Planta Med 2016; 82(09/10): 832-842
DOI: 10.1055/s-0042-103496
Reviews
Georg Thieme Verlag KG Stuttgart · New York

Secondary Metabolites from the Marine Algal-Derived Endophytic Fungi: Chemical Diversity and Biological Activity

Peng Zhang
1   Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
2   Tobacco Research Institute of Chinese Academy of Agricultural Sciences, Qingdao, China
,
Xin Li
1   Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
,
Bin-Gui Wang
1   Laboratory of Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
› Institutsangaben
Weitere Informationen

Publikationsverlauf

received 09. September 2015
revised 08. Februar 2016

accepted 12. Februar 2016

Publikationsdatum:
24. Mai 2016 (online)

Abstract

Marine algal-derived endophytic fungi have attracted considerable attention in the most recent two decades due to their prolific production of structurally diverse secondary metabolites with various biological activities. This review summarizes a total of 182 natural products isolated from marine algal-derived endophytic fungi in the past two decades. The emphasis is on the unique chemical diversity of these metabolic products, together with relevant biological activities.

 
  • References

  • 1 Strobel G, Daisy B. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 2003; 67: 491-502
  • 2 Bugni TS, Ireland CM. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 2004; 21: 143-163
  • 3 Strobel G, Daisy B, Castillo U, Harper J. Natural products from endophytic microorganisms. J Nat Prod 2004; 67: 257-268
  • 4 Rateb ME, Ebel R. Secondary metabolites of fungi from marine habitats. Nat Prod Rep 2011; 28: 290-344
  • 5 Kjer J, Debbab A, Aly AH, Proksch P. Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat Protoc 2010; 5: 479-490
  • 6 Wang S, Li XM, Teuscher F, Li DL, Diesel A, Ebel R, Proksch P, Wang BG. Chaetopyranin, a benzaldehyde derivative, and other related metabolites from Chaetomium globosum, an endophytic fungus derived from the marine red alga Polysiphonia urceolata . J Nat Prod 2006; 69: 1622-1625
  • 7 Son BW, Choi JS, Kim JC, Nam KW, Kim DS, Chung HY, Kang JS, Choi HD. Parasitenone, a new epoxycyclohexenone related to gabosine from the marine-derived fungus Aspergillus parasiticus . J Nat Prod 2002; 65: 794-795
  • 8 Osterhage C, König GM, Jones PG, Wright AD. 5-Hydroxyramulosin, a new natural product produced by Phoma tropica, a marine-derived fungus isolated from the alga Fucus spiralis . Planta Med 2002; 68: 1052-1054
  • 9 Abdel-Lateff A, Klemke AC, König GM, Wright AD. Two new xanthone derivatives from the algicolous marine fungus Wardomyces anomalus . J Nat Prod 2003; 66: 706-708
  • 10 Ogawa A, Murakami C, Kamisuki S, Kuriyama I, Yoshida H, Sugawara F, Mizushina Y. Pseudodeflectusin, a novel isochroman derivative from Aspergillus pseudodeflectus a parasite of the sea weed, Sargassum fusiform, as a selective human cancer cytotoxin. Bioorg Med Chem Lett 2004; 14: 3539-3543
