As the need for new and more effective antibiotics increases, untapped sources of biodiversity are being explored in an effort to provide lead structures for drug discovery. Endophytic fungi from marine macroalgae have been identified as a potential source of biologically active natural products, although data to support this is limited. To assess the antibiotic potential of temperate macroalgal endophytes we isolated endophytic fungi from algae collected in the Bay of Fundy, Canada and screened fungal extracts for the presence of antimicrobial compounds. A total of 79 endophytes were isolated from 7 species of red, 4 species of brown, and 3 species of green algae. Twenty of the endophytes were identified to the genus or species level, with the remaining isolates designated codes according to their morphology. Bioactivity screening assays performed on extracts of the fermentation broths and mycelia of the isolates revealed that 43 endophytes exhibited antibacterial activity, with 32 displaying antifungal activity. Endophytic fungi from Bay of Fundy macroalgae therefore represent a significant source of antibiotic natural products and warrant further detailed investigation.
References
[1]
Appelbaum, P.C. 2012 and beyond: Potential for the start of a second pre-antibiotic era? J. Antimicrob. Chemother. 2012, 67, 2062–2068, doi:10.1093/jac/dks213.
[2]
Ashkenazi, S. Beginning and possibly the end of the antibiotic era. J. Paediatr. Child Health 2012, 49, 179–182.
[3]
Spellberg, B.; Bartlett, J.G.; Gilbert, D.N. The future of antibiotics and resistance. N. Engl. J. Med. 2013, 368, 299–302, doi:10.1056/NEJMp1215093.
[4]
Chopra, I. The 2012 garrod lecture: Discovery of antibacterial drugs in the 21st century. J. Antimicrob. Chemother. 2013, 68, 496–505, doi:10.1093/jac/dks436.
[5]
Butler, M.S.; Cooper, M.A. Screening strategies to identify new antibiotics. Curr. Drug Targets 2012, 13, 373–387, doi:10.2174/138945012799424624.
[6]
Debbab, A.; Aly, A.H.; Proksch, P. Endophytes and associated marine derived fungi-ecological and chemical perspectives. Fungal Divers. 2012, 57, 45–83, doi:10.1007/s13225-012-0191-8.
[7]
Suryanarayanan, T.S. Fungal Endosymbionts of Seaweeds. In Biology of Marine Fungi; Raghukumar, C., Ed.; Springer: Berlin, Germany, 2012; pp. 53–69.
[8]
Jones, E.B.G.; Pang, K.-L.; Stanley, S.J. Fungi from Marine Algae. In Marine Fungi and Fungal-Like Organisms; Jones, E.B.G., Pang, K.-L., Eds.; Walter de Gruyter: Berlin, Germany, 2012; pp. 329–344.
[9]
Suryanarayanan, T.S.; Venkatachalam, A.; Thirunavukkarasu, N.; Ravishankar, J.P.; Doble, M.; Geetha, V. Internal mycobiota of marine macroalgae from the tamilnadu coast: Distribution, diversity and biotechnological potential. Bot. Mar. 2010, 53, 457–468.
[10]
Schulz, B.; Boyle, C.; Draeger, S.; Rommert, A.K.; Rohn, K. Endophytic fungi: A source of novel biologically active secondary metabolites. Mycol. Res. 2002, 106, 996–1004, doi:10.1017/S0953756202006342.
[11]
Flewelling, A.J.; Johnson, J.A.; Gray, C.A. Isolation and bioassay screening of fungal endophytes from north atlantic marine macroalgae. Bot. Mar. 2013, 56, 287–297.
[12]
Petrini, O.; Fisher, P.; Petrini, L. Fungal endophytes of bracken (Pteridium aquilinum), with some reflections on their use in biological control. Sydowia 1992, 44, 282–293.
[13]
White, T.J.; Bruns, T.D.; Lee, S.B.; Taylor, J.W. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., Eds.; Academic Press: New York, NY, USA, 1990; pp. 315–322.
[14]
Dobranic, J.K.; Johnson, J.A.; Alikhan, Q.R. Isolation of endophytic fungi from eastern larch (Larix laricina) leaves from new-brunswick, Canada. Can. J. Microbiol. 1995, 41, 194–198, doi:10.1139/m95-026.
[15]
Suryanarayanan, T.S.; Kumaresan, V.; Johnson, J.A. Foliar fungal endophytes from two species of the mangrove Rhizophora. Can. J. Microbiol. 1998, 44, 1003–1006.
