Abstract
Studies investigating disease resistance in marine plants have indicated that secondary metabolites may have important defensive functions against harmful marine microorganisms. The goal of this study was to systematically screen extracts from marine plants for antimicrobial effects against marine pathogens and saprophytes. Lipophilic and hydrophilic extracts from species of 49 marine algae and 3 seagrasses collected in the tropical Atlantic were screened for antimicrobial activity against five ecologically relevant marine microorganisms from three separate kingdoms. These assay microbes consisted of the pathogenic fungus Lindra thalassiae, the saprophytic fungus Dendryphiella salina, the saprophytic stramenopiles, Halophytophthora spinosa and Schizochytrium aggregatum, and the pathogenic bacterium Pseudoaltermonas bacteriolytica. Overall, 90% of all species surveyed yielded extracts that were active against one or more, and 77% yielded extracts that were active against two or more assay microorganisms. Broad-spectrum activity against three or four assay microorganisms was observed in the extracts from 48 and 27% of all species, respectively. The green algae Halimeda copiosa and Penicillus capitatus (Chlorophyta) were the only species to yield extracts active against all assay microorganisms. Among all assay microorganisms, both fungi were the most resistant to the extracts tested, with less than 21% of all extracts inhibiting the growth of either L. thalassiae or D. salina. In contrast, over half of all lipophylic extracts were active against the stramenopiles H. spinosa and S. aggregatum, and the bacterium P. bacteriolytica. Growth sensitivity to hydrophilic extracts varied considerably between individual assay microorganisms. While 48% of all hydrophilic extracts were active against H. spinosa, 27% were active against P. bacteriolytica, and only 14% were active against S. aggregatum. Overall, more lipophilic extracts inhibited microbial growth than hydrophilic extracts. The variability observed in the antimicrobial effects of individual extracts against each assay microorganism reflects the importance of choosing appropriate test microbes in assays from which ecologically relevant information is sought. Results from this survey demonstrate that antimicrobial activities are prevalent among extracts from marine algae and seagrasses, suggesting that antimicrobial chemical defenses are widespread among marine plants.
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References
Alker AP, Smith GW, Kim K (2001) Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia 460:105–111
Andrews JH (1976) The pathology of marine algae. Biol Rev 51:211–253
Andrews JH (1979) Pathology of seaweeds. Experientia 35:429–570
Ballantine DL, Gerwick WH, Velez SM, Alexander E, Guevara P (1987) Antibiotic activity of lipid-soluble extracts from Caribbean marine algae. Hydrobiologia 151/152:463–469
Ballesteros E, Martin D, Uriz MJ (1992) Biological activity of extracts from some Mediterranean macrophytes. Bot Mar 35:481–485
Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR (2003) Marine natural products. Nat Prod Rep 20:1–48
Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR (2004) Marine natural products. Nat Prod Rep 21:1–49
Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR (2005) Marine natural products. Nat Prod Rep 22:15–61
Bremer GB (1995) Lower marine fungi (Labyrinthulomycetes) and decay of mangrove leaf litter. Hydrobiologia 295:89–95
Burkholder PR, Burkholder LM, Almodovar LR (1960) Antibiotic activity of some marine algae of Puerto Rico. Bot Mar 2:149–156
Caccamese S, Azzolina R, Furnari G, Cormaci M, Grasso S (1980) Antimicrobial and antiviral activities of extracts from Mediterranean algae. Bot Mar 23:285–288
Caccamese S, Azzolina R, Furnari G, Cormaci M, Grasso S (1981) Antimicrobial and antiviral activities of some marine algae from eastern Sicily. Bot Mar 24:365–367
Caccamese S, Toscano MG, Furnari M, Cormaci M (1985) Antimicrobial activity of red and brown algae from Southern Italy Coast. Bot Mar 28:505–507
Correa JA (1997) Infectious diseases of marine algae: current knowledge and approaches. Prog Phycol Res 12:49–180
