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Mangrove derived fungal endophytes – a chemical and biological perception

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Abstract

The potential of mangrove-derived endophytic fungi as a promising source of diverse and structurally unprecedented bioactive natural products is unquestionable and continues to attract considerable attention. This review highlights new bioactive mangrove fungal metabolites and known compounds with hitherto unreported biological activities described during the last 10 years. The compounds are categorized according to their reported biological activities, including cytotoxic, anti-infective, in addition to a wide range of miscellaneous activities such as protein kinase, α-glucosidase, acetylcholinesterase and tyrosinase inhibitory activities, as well as antiangiogenic and neovascularisation effects, radical scavenging, DNA-binding affinity, and calcium and potassium channel blocking activity.

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References

  • Akello J, Dubois T, Gold CS, Coyne D, Nakavuma J, Paparu P (2007) Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J Invertebr Pathol 96:34–42

    Article  PubMed  Google Scholar 

  • Anada K, Sridhar KR (2002) Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. Can J Microbiol 48:871–878

    Article  Google Scholar 

  • Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654

    Article  PubMed  CAS  Google Scholar 

  • Bacon CW, White JF (2000) Microbial Endophytes. Marcel Dekker, New York, pp 341–388

    Google Scholar 

  • Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295

    Article  PubMed  CAS  Google Scholar 

  • Bandaranayake WM (1998) Traditional and medicinal uses of mangroves. Mangroves Salt Marshes 2:133–148

    Article  Google Scholar 

  • Bandaranayake WM (2002) Bioactivities, bioactive compounds and chemical constituents of mangrove plants. Wetl Ecol Manag 10:421–452

    Article  CAS  Google Scholar 

  • Bialy L, Waldmann H (2005) Inhibitors of protein tyrosine phosphatases: next-generation drugs? Angew Chem Int Ed 44:3814–3839

    Article  CAS  Google Scholar 

  • Chokpaiboon S, Sommit D, Bunyapaiboonsri T, Matsubara K, Pudhom K (2011) Antiangiogenic effect of chamigrane endoperoxides from a Thai mangrove-derived fungus. J Nat Prod 74:2290–2294

    Article  PubMed  CAS  Google Scholar 

  • Ebrahim W, Kjer J, El Amrani M, Wray V, Lin W, Ebel R, Lai D, Proksch P (2012a) Pullularins E and F, two new peptides from the endophytic fungus Bionectria ochroleuca isolated from the mangrove plant Sonneratia caseolaris. Mar Drugs 10:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Ebrahim W, Aly AH, Mándi A, Totzke F, Kubbutat MHG, Wray V, Lin WH, Dai H, Proksch P, Kurtán T, Debbab A (2012b) Decalactone derivatives from Corynespora cassiicola, an endophytic fungus of the mangrove plant Laguncularia racemosa. Eur J Org Chem: 3476–3484

  • Giordano L, Gonthier P, Varese GC, Miserere L, Nicolotti G (2009) Mycobiota inhabiting sapwood of healthy and declining Scots pine (Pinus sylvestris L.) trees in the Alps. Fungal Divers 38:69–83

    Google Scholar 

  • Gopal B, Chauhan M (2006) Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquat Sci 68:338–354

    Article  Google Scholar 

  • Huang Z, Cai X, Shao C, She Z, Xia X, Chen Y, Yang J, Zhou S, Lin Y (2008) Chemistry and weak antimicrobial activities of phomopsins produced by mangrove endophytic fungus Phomopsis sp. ZSU-H76. Phytochemistry 69:1604–1608

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Guo Z, Yang R, Yin X, Li X, Luo W, She Z, Lin Y (2009) Chemistry and cytotoxic activities of polyketides produced by the mangrove endophytic fungus Phomopsis SP. ZSU-H76. Chem Nat Compd 45:625–628