  • 11 Shigemori H, Kasai Y, Komatsu K, Tsuda M, Mikami Y, Kobayashi J. Sporiolides A and B, new cytotoxic twelve-membered macrolides from a marine-derived fungus Cladosporium species. Mar Drugs 2004; 2: 164-169
  • 12 Klemke C, Kehraus S, Wright AD, König GM. New secondary metabolites from the marine endophytic fungus Apiospora montagnei . J Nat Prod 2004; 67: 1058-1063
  • 13 Yang RY, Li CY, Lin YC, Peng GT, She ZG, Zhou SN. Lactones from a brown alga endophytic fungus (No. ZZF36) from the South China Sea and their antimicrobial activities. Bioorg Med Chem Lett 2006; 16: 4205-4208
  • 14 Teuscher F, Lin WH, Wray V, Edrada R, Padmakumar K, Proksch P, Ebel R. Two new cyclopentanoids from the endophytic fungus Aspergillus sydowii associated with the marine alga Acanthophora spicifera . Nat Prod Commun 2006; 1: 927-933
  • 15 Lang G, Mitova MI, Ellis G, van der Sar S, Phipps RK, Blunt JW, Cummings NJ, Cole ALJ, Munro MHG. Bioactivity profiling using HPLC/microtiter-plate analysis: application to a New Zealand marine alga-derived fungus, Gliocladium sp. J Nat Prod 2006; 69: 621-624
  • 16 Li Y, Li XF, Lee U, Kang JS, Choi HD, Son BW. A new radical scavenging anthracene glycoside, asperflavin ribofuranoside, and polyketides from a marine isolate of the fungus Microsporum . Chem Pharm Bull 2006; 54: 882-883
  • 17 Krali A, Kehraus S, Krick A, Eguereva E, Kelter G, Maurer M, Wortmann A, Fiebig HH, König GM. Arugosins G and H: prenylated polyketides from the marine-derived fungus Emericella nidulans var. acristata . J Nat Prod 2006; 69: 995-1000
  • 18 Krick A, Kehraus S, Gerhäuser CK, Nieger M, Maier A, Fiebig HH, Atodiresei I, Raabe G, Fleischhauer J, König GM. Potential cancer chemopreventive in vitro activities of monomeric xanthone derivatives from the marine algicolous fungus Monodictys putredinis . J Nat Prod 2007; 70: 353-360
  • 19 Lösgen S, Schlörke O, Meindl K, Herbst-Irmer R, Zeeck A. Structure and biosynthesis of chaetocyclinones, new polyketides produced by an endosymbiotic fungus. Eur J Org Chem 2007; 2191-2196
  • 20 Pontius A, Krick A, Mesry R, Kehraus S, Foegen SE, Müller M, Klimo K, Gerhäuser C, König GM. Monodictyochromes A and B, dimeric xanthone derivatives from the marine algicolous fungus Monodictys putredinis . J Nat Prod 2008; 71: 1793-1799
  • 21 Naganuma M, Nishida M, Kuramochi K, Sugawara F, Yoshida H, Mizushina Y. 1-deoxyrubralactone, a novel specific inhibitor of families X and Y of eukaryotic DNA polymerases from a fungal strain derived from sea algae. Bioorg Med Chem 2008; 16: 2939-2944
  • 22 Pontius A, Krick A, Kehraus S, Brun R, König GM. Antiprotozoal activities of heterocyclic-substituted xanthones from the marine-derived fungus Chaetomium sp. J Nat Prod 2008; 71: 1579-1584
  • 23 Greve H, Schupp PJ, Eguereva E, Kehraus S, König GM. Ten-membered lactones from the marine-derived fungus Curvularia sp. J Nat Prod 2008; 71: 1651-1653
  • 24 Greve H, Schupp PJ, Eguereva E, Kehraus S, Kelter G, Maier A, Fiebig HH, König GM. Apralactone A and a New Stereochemical Class of Curvularins from the Marine Fungus Curvularia sp. European J Org Chem 2008; 2008: 5085-5092
