicissimum. Proteins 27:601–603

    Article  CAS  PubMed  Google Scholar 

  • Müller WEG (1997) Origin of metazoan adhesion molecules and adhesion receptors as deduced from their cDNA analyses from the marine sponge Geodia cydonium. Cell Tissue Res 289:383–395

    PubMed  Google Scholar 

  • Müller WEG (2001) How was metazoan threshold crossed: the hypothetical Urmetazoa. Comp Biochem Physiol A 129:433–460

    Google Scholar 

  • Müller WEG, Müller IM (2003) Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43:281–292

    Google Scholar 

  • Müller WEG, Zahn RK, Beyer R, Falke D (1977a) 9-ß-D-Arabinofuranosyladenine as a tool to study herpes simplex virus DNA replication in vitro. Virology 76:787–796

    PubMed  Google Scholar 

  • Müller WEG, Zahn RK, Bittlingmeier K, Falke D (1977b) Inhibition of herpesvirus DNA-synthesis by 9-ß-D-arabinofuranosyladenosine in vitro and in vivo. Ann NY Acad Sci 284:34–48

    PubMed  Google Scholar 

  • Müller WEG, Batel R, Lacorn M, Steinhart H, Simat T, Lauenroth S, Hassanein H, Schröder HC (1998) Accumulation of cadmium and zinc in the marine sponge Suberites domuncula and its potential consequences on single-strand breaks and on expression of heat-shock protein: a natural field study. Mar Ecol Prog Ser 167:127–135

    Google Scholar 

  • Müller WEG, Blumbach B, Müller IM (1999a) Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum [Porifera] and those in vertebrates. Transplantation 68:1215–1227

    PubMed  Google Scholar 

  • Müller WEG, Wiens M, Batel R, Steffen R, Borojevic R, Custodio MR (1999b) Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula. Mar Ecol Prog Ser 178:205–219

    Google Scholar 

  • Müller WEG, Krasko A, Skorokhod A, Bünz C, Grebenjuk VA, Steffen R, Batel R, Müller IM, Schröder HC (2002) Histocompatibility reaction in the sponge Suberites domuncula on tissue and cellular level: central role of the allograft inflammatory factor 1. Immunogenetics 54:48–58

    Article  PubMed  Google Scholar 

  • Müller WEG, Wiens M, Müller IM, Schröder HC (2003) The chemokine networks in sponges: potential roles in morphogenesis, immunity and stem cell formation. Prog Mol Subcell Biol 34:103–143

    Google Scholar 

  • Nagan N, Zoeller RA (2001) Plasmalogens: biosynthesis and functions. Prog Lipid Res 40:199–229

    Article  CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments, ver 1.1.004. Distributed by the author. http://cris.com/~ketchup/genedoc.shtml

  • Noda N, Tsunefuka S, Tanaka R, Miyahara K (1992a) Isolation and characterization of eight 1-O-alkyl-sn-glycero-3-phosphocholines from the crude drug "Jiryu" (the earthworm, Pheretima asiatica). Chem Pharm Bull (Tokyo) 40:2756–2758

    Google Scholar 

  • Noda N, Tsunefuka S, Tanaka R, Miyahara K (1992b) Isolation of two 1-O-alkyl-sn-glycero-3-phosphocholines from the earthworm, Pheretima asiatica. Chem Pharm Bull (Tokyo) 40:1349–1351

    Google Scholar 

  • Noda N, Tanaka R, Nishi M, Inoue S, Miyahara K (1993) Isolation and characterization of seven lyso platelet-activating factors and two lyso phosphatidylcholines from the crude drug "Suitetsu" (the leech, Hirudo nipponica). Chem Pharm Bull (Tokyo) 41:1366–1368

    Google Scholar 

  • Pawlik JR, Puyana M, Fenical W (2002) Just how "optimized" are the chemical defenses in marine sponges? In: Abstracts 3rd European conference on marine natural products. Universität München, München, p 57