[16]
Bates, C.R.; Saunders, G.; Chopin, T. Historical versus contemporary measures of seaweed biodiversity in the bay of fundy. Botany 2009, 87, 1066–1076, doi:10.1139/B09-067.
[17]
South, G.R. A checklist of marine algae of eastern canada, 2nd revision. Can. J. Bot. 1984, 62, 680–704, doi:10.1139/b84-102.
[18]
Fries, N.; Thorentolling, K. Identity of fungal endophyte of Ascophyllum with Mycosphaerella ascophylli established by means of fluorescent-antibody technique. Bot. Mar. 1978, 21, 409–411.
[19]
Fries, N. Physiological characteristics of Mycosphaerella ascophylli, a fungal endophyte of the marine brown alga Ascophyllum nodosum. Physiol. Plant. 1979, 45, 117–121, doi:10.1111/j.1399-3054.1979.tb01674.x.
[20]
Fries, L. Ascophyllum nodosum (Phaeophyta) in Axenic culture and its response to the endophytic fungus Mycosphaerella ascophylli and epiphytic bacteria. J. Phycol. 1988, 24, 333–337.
[21]
Garbary, D.J.; Gautam, A. The Ascophyllum/Polysiphonia/Mycosphaerella symbiosis. I. Population ecology of Mycosphaerella from Nova Scotia. Bot. Mar. 1989, 32, 181–186.
[22]
Garbary, D.J.; Burke, J.; Tian, L.N. The Ascophyllum/Polysiphonia/Mycosphaerella symbiosis. II. Aspects of the ecology and distribution of Polysiphonia lanosa in Nova Scotia. Bot. Mar. 1991, 34, 391–401.
[23]
Stanley, S.J. Observations on the seasonal occurance of marine endophytic and parasitic fungi. Can. J. Bot. 1992, 70, 2089–2096, doi:10.1139/b92-259.
[24]
Garbary, D.J.; London, J.F. The Ascophyllum/Polysiphonial/Mycosphaerella symbiosis. V. Fungal infection protects A. nosodum from desiccation. Bot. Mar. 1995, 38, 529–533.
[25]
Osterhage, C.; Kaminsky, R.; Konig, G.M.; Wright, A.D. Ascosalipyrrolidinone A, an antimicrobial alkaloid, from the obligate marine fungus Ascochyta salicorniae. J. Org. Chem. 2000, 65, 6412–6417, doi:10.1021/jo000307g.
[26]
Abdel-Lateff, A.; Fisch, K.M.; Wright, A.D.; Konig, G.M. A new antioxidant isobenzofuranone derivative from the algicolous marine fungus Epicoccum sp. Planta Med. 2003, 69, 831–834, doi:10.1055/s-2003-43209.
[27]
Deckert, R.; Garbary, D. Ascophyllum and its symbionts. VI. Microscopic characterization of the Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) symbiotum. Algae 2005, 20, 225–232, doi:10.4490/ALGAE.2005.20.3.225.
[28]
Garbary, D.J.; Jamieson, M.M.; Fraser, S.J.; Ferguson, C.A.; Cranston, P.S. Ascophyllum (Phaeophyceae) and its symbionts. IX. A novel symbiosis between Halocladius variabilis (Chironomidae, Insecta) and Elachista fucicola (Elachistaceae, Phaeophyceae) from marine rocky shores of Nova Scotia. Symbiosis 2005, 40, 61–68.
[29]
Schulz, B.; Draeger, S.; dela Cruz, T.E.; Rheinheimer, J.; Siems, K.; Loesgen, S.; Bitzer, J.; Schloerke, O.; Zeeck, A.; Kock, I.; et al. Screening strategies for obtaining novel, biologically active, fungal secondary metabolites from marine habitats. Bot. Mar. 2008, 51, 219–234.
[30]
Xu, H.; Deckert, R.J.; Garbary, D.J. Ascophyllum and its symbionts. X. Ultrastructure of the interaction between A. nodosum (Phaeophyceae) and Mycophycias ascophylli (Ascomycetes). Botany 2008, 86, 185–193, doi:10.1139/B07-122.
[31]
Webber, F.C. Observations on the structure, life history and biology of Mycosphaerella ascophylli. Trans. Br. Mycol. Soc. 1967, 50, 583–601, doi:10.1016/S0007-1536(67)80090-1.