  • 25 Elsebai MF, Kehraus S, Lindequist U, Sasse F, Shaaban S, Gütschow M, Josten M, Sahl HG, König GM. Antimicrobial phenalenone derivatives from the marine-derived fungus Coniothyrium cereal . Org Biomol Chem 2011; 9: 802-808
  • 26 Gao SS, Li XM, Du FY, Li CS, Proksch P, Wang BG. Secondary metabolites from a marine-derived endophytic fungus Penicillium chrysogenum QEN-24S. Mar Drugs 2011; 9: 59-70
  • 27 Zhang Y, Li XM, Wang BG. Anthraquinone derivatives produced by marine-derived fungus Aspergillus versicolor EN-7. Biosci Biotechnol Biochem 2012; 76: 1774-1776
  • 28 Hawas UW, EI-Beih AA, EI-Halawany AM. Bioactive anthraquinones from endophytic fungus Aspergillus versicolor isolated from red sea algae. Arch Pharm Res 2012; 35: 1749-1756
  • 29 Tarman K, Palm GJ, Porzel A, Merzweiler K, Arnold N, Wessjohann LA, Unterseher M, Lindequist U. Helicascolide C, a new lactone from an Indonesian marine algicolous strain of Daldinia eschscholzii (Xylariaceae, Ascomycota). Phytochem Lett 2012; 5: 83-86
  • 30 Elsebai MF, Nazir M, Kehraus S, Egereva E, Ioset KN, Marcourt L, Jeannerat D, Gütschow M, Wolfender JL, König GM. Polyketide skeletons from the marine alga-derived fungus Coniothyrium cereale . Eur J Org Chem 2012; 2012: 6197-6203
  • 31 Haroon MH, Premaratne SR, Choudhry MI, Dharmaratne HRW. A new β-glucuronidase inhibiting butyrolactone from the marine endophytic fungus Aspergillus terreus . Nat Prod Res 2013; 27: 1060-1066
  • 32 Sun HF, Li XM, Meng LH, Cui CM, Gao SS, Li CS, Wang BG. Two new secoanthraquinone derivatives from the marine-derived endophytic fungus Aspergillus wentii EN-48. Helv Chim Acta 2013; 96: 458-462
  • 33 Oliveira MN, Santos LS, Guilhon GMSP, Santos AS, Ferreira ICS, Lopes-Junior ML, Arruda MSP, Marinho AMR, da Silva MN, Rodrigues-Filho E, Oliveira MCF. Novel anthraquinone derivatives produced by Pestalotiopsis guepinii, an endophytic of the medicinal plant Virola michelii (Myristicaceae). J Braz Chem Soc 2011; 22: 993-996
  • 34 Abdissa N, Heydenreich M, Midiwo JO, Ndakala A, Majer Z, Neumann B, Stammler HG, Sewald N, Yenesew A. A xanthone and a phenylanthraquinone from the roots of Bulbine frutescens, and the revision of six seco-anthraquinones into xanthones. Phytochem Lett 2014; 9: 67-73
  • 35 Sun RR, Miao FP, Zhang J, Wang G, Yin XL, Ji NY. Three new xanthone derivatives from an algicolous isolate of Aspergillus wentii . Magn Reson Chem 2013; 51: 65-68
  • 36 Du FY, Li XM, Song JY, Li CS, Wang BG. Anthraquinone derivatives and an orsellinic acid ester from the marine alga-derived endophytic fungus Eurotium cristatum EN-220. Helv Chim Acta 2014; 97: 973-978
  • 37 Li X, Li XM, Xu GM, Li CS, Wang BG. Antioxidant metabolites from marine alga-derived fungus Aspergillus wentii EN-48. Phytochem Lett 2014; 7: 120-123
  • 38 Zhang P, Li XM, Wang JN, Li X, Wang BG. New butenolide derivatives from the marine-derived fungus Paecilomyces variotii with DPPH radical scavenging activity. Phytochem Lett 2015; 11: 85-88
