Abstract
We investigated the relationship between the structures of pyrrole-containing alkaloids from marine sponges of the genus Agelas and their capacity to deter feeding by the omnivorous Caribbean reef fish, Thalassoma bifasciatum. Seven natural products were assayed at volumetric concentrations of 1, 5, and 10 mg/ml: dispacamide A, keramadine, oroidin, midpacamide, 4,5-dibromopyrrole-2-carboxylic acid, 4,5-dibromopyrrole-2carboxamide, and racemic longamide A. We also assayed 14 structural analogs obtained mostly by chemical synthesis. Of the seven natural products, only rac-longamide A was not significantly deterrent at any of the assay concentrations. The pyrrole moiety was required for feeding inhibition activity, while the addition of the imidazole group enhanced this activity. Variously functionalized imidazoles lacking the pyrrole moiety were not deterrent. Combinations of the natural products appeared to have an additive effect on feeding inhibition; there was no evidence of synergy. Given their high concentrations in sponge tissue, dispacamide A and oroidin most probably serve as the primary chemical defenses of many Agelas sp., while minor compounds such as keramadine are not present in high enough concentrations to contribute much to chemical defense.
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REFERENCES
Assmann, M., Lichte, E., Pawlik, J. R., and KÖck, M. 2000. Chemical defenses of the Caribbean sponges Agelas wiednemayeri and Agelas conifera. Submitted to Mar. Ecol. Prog. Ser.
Bailey, D. M., and Johnson, R. E. 1973. Pyrrole antibacterial agents. 2. 4,5-Dihalopyrrole-2-carboxylic acid derivatives. J. Med. Chem. 16:1300–1302.
Braekman, J. C., Daloze, D., Moussiaux, B., Stoller, C., and Deneubourg, F. 1989. Sponge secondary metabolites: new results. Pure Appl. Chem. 61:509–512.
Cafieri, F., Fattorusso, E., Mangoni, A., and Taglialatela-Scafati, O. 1995. Longamide and 3,7-dimethylisoguanine, two novel alkaloids from the marine sponge Agelas longissima. Tetrahedron Lett. 36:7893–7896.
Cafieri, F., Fattorusso, E., Mangoni, A., and Taglialatela-Scafati, O. 1996. Dispacamides, anti-histamine alkaloids from Caribbean Agelas sponges. Tetrahedron Lett. 37:3587–3590.
Cafieri, F., Carnuccio, R., Fattorusso, E., Taglialatela-Scafati, O., and Vallefuoco, T. 1997. Anti-histaminic activity of bromopyrrole alkaloids isolated from Caribbean Agelas spones. Bioorg. Med. Chem. Lett. 7:2283–2288.
Cafieri, F., Fattorusso, E., and Taglialatela-Scafati, O. 1998. Novel bromopyrrole alkaloids from the sponge Agelas dispar. J. Nat. Prod. 61:122–125.
Chanas, B., and Pawlik, J. R. 1995. Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar. Ecol. Prog. Ser. 127:195–211.
Chanas, B., Pawlik, J. R., Lindel, T., and Fenical, W. 1996. Chemical defense of the Caribbean sponge Agelas clathrodes. J. Exp. Mar. Biol. Ecol. 208:185–196.
Chevolot, L., Padua, S., Ravi, B. N., Blyth, P. C., and Scheuer, P. J. 1977. Isolation of 1-methyl-4,5-dibromopyrrole-2-carboxylic acid and its 3′-(hydantoyl)propylamide (midpacamide) from a marine sponge. Heterocycles 7:891–894.
De Nanteuil, G., Ahond, A., Guilhem, J., Poupat, C., Trans Huu Dau, E., Potier, P., Pusset, M., Pusset, J., and Laboute, P. 1985. Isolement et identification des metabolites d'une nouvelle espece de spongaire, Pseudaxinyssa cantharella. Tetrahedron 41:6019–6033.
Duffy, J. E., and Paul, V. J. 1992. Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339.