  • Perez T, Garrabou J, Sartoretto S, Harmelin JG, Francour P, Vacelet J (2000) Mortalité massive d'invertébrés marins: un événement san précédent en Méditerranée nord-occidentale. CR Acad Sci Ser III Sci Vie 323:853–865

    Article  CAS  Google Scholar 

  • Pfam database (2001) Protein families: database of alignments and HMMs. Available via INTERNET. http://www.sanger.ac.uk/cgi-bin/Pfam

    Google Scholar 

  • Proksch P (1994) Defensive role for secondary metabolites from marine sponges and sponge-feeding nudibranchs. Toxicon 32:639–655

    CAS  PubMed  Google Scholar 

  • Proksch P, Edrada RA, Ebel R (2002) Drugs from the sea—current status and microbiological implications. Appl Microbiol Biotechnol 59:125–134

    Article  CAS  PubMed  Google Scholar 

  • Sarà M, Vacelet J (1973) Ecologie des démosponges. In: Grassé PP (ed) Traité de zoologie: Spongiaires, tome III (1). Masson, Paris, pp 462–576

  • Sarma AS, Daum T, Müller WEG (1993) Secondary metabolites from marine sponges. Akademie gemeinnütziger Wissenschaften zu Erfurt, Ullstein-Mosby, Berlin

  • Schröder HC, Krasko A, Batel R, Skorokhod A, Pahler S, Kruse M, Müller IM, Müller WEG (2000) Stimulation of protein (collagen) synthesis in sponge cells by a cardiac myotrophin-related molecule from Suberites domuncula. FASEB J 14:2022–2031

    PubMed  Google Scholar 

  • Schröder HC, Sudek S, De Caro S, De Rosa S, Perovic S, Steffen R, Müller IM, Müller WEG (2002) Synthesis of the neurotoxin quinolinic acid in apoptotic tissue from Suberites domuncula: cell biological, molecular biological and chemical analyses. Mar Biotechnol 4:546–558

    Article  Google Scholar 

  • Shin BA, Kim YR, Lee IS, Sung CK, Hong J, Sim C, Im KS, Jung JH (1999) Lyso-PAF analogues and lysophosphatidylcholines from the marine sponge Spirastrella abata as inhibitors of cholesterol biosynthesis. J Nat Prod (Lloydia) 62:1554–1557

    Google Scholar 

  • Steel HC, Cockeran R, Anderson A (2002) Platelet-activating factor and lyso-PAF possess direct antimicrobial properties in vitro. APMIS 110:158–164

    Article  CAS  PubMed  Google Scholar 

  • Sugiura T, Fukuda T, Miyamoto T, Waku K (1992) Distribution of alkyl and alkenyl ether-linked phospholipids and platelet-activating factor-like lipid in various species on invertebrates. Biochim Biophys Acta 1126:298–308

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Hashimoto A, Noda N, Miyahara K (1995) Two 1-alkyl-2-acyl choline glycerophospholipids having an arachidonoyl or eicosapentaenoyl group, from the clam worm (Marphysa sanguinea). Chem Pharm Bull (Tokyo) 43:156–158

    Google Scholar 

  • Tanaka R, Ishizaki H, Kawano S, Okuda H, Miyahara K, Noda N (1997) Fruiting-inducing activity and antifungal properties of lipid components in members of Annelida. Chem Pharm Bull (Tokyo) 45:1702–1704

    Google Scholar 

  • Thakur NL, Hentschel U, Krasko A, Pabel CT, Anil AC, Müller WEG (2003) Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for the defense. Aquat Microbial Ecol 31:77–83

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Ulevitch RJ, Tobias PS (1994) Recognition of endotoxin by cells leading to transmembrane signaling. Curr Opin Immunol 6:125–130

    Google Scholar 

  • Wagner C, Steffen R, Koziol C, Batel R, Lacorn M, Steinhart H, Simat T, Müller WEG (1998) Apoptosis in marine sponges: a biomarker for environmental stress (cadmium and bacteria). Mar Biol 131:411–421