    Article  CAS  Google Scholar 

  • Huang Z, Yang R, Guo Z, She Z, Lin Y (2010a) A new naphto-α-pyrone from mangrove endophytic fungus ZSU-H26. Chem Nat Compd 46:15–18

    Article  CAS  Google Scholar 

  • Huang Z, Yang R, Yin X, Shec Z, Lin Y (2010b) Structure elucidation and NMR assignments for two xanthone derivatives from a mangrove endophytic fungus (No. ZH19). Magn Reson Chem 48:80–82

    PubMed  CAS  Google Scholar 

  • Huang HB, Feng XJ, Liu L, Chen B, Lu YJ, Ma L, She ZG, Lin YC (2010c) Three dimeric naphtho-γ-pyrones from the mangrove endophytic fungus Aspergillus tubingensis isolated from Pongamia pinnata. Planta Med 76:1888–1891

    Article  PubMed  CAS  Google Scholar 

  • Huang HB, Xiao ZE, Feng XJ, Huang CH, Zhu X, Ju JH, Li MF, Lin YC, Liu L, She ZG (2011a) Cytotoxic naphtho-g-pyrones from the mangrove endophytic fungus Aspergillus tubingensis (GX1-5E). Helv Chim Acta 94:1732–1740

    Article  CAS  Google Scholar 

  • Huang CH, Pan JH, Chen B, Yu M, Huang HB, Zhu X, Lu YJ, She ZG, Lin YC (2011b) Three bianthraquinone derivatives from the mangrove endophytic fungus Alternaria sp. ZJ9-6B from the south China sea. Mar Drugs 9:832–843

    Article  PubMed  CAS  Google Scholar 

  • Huang H, Feng X, Xiao Z, Liu L, Li H, Ma L, Lu Y, Ju J, She Z, Lin Y (2011c) Azaphilones and p-terphenyls from the mangrove endophytic fungus Penicillium chermesinum (ZH4-E2) isolated from the South China Sea. J Nat Prod 74:997–1002

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Huang H, Li H, Sun X, Huang H, Lu Y, Lin Y, Long Y, She Z (2013) Asperterpenoid A, a new sesterterpenoid as an inhibitor of Mycobacterium tuberculosis protein tyrosine phosphatase B from the culture of Aspergillus sp. 16-5c. Org Lett 15:721–723

    Article  PubMed  CAS  Google Scholar 

  • Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  • Jones G, Stanley SJ, Pinruan U (2008) Marine endophyte sources of new chemical natural products: a review. Bot Mar 51:163–170

    Article  Google Scholar 

  • Kjer J, Wray V, Edrada-Ebel RA, Ebel R, Pretsch A, Lin WH, Proksch P (2009) Xanalteric acids I and II and related phenolic compounds from an endophytic Alternaria sp. isolated from the mangrove plant Sonneratia alba. J Nat Prod 72:2053–2057

    Article  PubMed  CAS  Google Scholar 

  • Klaiklay S, Rukachaisirikul V, Phongpaichit S, Pakawatchai C, Saithong S, Buatong J, Preedanon S, Sakayaroj J (2012a) Anthraquinone derivatives from the mangrove-derived fungus Phomopsis sp. PSU-MA214. Phytochem Lett 5:738–742

    Article  CAS  Google Scholar 

  • Klaiklay S, Rukachaisirikul V, Tadpetch K, Sukpondma Y, Phongpaichit S, Buatong J, Sakayaroj J (2012b) Chlorinated chromone and diphenyl ether derivatives from the mangrove-derived fungus Pestalotiopsis sp. PSU-MA69. Tetrahedron 68:2299–2305

    Article  CAS  Google Scholar 

  • Klaiklay S, Rukachaisirikul V, Phongpaichit S, Buatong J, Preedanon S, Sakayaroj J (2012c) Flavodonfuran: a new difuranylmethane derivative from the mangrove endophytic fungus Flavodon flavus PSU-MA201. Nat Prod Res 1–5