  • 39 Osterhage C, König GM, Höller U, Wright AD. Rare sesquiterpenes from the algicolous fungus Drechslera dematioidea . J Nat Prod 2002; 65: 306-313
  • 40 Krohn K, Dai JQ, Flörke U, Aust HJ, Dräger S, Schulz B. Botryane metabolites from the fungus Geniculosporium sp. isolated from the marine red alga Polysiphonia . J Nat Prod 2005; 68: 400-405
  • 41 Almeida C, Eguereva E, Kehraus S, Siering C, König GM. Hydroxylated sclerosporin derivatives from the marine-derived fungus Cadophora malorum . J Nat Prod 2010; 73: 476-478
  • 42 Almeida C, Elsaedi S, Kehraus S, König GM. Novel bisabolane sesquiterpenes from the marine-derived fungus Verticillium tenerum . Nat Prod Commun 2010; 5: 507-510
  • 43 Liu XH, Miao FP, Li XD, Ji NY. A new sesquiterpene from an endophytic Aspergillus versicolor strain. Nat Prod Commun 2012; 7: 819-820
  • 44 Wu B, Wu XD, Sun M, Li MH. Two novel tyrosinase inhibitory sesquiterpenes induced by CuCl2 from a marine-derived fungus Pestalotiopsis sp. Z233. Mar Drugs 2013; 11: 2713-2721
  • 45 Koyama K, Ishino M, Takatori K, Sugita T, Kinoshita K, Takahashi K. Phomactin H, a novel diterpene from an unidentified marine-derived fungus. Tetrahedron Lett 2004; 45: 6947-6948
  • 46 Ishino M, Kiyomichi N, Takatori K, Sugita T, Shiro M, Kinoshita K, Takahashi K, Koyama K. Phomactin I, 13-epi-Phomactin I, and Phomactin J, three novel diterpenes from a marine-derived fungus. Tetrahedron 2010; 66: 2594-2597
  • 47 Ishino M, Kinoshita K, Takahashi K, Sugita T, Shiro M, Hasegawa K, Koyama K. Phomactins K–M, three novel phomactin-type diterpenes from a marine-derived fungus. Tetrahedron 2012; 68: 8572-8576
  • 48 Sun HF, Li XM, Meng L, Cui CM, Gao SS, Li CS, Huang CG, Wang BG. Asperolides A–C, tetranorlabdane diterpenoids from the marine alga-derived endophytic fungus Aspergillus wentii EN-48. J Nat Prod 2012; 75: 148-152
  • 49 Liu XH, Miao FP, Qiao MF, Cichewicz RH, Ji NY. Terretonin, ophiobolin, and drimane terpenes with absolute configurations from an algicolous Aspergillus ustus . RSC Adv 2013; 3: 588-595
  • 50 Cui CM, Li XM, Meng L, Li CS, Huang CG, Wang BG. 7-Nor-ergosterolide, a pentalactone-containing norsteroid and related steroids from the marine-derived endophytic Aspergillus ochraceus EN-31. J Nat Prod 2010; 73: 1780-1784
  • 51 Onodera H, Ichimura M, Baba K, Agatsuma T, Sasho S, Suzuki M, Iwamoto S, Kakita S. PCT Int Appl 2009; WO 2009096445, A1 20090806, CAN 151: 239605, AN 2009: 944135.
  • 52 Qiao MF, Ji NY, Miao FP, Yin XL. Steroids and an oxylipin from an algicolous isolate of Aspergillus flavus . Magn Reson Chem 2011; 49: 366-369
  • 53 Liu XH, Tang XZ, Miao FP, Ji NY. A new pyrrolidine derivative and steroids from an algicolous Gibberella zeae strain. Nat Prod Commun 2011; 6: 1243-1246
  • 54 Gao SS, Li XM, Li CS, Proksch P, Wang BG. Penicisteroids A and B, antifungal and cytotoxic polyoxygenated steroids from the marine alga-derived endophytic fungus Penicillium chrysogenum QEN-24S. Bioorg Med Chem Lett 2011; 21: 2894-2897