Enriz, R. D., Baldoni, H. A., Jauregui, E. A., Sosa, M. E., Tonn, C. E., and Giordano, O. S. 1994. Structure-activity relationship of clerodane diterpenoids acting as antifeeding agents. J. Agric. Food Chem. 42:2958–2963.
Fathi-Afshar, R., and Allen, T. M. 1988. Biologically active metabolites from Agelas mauritiana. Can. J. Chem. 66:45–50.
Faulkner, D. J. 1998. Marine natural products. Nat. Prod. Rep. 15:113–158.
Forenza, S., Minale, L., and Riccio, R. 1971. New bromopyrrole derivatives from the sponge Agelas oroides. J. Chem. Soc. Chem. Commun. 1971:1129–1130.
Gonzalez-Coloma, A., Guadano, A., Gutierrez, C., Cabrera, R., De La PeÑa, E., De La Fuente, G., and Reina, M. 1998. Antifeedant delphinium diterpenoid alkaloids. Structure-activity relationships. J. Agric. Food Chem. 46:286–290.
Gunasekera, S. P., Cranick, S., and Longley, R. E. 1989. Immunosuppressive compounds from a deep water marine sponge, Agelas flabelliformis. J. Nat. Prod. 52:757–761.
Hay, M. E., Piel, J., Boland, W., and Schnitzler, I. 1998. Seaweed sex pheromones and their degradation products frequently suppress amphipod feeding but rarely suppress sea urchin feeding. Chemoecology 8:91–98.
Hixon, M. A. 1983. Fish grazing and community structure of coral reefs and algae: A synthesis of recent studies, pp. 79–87, in M. S. Reaka (ed.). The Ecology of Deep and Shallow Coral Reefs. Symposia series for undersea research, NOAA /NURP, Washington, DC.
JimÉnez, C., and Crews, P. 1994. Mauritamide A and accompanying oroidin alkaloids from the sponge Agelas mauritiana. Tetrahedron Lett. 35:1375–1378.
KÖnig, G. M., Wright, A. D., and Linden, A. 1998. Antiplasmodial and cytotoxic metabolites from the maltese sponge Agelas oroides. Planta Med. 64:443–447.
Lindel, T., and HochgÜrtel, M. 1998. The alkyne pathway to keramadine from the marine sponge Agelas sp. Tetrahedron Lett. 39:2541–2544.
Lindel, T., and Hoffmann, H. 1997a. Synthesis of dispacamide from the maine sponge Agelas dispar. Tetrahedron Lett. 38:8935–8938.
Lindel, T., and Hoffmann, H. 1997b. Synthesis of rac-midpacamide and the spiro-cyclization of its precursor. Liebigs Ann. Recueil 1997:1525–1528.
Lindel, T., Junker, J., and KÖck, M. 1999. 2D-NMR-guided constitutional analysis of organic compounds employing the computer program COCON. Eur. J. Org. Chem. 1999:573–577.
Mancini, I., Guella, G., Amade, P., Roussakis, C., and Pietra, F. 1997. Hanishin, a semiracemic, bioactive C9 alkaloid of the axinellid sponge Acanthella carteri from the Hanish Islands. A shunt metabolite? Tetrahedron Lett. 38:6271–6274.
Meanwell, N. A., Roth, H. R., Smith, E. C. R., Wedding, D. L., and Wright, J. J. K. 1991. Diethyl 2,4-dioxoimidazoline-5-phosphonates: Horner-Wadsworth-Emmons reagents for the mild and efficient preparation of C-5 unsaturated hydantoin derivatives. J. Org. Chem. 56:6897–6904.
Messchendorp, L., Gols, G. J. Z., and Van Loon, J. J. A. 1998. Behavioral effects and sensory detection of drimane deterrents in Myzus persicae and aphis gossypii nymphs. J. Chem. Ecol. 24:1433–1446.
Moe, O. A., and Warner, D. T. 1949. 1,4 Addition reactions. III. The addition of cyclic imides to α,β-unsaturated aldehydes. A synthesis of β-alanine hydrochloride. J. Am. Chem. Soc. 71:1251–1253.