Cronin G, Lindquist N, Hay ME, Fenical W (1995) Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis. Mar Ecol Prog Ser 119:265–273
Da Gama BAP, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue-Valentin Y (2002) Effects on seaweed secondary metabolites on biofouling. Biofouling 18:13–20
Devi P, Solimabi W, D’Souza L, Sonak S, Kamat SY, Singbal SYS (1997) Screening of some marine plants for activity against marine fouling bacteria. Bot Mar 40:87–91
Echigoya R, Rhodes LO, Oshima Y, Satake M (2005) The structure of five new antifungalo and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand. Harmful Algae 4:383–389
Elston R, Lockwood GS (1983) Pathogenesis of vibriosis in cultured juvenile red abalone, Haliotis rufescens Swainson. J Fish Dis 6:111
Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28:1971–1985
Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–48
Gil-Turnes S, Fenical W (1992) Embryos of Homarus americanus are protected by epibiotic bacteria. Biol Bull 182:105–108
Gil-Turnes S, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118
Hammerschmidt R (1999) Phytoalexins: what have we learned after 60 years? Annu Rev Phytopathol 37:285–306
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Vasta GR (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505–1510
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Osfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Hay ME (1996) Marine chemical ecology: what’s known and what’s next. Mar Ecol Prog Ser 200:103–134
Hellio C, Bremer G, Pons AM, Le Gal Y, Bourgougnon N (2000) Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany, France. Appl Microbiol Biotechnol 54:543–549
Hellio C, De La Broise D, Dufosse L, Le Gal Y, Bourgougnon N (2001) Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar Environ Res 52:231–247
Hellio C, Marechal J, Veron B, Bremer G, Clare A, Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany Coast (France). Mar Biotechnol 6:67–82
Hornsey IS, Hide D (1974) The production of antimicrobial substances by British marine algae I. Antibiotic producing marine algae. Br phycol J 9:353–361
Hyde KD, Jones GEB, Leano E, Pointing SB, Poonyth AD, Virjmoed LLP (1998) Role of fungi in marine ecosystems. Biodivers Conserv 7:1147–1161
Ingham JL (1972) Phytoalexins and other natural products as factors in plant disease resistance. Bot Rev 38:343–424
Ingham JL (1973) Disease resistance in higher plants. Phytopathol Z 78:314–335
Jensen PR, Jenkins KM, Porter D, Fenical W (1998) Evidence that a new antibiotic flavone glycoside chemically defends the seagrass Thalassia testudinum against a zoosporic fungi. Appl Environ Microbiol 64:1490–1496
Kazama FY (1979) Pythium “red rot disease” of Porphyra. Experientia 35:443
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic, New York
König G, Wright A (1997) Laurencia rigida: chemical investigations of its antifouling dichloromethane extract. J Nat Prod 60:967–970
Kubanek J, Jensen PR, Keifer PA, Sullards C, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci USA 100:6919–6921
Leaño EM (2002) Ecology of straminipiles from mangrove habitats. In: Hyde KD (ed) Fungi in marine environments. Fungal diversity research series 7:111–134
Lightner DV, Fontaine CT (1975) A mycosis of the American lobster, Homarus americanus, caused by Fusarium sp. J Invertebr Pathol 25:239
Littler MM, Littler DS (1995) Impact of CLOD pathogen on pacific coral reefs. Science 267:1356–1360
Littler MM, Littler DS (eds) (2000) Caribbean reef plants. Off Shore Graphics Inc., Washington
Martin Y, Bonnefont JL, Chancerelle L (2002) Gorgonian mass mortality during the late summer in French Mediterranean coastal waters: the bacterial hypothesis. Water Res 36:779–782
Maximilien R, de Nys R, Holmström C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233–246
Moss ST (1986) Biology and phylogeny of the Labyrinthulales and Thrausochytriales. In: Moss ST (ed) The biology of marine fungi. Cambridge University Press, Cambridge, pp 105–129
Muehlstein LK, Porter D, Short FT (1991) Labyrinthula zosterae sp. nov. the causative agent of wasting disease in eelgrass Zostera marina. Mycologia 83:180
