Skip to main content
Log in

Effects of Tricyclazole on Cadmium Tolerance and Accumulation Characteristics of a Dark Septate Endophyte (DSE), Exophiala pisciphila

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Exophiala pisciphila is a cadmium-tolerant fungus, and produces 1,8-dihydroxynaphthalene melanin which can be inhibited by tricyclazole. Tricyclazole at higher levels (20 and 40 µg mL−1) reduced the growth and sporulation of E. pisciphila, but toxicity was not observed at a low concentration (2.5 µg mL−1). Under cadmium (Cd) stress (50, 100 and 200 mg L−1), 2.5 µg mL−1 of tricyclazole reduced fungal growth and sporulation. These reduces indicated a decrease on Cd tolerance of E. pisciphila. For both the 0 and 2.5 µg mL−1 tricyclazole treatments, Cd was associated mostly with cell walls and was extracted by 2 % acetic acid and 1 M NaCl. The FTIR spectra of the E. pisciphila mycelia were similar for both 0 and 2.5 µg mL−1 tricyclazole treatments, which showed hydroxyl, amine, carboxyl and phosphate groups. Thus inhibition of melanin synthesis by tricyclazole did not change Cd accumulation characteristics in E. pisciphila. Results suggested that melanin played a protective role for E. pisciphila against Cd stress, but inhibition of melanin synthesis did not have a remarkable impact on Cd accumulation in E. pisciphila.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ban Y, Tang M, Chen H, Xu Z, Zhang H, Yang Y (2012) The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One 7(10):e47968

    Article  CAS  Google Scholar 

  • Bell AA, Wheeler MH (1986) Biosynthesis and functions of fungal melanins. Annu Rev Phytopathol 24(1):411–451

    Article  CAS  Google Scholar 

  • Buszman E, Pilawa B, Zdybel M, Wilczynski S, Gondzik A, Witoszynska T, Wilczok T (2006) EPR examination of Zn2+ and Cu2+ binding by pigmented soil fungi Cladosporium cladosporioides. Sci Total Environ 363(1):195–205

    Article  CAS  Google Scholar 

  • Caesar-Tonthat T, Van Ommen KF, Geesey GG, Henson JM (1995) Melanin production by a filamentous soil fungus in response to copper and localization of copper sulfide by sulfide–silver staining. Appl Environ Microb 61(5):1968–1975

    CAS  Google Scholar 

  • Cunha MM, Franzen AJ, Alviano DS, Zanardi E, Alviano CS, De Souza W, Rozental S (2005) Inhibition of melanin synthesis pathway by tricyclazole increases susceptibility of Fonsecaea pedrosoi against mouse macrophages. Microsc Res Tech 68(6):377–384

    Article  CAS  Google Scholar 

  • Deram A, Languereau-Leman F, Howsam M, Petit D, Van Haluwyn C (2008) Seasonal patterns of cadmium accumulation in Arrhenatherum elatius (Poaceae): influence of mycorrhizal and endophytic fungal colonisation. Soil Biol Biochem 40:845–848

    Article  CAS  Google Scholar 

  • Eisenman HC, Nosanchuk JD, Webber JBW, Emerson RJ, Camesano TA, Casadevall A (2005) Microstructure of cell wall-associated melanin in the human pathogenic fungus Cryptococcus neoformans. Biochemistry 44(10):3683–3693

    Article  CAS  Google Scholar 

  • Elliott ML (1995) Effect of melanin biosynthesis inhibiting compounds on Gaeumannomyces species. Mycologia 87:370–374

    Article  CAS  Google Scholar 

  • Fernando T, Bean G (1986) Effects of tricyclazole on growth, release of aflatoxin, and sterol and fatty acid content, by Aspergillus isolates. Trans Br Mycol Soc 87(3):445–449

    Article  CAS  Google Scholar 

  • Fomina M, Gadd GM (2003) Metal sorption by biomass of melanin-producing fungi grown in clay-containing medium. J Chem Technol Biotechnol 78(1):23–34

    Article  CAS  Google Scholar 

  • Franzen AJ, Cunha MM, Batista EJ, Seabra SH, De Souza W, Rozental S (2006) Effects of tricyclazole (5-methyl-1,2,4-triazol[3,4]benzothiazole), a specific DHN-melanin inhibitor, on the morphology of Fonsecaea pedrosoi conidia and sclerotic cells. Microsc Res Tech 69(9):729–737