  • 55 Elsebai MF, Kehraus S, König GM. Caught between triterpene- and steroid-metabolism: 4α-carboxylic pregnane-derivative from the marine alga-derived fungus Phaeosphaeria spartinae . Steroids 2013; 78: 880-883
  • 56 Huang YF, Li LH, Tian L, Qiao L, Hua HM, Pei YH. Sg17-1-4, a novel isocoumarin from a marine fungus Alternaria tenuis Sg17-1. J Antibiot (Tokyo) 2006; 59: 355-357
  • 57 de Silva ED, Geiermann AS, Mitova MI, Kuegler P, Blunt JW, Cole ALJ, Munro MHG. Isolation of 2-pyridone alkaloids from a New Zealand marine-derived Penicillium species. J Nat Prod 2009; 72: 477-479
  • 58 Zhang Y, Li XM, Feng Y, Wang BG. Phenethyl-α-pyrone derivatives and cyclodipeptides from a marine algous endophytic fungus Aspergillus niger EN-13. Nat Prod Res 2010; 24: 1036-1043
  • 59 Yang GH, Sandjo L, Yun K, Leutou AS, Kim GD, Choi HD, Kang JS, Hong J, Son BW. Flavusides A and B, antibacterial cerebrosides from the marine-derived fungus Aspergillus flavus . Chem Pharm Bull 2011; 59: 1174-1177
  • 60 Abdel-Lateff A. Chaetominedione, a new tyrosine kinase inhibitor isolated from the algicolous marine fungus Chaetomium sp. Tetrahedron Lett 2008; 49: 6398-6400
  • 61 Cui CM, Li XM, Li CS, Sun HF, Gao SS, Wang BG. Benzodiazepine alkaloids from marine-derived endophytic fungus Aspergillus ochraceus . Helv Chim Acta 2009; 92: 1366-1370
  • 62 Zhuravleva OI, Afiyatullov SS, Denisenko VA, Ermakova SP, Slinkina NN, Dmitrenok PS, Kim NY. Secondary metabolites from a marine-derived fungus Aspergillus carneus Blochwitz. Phytochemistry 2012; 80: 123-131
  • 63 Zhuravleva OI, Afiyatullov SS, Yurchenko EA, Denisenko VA, Kirichuk NN, Dmitrenok PS. New metabolites from the algal associated marine-derived fungus Aspergillus carneus . Nat Prod Commun 2013; 8: 1071-1074
  • 64 Zhang P, Mándi A, Li XM, Du FY, Wang JN, Li X, Kurtán T, Wang BG. Varioxepine A, a 3H-oxepine-containing alkaloid with a new oxa-cage from the marine algal-derived endophytic fungus Paecilomyces variotii . Org Lett 2014; 16: 4834-4837
  • 65 Zhang P, Li XM, Wang JN, Wang BG. Oxepine-containing diketopiperazine alkaloids from the algal-derived endophytic fungus Paecilomyces variotii EN-291. Helv Chim Acta 2015; 98: 800-804
  • 66 Tsuda M, Kasai Y, Komatsu K, Sone T, Tanaka M, Mikami Y, Kobayashi J. Citrinadin A, a novel pentacyclic alkaloid from marine-derived fungus Penicillium citrinum . Org Lett 2004; 6: 3087-3089
  • 67 Mugishima T, Tsuda M, Kasai Y, Ishiyama H, Fukushi E, Kawabata J, Watanabe M, Akao K, Kobayashi J. Absolute stereochemistry of citrinadins A and B from marine-derived fungus. J Org Chem 2005; 70: 9430-9435
  • 68 Lin AQ, Du L, Fang YC, Wang FZ, Zhu TJ, Gu QQ, Zhu WM. iso-α-Cyclopiazonic acid, a new natural product isolated from the marine-derived fungus Aspergillus flavus C–F-3. Chem Nat Compd 2009; 45: 677-680
  • 69 Izumikawa M, Hashimoto J, Takagi M, Shin-ya K. Isolation of two new terpeptin analogs-JBIR-81 and JBIR-82-from a seaweed-derived fungus, Aspergillus sp. SpD081030G1f1. J Antibiot 2010; 63: 389-391
  • 70 Qiao MF, Ji NY, Liu XH, Li K, Zhu QM, Xue QZ. Indoloditerpenes from an algicolous isolate of Aspergillus oryzae . Bioorg Med Chem Lett 2010; 20: 5677-5680