Mullin, C. A., Gonzalez-Coloma, A., Gutierrez, C., Reina, M., Eichenseer, H., Hollister, B., and Chyb, S. 1997. Antifeedant effects of some novel terpenoids on chrysomelidae beetles: Comparisons with alkaloids on an alkaloid-adapted an nonadapted species. J. Chem. Ecol. 23:1851–1866.
Nakamura, H., Ohizumi, Y., Kobayashi, J., and Hirata, Y. 1984. Keramadine, a novel antagonist of serotonergic receptors isolated from the Okinawan sea sponge Agelas sp. Tetrahedron Lett. 25:2475–2478.
Pawlik, J. R. 1993. Marine invertebrate chemical defenses. Chem. Rev. 93:1911–1922.
Pawlik, J. R., and Fenical, W. 1992. Chemical defense of Pterogorgia anceps, a Caribbean gorgonian coral. Mar. Ecol. Prog. Ser. 87:183–188.
Pawlik, J. R., Burch, M. T., and Fenical, W. 1987. Patterns of chemical defense among Caribbean gorgonian corals: A preliminary survey. J. Exp. Mar. Biol. Ecol. 108:55–66.
Pawlik, J. R., Chanas, B., Toonen, R. J., and Fenical, W. 1995. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar. Ecol. Prog. Ser. 127:183–194.
Pennings, S. C., Pablo, S. R., Paul, V. J., and Duffy, E. 1994. Effects of sponge secondary metabolites in different diets on feeding by three groups of consumers. J. Exp. Mar. Biol. Ecol. 180:137–149.
Randall, J. R., and Hartman, W. D. 1968. Sponge-feeding fishes of the West Indies. Mar. Biol. 1:216–225.
Rogers, S. D., and Paul, V. J. 1991. Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Mar. Ecol. Prog. Ser. 77:221–232.
Rowan, D. D., Hunt, M. B., and Gaynor, D. L. 1986. Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acromonium lolii. J. Chem. Soc. Chem. Commun. 1986:935–936.
Tsukamoto, S., Kato, H., Hirota, H., and Fusetani, N. 1996. Ceratinamides A and B: New antifouling dibromotyrosine derivatives from the marine sponge Pseudoceratina purpurea. Tetrahedron 52:8181–8186.
Umeyana, A., Ito, S., Yuasa, E., Arihara, S., and Yamada, T. 1998. A new bromopyrrole alkaloid and the optical resolution of the racemate from the marine sponge Homaxinella sp. J. Nat. Prod. 61:1433–1434.
Vervoort, H. C., Pawlik, J. R., and Fenical, W. 1998. Chemical defense of the Caribbean ascidian Didemnum conchyliatum. Mar. Ecol. Prog. Ser. 164:221–228.
Walker, R. P., Faulkner, D. J., Van Engen, D., and Clardy, J. 1981. Sceptrin, an antimicrobial agent from the sponge Agelas sceptrum. J. Am. Chem. Soc. 103:6772–6773.
Wilson, D. M., Puyana, M., Fenical, W., and Pawlik, J. R. 1999. Chemical defense of the Caribbean reef sponge Axinella corrugata against predatory fishes. J. Chem. Ecol. 25:2811–2823.
Yamazaki, T., Benedetti, E., Kent, D., and Goodman, M. 1994. Konformationsvoraussetzungen für den süssen Geschmack von Dipeptiden und Dipeptidmimetica. Angew. Chem. 106:1502–1517.
Zar, J. H. 1984. Biostatistical Analysis, 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey.
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Lindel, T., Hoffmann, H., Hochgürtel, M. et al. Structure–Activity Relationship of Inhibition of Fish Feeding by Sponge-derived and Synthetic Pyrrole–Imidazole Alkaloids. J Chem Ecol 26, 1477–1496 (2000). https://doi.org/10.1023/A:1005591826613
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DOI: https://doi.org/10.1023/A:1005591826613