    Article  CAS  Google Scholar 

  • Gaur N, Flora G, Yadav M, Tiwari A (2014) A review with recent advancements on bioremediation-based abolition of heavy metals. Environ Sci Process Impacts 16(2):180–193

    Article  CAS  Google Scholar 

  • Geis PA, Wheeler MH, Szaniszlo PJ (1984) Pentaketide metabolites of melanin synthesis in the dematiaceous fungus Wangiella dermatitidis. Arch Microbiol 137(4):324–328

    Article  CAS  Google Scholar 

  • Gessler NN, Egorova AS, Belozerskaya TA (2014) Melanin pigments of fungi under extreme environmental conditions. Appl Biochem Microbiol 50(2):105–113

    Article  CAS  Google Scholar 

  • Guo X, Jia H, Cao Z, Hao Z, Dong J (2012) Effects of tricyclazole on the pathogenicity of Setosphaeria turcica. Acta Phytophylacica Sin 39:364–368

    CAS  Google Scholar 

  • Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47(6):453–467

    Article  CAS  Google Scholar 

  • Henson JM, Butler MJ, Day AW (1999) The dark side of the mycelium: melanins of phytopathogenic fungi. Annu Rev Phytopathol 37(1):447–471

    Article  CAS  Google Scholar 

  • Jeong SA, Thapa SP, Park HR, Choi NG, Hur JH (2012) Distribution and persistence of tricyaclazole in agricultural field soils. Bull Environ Contam Toxicol 89(6):1181–1185

    Article  CAS  Google Scholar 

  • Jumpponen ARI (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11(4):207–211

    Article  Google Scholar 

  • Jumpponen ARI, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140(2):295–310

    Article  Google Scholar 

  • Kogej T, Wheeler MH, Rizner TL, Gunde-Cimerman N (2004) Evidence for 1,8-dihydroxynaphthalene melanin in three halophilic black yeasts grown under saline and non-saline conditions. FEMS Microbiol Lett 232(2):203–209

    Article  CAS  Google Scholar 

  • Kogej T, Gorbushina AA, Gunde-Cimerman N (2006) Hypersaline conditions induce changes in cell-wall melanization and colony structure in a halophilic and a xerophilic black yeast species of the genus Trimmatostroma. Mycol Res 110(6):713–724

    Article  Google Scholar 

  • Kunova A, Pizzatti C, Cortesi P (2013) Impact of tricyclazole and azoxystrobin on growth, sporulation and secondary infection of the rice blast fungus, Magnaporthe oryzae. Pest Manag Sci 69(2):278–284

    Article  CAS  Google Scholar 

  • Latge JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66(2):279–290

    Article  CAS  Google Scholar 

  • Lee J, Jung H, Kim S (2003) 1,8-dihydroxynaphthalene (DHN)-melanin biosynthesis inhibitors increase erythritol production in Torula corallina, and DHN-melanin inhibits erythrose reductase. Appl Environ Microbiol 69(6):3427–3434

    Article  CAS  Google Scholar 

  • Li H, Li D, He C, Zhou Z, Mei T, Xu H (2012) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland in China. Fungal Ecol 5(3):309–315

    Article  Google Scholar 

  • Loayza-Muro RLA, Marticorena-Ruiz JK, Palomino EJ, Merritt C, De Baat ML, Van Gemert M, Verweij RA, Kraak MH, Admiraal W (2012) Persistence of chironomids in metal polluted andean high altitude streams: does melanin play a role? Environ Sci Technol 47(1):601–607

    Article  Google Scholar 

  • McLean J, Purvis OW, Williamson BJ, Bailey EH (1998) Role for lichen melanins in uranium remediation. Nature 391(6668):649–650

    Article  CAS  Google Scholar 

  • Padovani L, Capri E, Padovani C, Puglisi E, Trevisan M (2006) Monitoring tricyclazole residues in rice paddy watersheds. Chemosphere 62(2):303–314

    Article  CAS  Google Scholar 

  • Phong TK, Nhung DTT, Yamazaki K, Takagi K, Watanabe H (2009) Behavior of sprayed tricyclazole in rice paddy lysimeters. Chemosphere 74(8):1085–1089

    Article  CAS  Google Scholar 

  • Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara J (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9(1):177