  • Klaiklay S, Rukachaisirikul V, Sukpondma Y, Phongpaichit S, Buatong J, Bussaban B (2012d) Metabolites from the mangrove-derived fungus Xylaria cubensis PSU-MA34. Arch Pharm Res 35:1127–1131

    Article  PubMed  CAS  Google Scholar 

  • Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite – what decides? Curr Opin Plant Biol 9:358–363

    Article  PubMed  Google Scholar 

  • Kohlmeyer J, Volkmann-Kohlmeyer B (1993) Two new genera of Ascomycotina from saltmarsh Juncus. Systema Ascomycetum 11:95–106

    Google Scholar 

  • Li MY, Xiao Q, Pan JY, Wu J (2009a) Natural products from semi-mangrove flora: source, chemistry and bioactivities. Nat Prod Rep 26:281–298

    Article  PubMed  Google Scholar 

  • Li DL, Li XM, Wang BG (2009b) Natural anthraquinone derivatives from a marine mangrove plant-derived endophytic fungus Eurotium rubrum: structural elucidation and DPPH radical scavenging activity. J Microbiol Biotechnol 19:675–680

    PubMed  CAS  Google Scholar 

  • Li KK, Lu YJ, Song XH, She ZG, Wuc XW, An LK, Ye CX, Lin YC (2010) The metabolites of mangrove endophytic fungus Zh6-B1 from the South China Sea. Bioorg Med Chem Lett 20:3326–3328

    Article  PubMed  CAS  Google Scholar 

  • Li H, Huang H, Shao C, Huang H, Jiang J, Zhu X, Liu Y, Liu L, Lu Y, Li M, Lin Y, She Z (2011a) Cytotoxic norsesquiterpene peroxides from the endophytic fungus Talaromyces flavus isolated from the mangrove plant Sonneratia apetala. J Nat Prod 74:1230–1235

    Article  PubMed  CAS  Google Scholar 

  • Li C, Zhang J, Shao C, Ding W, She Z, Lin Y (2011b) A new xanthone derivative from the co-culture broth of two marine fungi (strain No. E33 and K38). Chem Nat Compd 47:382–384

    Article  CAS  Google Scholar 

  • Li S, Wei M, Chen G, Lin Y (2012) Two new dihydroisocoumarins from the endophytic fungus Aspergillus sp. collected from the South China Sea. Chem Nat Compd 48:371–373

    Article  CAS  Google Scholar 

  • Lin Z, Zhu T, Fang Y, Gu Q (2008a) 1Hand 13C NMR assignments of two new indolic enamide diastereomers from a mangrove endophytic fungus Aspergillus sp. Magn Reson Chem 46:1212–1216

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Zhu T, Fang Y, Gu Q, Zhu W (2008b) Polyketides from Penicillium sp. JP-1, an endophytic fungus associated with the mangrove plant Aegiceras corniculatum. Phytochemistry 69:1273–1278

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Zhang GJ, Zhu TJ, Liu R, Wei HJ, Gu QQ (2009) Bioactive cytochalasins from Aspergillus flavipes, an endophytic fungus associated with the mangrove plant Acanthus ilicifolius. Helv Chim Acta 92:1538–1544

    Article  CAS  Google Scholar 

  • Liu F, Cai X-L, Yang H, Xia X-K, Guo Z-Y, Yuan J, Li M-F, She Z-G, Lin Y-C (2010) The bioactive metabolites of the mangrove endophytic fungus Talaromyces sp. ZH-154 isolated from Kandelia candel (L.). Planta Med 76:185–189

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Li XM, Meng L, Li CS, Gao SS, Shang Z, Proksch P, Huang CG, Wang BG (2011) Nigerapyrones A-H, α-pyrone derivatives from the marine mangrove-derived endophytic fungus Aspergillus niger MA-132. J Nat Prod 74:1787–1791