Muroga K (2001) Viral and bacterial diseases of marine fish and shellfish in Japanese hatcheries. Aquaculture 202:23–44
Nakagiri A (2002) Halophytophthora species from tropical and subtropical mangroves: a review of their characteristics. In: Hyde KD (ed) Fungi in marine environments. Fungal diversity research series 7:1–14
Paul VJ (ed) (1992) Ecological roles of marine natural products. Comstock Press, Ithaca
Pesando D (ed) (1990) Introduction to applied phycology. SPB Academic, The Hague, pp 3–26
Porter D (1986) Mycoses of marine organisms: an overview of pathogenic fungi. In: Moss ST (ed) The biology of marine fungi. Cambridge University Press, New York, pp 141–154
Pratt R, Mautner H, Gardner GMG, Sha H, Dufenoy J (1951) Antibiotic activity of seaweed extracts. J Am Pharm Assoc 40:575
Puglisi MP, Tan LT, Jensen PR, Fenical W (2004) Capisterones A and B from the tropical green alga Penicillus capitatus: unexpected anti-fungal defenses targeting the marine pathogen Lindra thalassiae. Tetrahedron 60:7035–7039
Pugh GJF, Jones EBG (1986) Antarctic marine fungi: a preliminary account. In: Moss ST (ed) The biology of marine fungi. Cambridge University Press, Cambridge, pp 323–330
Raghukumar S, Anil AC, Khandeparker L, Patil JS (2000) Thraustochytrid protests as a component of marine microbial films. Mar Biol 136:603–609
Rao PS, Parekh KS (1981) Antibacterial activities of Indian seaweed extracts. Bot Mar 24:577–582
Reichelt JL, Borowitzka MA (1984) Antimicrobial activity from marine algae: Results of a large-scale screening programme. Hydrobiologia 116/117:158–168
Richardson L (1998) Coral diseases: what is really known? Trends Ecol Evol 13:438
Rinehart KL, Shaw PD, Shield LS, Gloer JB, Harbour GC, Koker MES, Samain D, Schwartz RE, Tymiak AA, Weller DL, Carter GT, Munro MHG, Hughes JRG, Renis HE, Swynenberg EB, Stringfellow DA, Varva JJ, Coats JH, Zurenko GE, Kuentzel SL, Li LH, Bakus GJ, Brusca RC, Craft LL, Young DN, Connor JL (1981) Marine natural products as sources of antiviral, antimicrobial, and antineoplastic agents. Pure Appl Chem 53:795–817
Sawabe T, Makino H, Tatsumi M, Nakano K, Tajima K, Iqbal MM, Yumoto I, Ezura Y, Christen R (1998) Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. Int J Syst Bacteriol 48:769–774
Short FT, Muehlstein LK, Porter D (1987) Eelgrass wasting disease: cause and recurrence of a marine epidemic. Biol Bull 173:557–562
Sieburth JM (1964) Antibacterial substances produced by marine algae. Develop Ind Microbiol 5:124–134
Sieburth JM, Conover JT (1965) Sargassum tannin, an antibiotic which retards fouling. Nature 208:52–53
Sparks AK (1985) Synopsis of invertebrate pathology. Elsevier, Amsterdam
Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629
Steinberg PD, de Nys R, Kjelleberg S (2002) Chemical cues for surface colonization. J Chem Ecol 28:1935–1951
Vlachos V, Critchley AT, Von Holy A (1996) Establishment of a protocol for testing antimicrobial activity in southern African macroalgae. Microbios 88:115–123
Acknowledgements
We thank Professor Joseph R. Pawlik, University of North Carolina at Wilmington, for his generous invitation to participate in his research expedition aboard the R/V Seward Johnson (NSF OCE97-11255 and OCE00-95724). We also thank the government of the Bahamas for allowing us to conduct research in their territorial waters. We thank Professors E. B. Gareth Jones, David Porter, and Tomoo Sawabe for providing assay microorganisms. We thank Chris Kauffman, Sara Kelly, Tatum Neely, Allan Spyere, Tracy Mincer, Craig Fairchild, and Micha Ilan for their assistance. This research was supported by a grant from the National Science Foundation NSF grant CHE01-11370 to WF and conducted in accordance with the current environmental regulations of the Bahamas.
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Communicated by P.W. Sammarco, Chauvin
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Engel, S., Puglisi, M.P., Jensen, P.R. et al. Antimicrobial activities of extracts from tropical Atlantic marine plants against marine pathogens and saprophytes. Mar Biol 149, 991–1002 (2006). https://doi.org/10.1007/s00227-006-0264-x
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DOI: https://doi.org/10.1007/s00227-006-0264-x