    Article  Google Scholar 

  • Romero-Martinez R, Wheeler M, Guerrero-Plata A, Rico G, Torres-Guerrero H (2000) Biosynthesis and functions of melanin in Sporothrix schenckii. Infect Immun 68(6):3696–3703

    Article  CAS  Google Scholar 

  • Ruotsalainen AL, Markkola A, Kozlov MV (2007) Root fungal colonisation in Deschampsia flexuosa: effects of pollution and neighbouring trees. Environ Pollut 147(3):723–728

    Article  CAS  Google Scholar 

  • Tokousbalides MC, Sisler HD (1978) Effect of tricyclazole on growth and secondary metabolism in Pyricularia oryzae. Pestic Biochem Phys 8(1):26–32

    Article  CAS  Google Scholar 

  • Tsochatzis ED, Tzimou-Tsitouridou R, Menkissoglu-Spiroudi U, Karpouzas DG, Katsantonis D (2013) Laboratory and field dissipation of penoxsulam, tricyclazole and profoxydim in rice paddy systems. Chemosphere 91(7):1049–1057

    Article  CAS  Google Scholar 

  • van der Wal A, Bloem J, Mulder C, de Boer W (2009) Relative abundance and activity of melanized hyphae in different soil ecosystems. Soil Biol Biochem 41(2):417–419

    Article  Google Scholar 

  • Wang X, Liu Y, Zeng G, Chai L, Song X, Min Z, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Gaud. Environ Exp Bot 62(3):389–395

    Article  CAS  Google Scholar 

  • Weigel HJ, Jager HJ (1980) Subcellular distribution and chemical form of cadmium in bean plants. Plant Physiol 65(3):480–482

    Article  CAS  Google Scholar 

  • Yang J, He J, Zhang G (1995) Tolerance mechanism of crops to cadmium pollution. J Appl Ecol 6:87–91

    Google Scholar 

  • Youngchim S, Morris-Jones R, Hay RJ, Hamilton AJ (2004) Production of melanin by Aspergillus fumigatus. J Med Microbiol 53(3):175–181

    Article  CAS  Google Scholar 

  • Zhan F, He Y, Zu Y, Li T, Zhao Z (2011) Characterization of melanin isolated from a dark septate endophyte (DSE), Exophiala pisciphila. World J Microbiol Biotechnol 27(10):2483–2489

    Article  CAS  Google Scholar 

  • Zhan F, He Y, Li T, Yang YY, Toor GS, Zhao Z (2015) Tolerance and antioxidant response of a dark septate endophyte (DSE), Exophiala pisciphila, to cadmium stress. Bull Environ Contam Toxicol 94(1):96–102

    Article  CAS  Google Scholar 

  • Zhang Y, Zhang Y, Liu M, Shi X, Zhao Z (2008) Dark septate endophyte (DSE) fungi isolated from metal polluted soils: their taxonomic position, tolerance, and accumulation of heavy metals in vitro. J Microbiol 46(6):624–632

    Article  Google Scholar 

  • Zhang C, Huang X, Wang J, Zhou M (2009) Resistance development in rice blast disease caused by Magnaporthe grisea to tricyclazole. Pestic Biochem Phys 94(1):43–47

    Article  CAS  Google Scholar 

  • Zhang Y, Li T, Zhao Z (2013) Colonization characteristics and composition of dark septate endophytes (DSE) in a lead and zinc slag heap in Southwest China. Soil Sediment Contam 22(5):532–545

    Article  CAS  Google Scholar 

  • Zhong J, Frases S, Wang H, Casadevall A, Stark RE (2008) Following fungal melanin biosynthesis with solid-state NMR: biopolymer molecular structures and possible connections to cell–wall polysaccharides. Biochemistry 47(16):4701–4710

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Nos. 41101486, 41461093, 31460114 and U1202236), and Key Research Project of Education Bureau of Yunnan Province, China (No. 09Z0037).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiwei Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhan, F., He, Y., Yang, Y. et al. Effects of Tricyclazole on Cadmium Tolerance and Accumulation Characteristics of a Dark Septate Endophyte (DSE), Exophiala pisciphila . Bull Environ Contam Toxicol 96, 235–241 (2016). https://doi.org/10.1007/s00128-015-1676-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-015-1676-4

Keywords

Navigation