    Article  PubMed  CAS  Google Scholar 

  • Lu Z, Zhu H, Fu P, Wang Y, Zhang Z, Lin H, Liu P, Zhuang Y, Hong K, Zhu W (2010) Cytotoxic polyphenols from the marine-derived fungus Penicillium expansum. J Nat Prod 73:911–914

    Article  PubMed  CAS  Google Scholar 

  • Mei WL, Zheng B, Zhao YX, Zhong HM, Chen XL, Zeng YB, Dong WH, Huang JL, Proksch P, Dai HF (2012) Meroterpenes from endophytic fungus A1 of mangrove plant Scyphiphora hydrophyllacea. Mar Drugs 10:1993–2001

    Article  PubMed  CAS  Google Scholar 

  • Pang KL, Vrijmoed LLP, Goh TK, Plaingam N, Jones GEB (2008) Fungal endophytes associated with Kandelia candel (Rhizophoraceae) in Mai Po nature reserve, Hong Kong. Bot Mar 51:171–178

    Article  Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716

    Article  Google Scholar 

  • Redman RS, Sheehan KB, Stout TG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114

    Article  PubMed  CAS  Google Scholar 

  • Rukachaisirikul V, Rodglin A, Sukpondma Y, Phongpaichit S, Buatong J, Sakayaroj J (2012) Phthalide and isocoumarin derivatives produced by an Acremonium sp. isolated from a mangrove Rhizophora apiculata. J Nat Prod 75:853–858

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Sengputa A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174

    Article  Google Scholar 

  • Shang Z, Li XM, Li CS, Wang BG (2012) Diverse secondary metabolites produced by marine-derived fungus Nigrospora sp. MA75 on various culture media. Chem Biodivers 9:1338–1348

    Article  PubMed  CAS  Google Scholar 

  • Shao C, Wang C, Wei M, Gu Y, Xia X, She Z, Lin Y (2008) Structure elucidation of two new xanthone derivatives from the marine fungus Penicillium sp. (ZZF 32#) from the South China Sea. Magn Reson Chem 46:1066–1069

    Article  PubMed  CAS  Google Scholar 

  • Shao SL, Wang CY, Gu YC, Wei MY, Pan JH, Deng DS, She ZG, Lin YC (2010) Penicinoline, a new pyrrolyl 4-quinolinone alkaloid with an unprecedented ring system from an endophytic fungus Penicillium sp. Bioorg Med Chem Lett 20:3284–3286

    Article  PubMed  CAS  Google Scholar 

  • Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanova L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal diversity in aquatic habitats. Biodivers Conserv 16:49–67

    Article  Google Scholar 

  • Song Y, Wang J, Huang H, Ma L, Wang J, Gu Y, Liu L, Lin Y (2012) Four eremophilane sesquiterpenes from the mangrove endophytic fungus Xylaria sp. BL321. Mar Drugs 10:340–348

    Article  PubMed  CAS  Google Scholar 

  • Sridhar KR (2004) Mangrove fungi in India. Curr Sci 86:1586–1587

    Google Scholar 

  • Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Article  PubMed  CAS  Google Scholar 

  • Tan N, Tao Y, Pan J, Wang S, Xu F, She Z, Lin Y, Gareth Jones EB (2008) Isolation, structure elucidation, and mutagenicity of four alternariol derivatives produced by the mangrove endophytic fungus No. 2240. Chem Nat Compd 44:296–300

    Article  CAS  Google Scholar 

  • Tao Y, Zeng X, Mou C, Li J, Cai X, She Z, Zhoub S, Lin Y (2008) 1H and 13C NMR assignments of three nitrogen containing compounds from the mangrove endophytic fungus (ZZF08). Magn Reson Chem 46:501–505

    Article  PubMed  CAS  Google Scholar 

  • Unterseher M, Schnittler M (2010) Species richness analysis and ITS rDNA phylogeny revealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecol 3:366–378