    CAS  Google Scholar 

  • Wanders RJ, Dekker C, Hovarth VA, Schutgens RB, Tager JM, Van Laer P, Lecoutere D (1994) Human alkyldihydroxyacetonephosphate synthase deficiency: a new peroxisomal disorder. J Inherit Metab Dis 17:315–318

    CAS  PubMed  Google Scholar 

  • Wiens M, Koziol C, Hassanein HMA, Batel R, Müller WEG (1998) Expression of the chaperones 14-3-3 and HSP70 induced by PCB 118 (2,3′,4,4′,5-pentachlorobiphenyl) in the marine sponge Geodia cydonium. Mar Ecol Prog Ser 165:247–257

    CAS  Google Scholar 

  • Wiens M, Krasko A, Perovic S, Müller WEG (2003a) Caspase-mediated apoptosis in sponges: cloning and function of the phylogenetic oldest apoptotic proteases from Metazoa. Biochim Biophys Acta 1593:179–189

    Article  CAS  PubMed  Google Scholar 

  • Wiens M, Luckas B, Ammar MSA, Steffen R, Batel R, Diehl-Seifert B, Schröder HC, Müller WEG (2003b) Okadaic acid: a potential defense toxin for the sponges Suberites domuncula. Mar Biol 142:213–223

    CAS  Google Scholar 

  • Wiens M, Mangoni A, D'Esposito M, Fattorusso E, Korchagina N, Schröder HC, Grebenjuk VA, Krasko A, Batel R, Müller IM, Müller WEG (2003c) The molecular basis for the evolution of the metazoan bodyplan: extracellular matrix-mediated morphogenesis in marine demosponges. J Mol Evol 57:1–16

  • Wimmer W, Perovic S, Kruse M, Krasko A, Batel R, Müller WEG (1999) Origin of the integrin-mediated signal transduction: functional studies with cell cultures from the sponge Suberites domuncula. Eur J Biochem 178:156–165

    Article  Google Scholar 

  • Yayli N, Findlay JA (1994) Polar metabolites from the sea cucumber Cucumaria frondosa. J Nat Prod (Lloydia) 57:84–89

    Google Scholar 

  • Zimmermann GA, Prescott SM, McIntyre TM (1992) Platelet-activating factor: a fluid and cell-associated mediator of inflammation. In: Gallin JL, Goldstein IM, Syderman R (eds) Inflammation: basic principles and clinical correlates. Raven, New York, pp 149–176

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Acknowledgements

This work was supported by grants from the Deutsche Forschungsgemeinschaft (Mü 348/14), the Bundesministerium für Bildung und Forschung (project: Center of Excellence BIOTECmarin), the European Commission (project: NOMATEC) and the International Human Frontier Science Program (RG-333/96-M). All experiments performed during these studies complied with the rules and regulations of Germany. Note: the sequence from Suberites domuncula has been deposited in the EMBL/GenBank database as alkyl-dihydroxyacetonephosphate synthase, SDADS, under the accession number AJ306615.

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  1. Abteilung Angewandte Molekularbiologie, Institut für Physiologische Chemie, Universität Mainz, Duesbergweg 6, 55099, Mainz, Germany

    W. E. G. Müller, M. Klemt, N. L. Thakur & H. C. Schröder

  2. Dipartimento di Chimica delle Sostanze Naturali, University of Naples, Via Montesano 49, 80131, Naples, Italy

    A. Aiello, M. D'Esposito, M. Menna & E. Fattorusso

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  1. W. E. G. Müller
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  2. M. Klemt
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  3. N. L. Thakur
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  4. H. C. Schröder
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  5. A. Aiello
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  6. M. D'Esposito
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  8. E. Fattorusso
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Correspondence to W. E. G. Müller.

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Communicated by R. Cattaneo-Vietti, Genova

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Müller, W.E.G., Klemt, M., Thakur, N.L. et al. Molecular/chemical ecology in sponges: evidence for an adaptive antibacterial response in Suberites domuncula . Marine Biology 144, 19–29 (2004). https://doi.org/10.1007/s00227-003-1184-7

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