  • 71 Cui CM, Li XM, Li CS, Proksch P, Wang BG. Cytoglobosins A–G, cytochalasans from a marine-derived endophytic fungus, Chaetomium globosum QEN-14. J Nat Prod 2010; 73: 729-733
  • 72 Miao FP, Li XD, Liu XH, Cichewicz RH, Ji NY. Secondary metabolites from an algicolous Aspergillus versicolor strain. Mar Drugs 2012; 10: 131-139
  • 73 Du FY, Li XM, Li CS, Wang BG. Cristatumins A–D, new indole alkaloids from the marine-derived endophytic fungus Eurotium cristatum EN-220. Bioorg Med Chem Lett 2012; 22: 4650-4653
  • 74 Ji NY, Liu XH, Miao FP, Qiao MF. Aspeverin, a new alkaloid from an algicolous strain of Aspergillus versicolor . Org Lett 2013; 15: 2327-2329
  • 75 Zhang P, Li XM, Wang JN, Li X, Wang BG. Prenylated indole alkaloids from the marine-derived fungus Paecilomyces variotii . Chin Chem Lett 2015; 26: 313-316
  • 76 Zhang P, Li XM, Li X, Wang BG. New indole-diterpenoids from the algal-associated fungus Aspergillus nidulans . Phytochem Lett 2015; 12: 182-185
  • 77 Cueto M, Jensen PR, Fenical W. N-Methylsansalvamide, a cytotoxic cyclic depsipeptide from a marine fungus of the genus Fusarium . Phytochemistry 2000; 55: 223-226
  • 78 Komatsu K, Shigemori H, Kobayashi J. Dictyonamides A and B, new peptides from marine-derived fungus. J Org Chem 2001; 66: 6189-6192
  • 79 Usami O, Aoki S, Hara T, Numata A. New dioxopiperazine metabolites from a Fusarium species separated from a marine alga. J Antibiot 2002; 55: 655-659
  • 80 Chu M, Mierzwa R, Truumees I, Gentile F, Patel M, Gullo V, Chan TM, Puar MS. Two novel diketopiperazines isolated from the fungus Tolypocladium sp. Tetrahedron Lett 1993; 34: 7537-7540
  • 81 Jiang Z, Barret MO, Boyd KG, Adams DR, Boyd ASF, Burgess JG. JM47, a cyclic tetrapeptide HC-toxin analogue from a marine Fusarium species. Phytochemistry 2002; 60: 33-38
  • 82 Li Y, Li XF, Kim SK, Kang JS, Choi HD, Rho JR, Son BW. Golmaenone, a new diketopiperazine alkaloid from the marine-derived fungus Aspergillus sp . Chem Pharm Bull 2004; 52: 375-376
  • 83 Meyer SW, Mordhorst TF, Lee C, Jensen PR, Fenical W, Köck M. Penilumamide, a novel lumazine peptide isolated from the marine-derived fungus, Penicillium sp. CNL-338. Org Biomol Chem 2010; 8: 2158-2163
  • 84 Gulder TAM, Hong H, Correa J, Egereva E, Wiese J, Imhoff JF, Gross H. Isolation, structure elucidation and total synthesis of lajollamide A from the marine fungus Asteromyces cruciatus . Mar Drugs 2012; 10: 2912-2935
  • 85 An CY, Li XM, Li CS, Gao SS, Shang Z, Wang BG. Triazoles and other N-containing metabolites from the marine-derived endophytic fungus Penicillium chrysogenum EN-118. Helv Chim Acta 2013; 96: 682-687
  • 86 Xu J. Bioactive natural products derived from mangrove-associated microbes. RSC Adv 2015; 5: 841-892
  • 87 Shen JH, Xu XY, Cheng F, Liu H, Luo XM, Shen JK, Chen KX, Zhao WM, Shen X, Jiang HL. Virtual screening on natural products for discovering active compounds and target information. Curr Med Chem 2003; 10: 2237-2242