    Article  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  PubMed  CAS  Google Scholar 

  • Wen L, Chen G, She Z, Yan C, Cai J, Mua L (2010) Two new paeciloxocins from a mangrove endophytic fungus Paecilomyces sp. Russ Chem B 59:1656–1659

    Article  CAS  Google Scholar 

  • Wu XY, Liu XH, Lin YC, Luo JH, She ZG, Houjin L, Chan WL, Antus S, Kurtan T, Elsässer B, Krohn K (2005) Xyloketal F: a strong L-calcium channel blocker from the mangrove fungus Xylaria sp. (#2508) from the South China Sea coast. Eur J Org Chem: 4061–4064

  • Xia XK, Huang HR, She ZG, Cai JW, Lan L, Zhang JY, Fuc LW, Vrijmoed LLP, Lin YC (2007) Structural and biological properties of vermistatin and two new vermistatin derivatives isolated from the marine-mangrove endophytic fungus Guignardia sp. No. 4382. Helv Chim Acta 90:1925–1931

    Article  CAS  Google Scholar 

  • Xu M, Gessner G, Groth I, Lange C, Christner A, Bruhn T, Deng Z, Li X, Heinemann SH, Grabley S, Bringmann G, Sattler I, Lin W (2007) Shearinines D-K, new indole triterpenoids from an endophytic Penicillium sp. (strain HKI0459) with blocking activity on large-conductance calcium-activated potassium channels. Tetrahedron 63:435–444

    Article  CAS  Google Scholar 

  • Xu J, Kjer J, Sendker J, Wray V, Guan H, Edrada RA, Lin WH, Wu J, Proksch P (2009a) Chromones from the endophytic fungus Pestalotiopsis sp. Isolated from the Chinese Mangrove plant Rhizophora mucronata. J Nat Prod 72:662–665

    Article  PubMed  CAS  Google Scholar 

  • Xu F, Pang J, Lu B, Wang J, Zhang Y, She Z, Vrijmoed LLP, Gareth Jones EB, Lin Y (2009b) Two metabolites with DNA-binding affinity from the mangrove fungus Xylaria sp. (#2508) from the South China Sea coast. Chin J Chem 27:365–368

    Article  CAS  Google Scholar 

  • Yan HJ, Lia XM, Lia CS, Wang BG (2012) Alkaloid and anthraquinone derivatives produced by the marine-derived endophytic fungus Eurotium rubrum. Helv Chim Acta 95:163–168

    Article  CAS  Google Scholar 

  • Yang J, Xu F, Huang C, Li J, She Z, Pei Z, Lin Y (2010) Metabolites from the mangrove endophytic fungus Phomopsis sp. (#zsu-H76). Eur J Org Chem, 3692–3695

  • Zeng YB, Wang H, Zuo WJ, Zheng B, Yang T, Dai HF, Mei WL (2012) A fatty acid glycoside from a marine-derived fungus isolated from mangrove plant Scyphiphora hydrophyllacea. Mar Drugs 10:598–603

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Sun S, Zhu T, Lin Z, Gu J, Li D, Gu Q (2011) Antiviral isoindolone derivatives from an endophytic fungus Emericella sp. associated with Aegiceras corniculatum. Phytochemistry 72:1436–1442

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Zhu T, Cai S, Gu Q, Li D (2011) Drimane sesquiterpenoids from the mangrove-derived fungus Aspergillus ustus. Chem Pharm Bull 59:762–766

    Article  PubMed  CAS  Google Scholar 

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Financial support to P.P. and A.D. by BMBF is gratefully acknowledged.

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Correspondence to Abdessamad Debbab, Amal H. Aly or Peter Proksch.

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Debbab, A., Aly, A.H. & Proksch, P. Mangrove derived fungal endophytes – a chemical and biological perception. Fungal Diversity 61, 1–27 (2013). https://doi.org/10.1007/s13225-013-0243-8

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