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Humicolopsis cephalosporioides synthesizes DHN-melanin in its chlamydospores

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Abstract

Humicolopsis cephalosporioides is a soil fungus that is associated with Nothofagus forests in South America. The aim of this study was to analyze the effect of environmental factors such as temperature, light, and nutrition on chlamydospore differentiation as well as pigment biosynthesis. Temperature did not affect chlamydospore production; it rather altered pigmentation development that also was affected by light. The composition of culture media as well as light modulated chlamydospore differentiation. Microscope observations, spectroscopic analysis as well as culture assays, using melanin inhibitors, suggest that the main pigment of chlamydospores of H. cephalosporioides is 1,8 dihydroxynaphthalene (DHN)-melanin–type compound. Furthermore, we found that the genome of H. cephalosporioides contains a sequence highly homologous to the pks sequences of other fungi that have been associated with the biosynthesis of 1,8 DHN-melanin. All this together suggests that melanization is among the most important features linked to survival of this fungus in the soils of Nothofagus forests in sub-Antarctica region and that the ITS, 18S, and 28S rDNA sequences did not provide enough information to delineate the phylogenetic relationships of the fungus within the class Leotiomycetes.

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References

  • Akaike H (1973) Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60:255–265

    Article  Google Scholar 

  • Akamatsu HO, Chilvers MI, Stewart JE, Peever TL (2010) Identification and function of a polyketide synthase gene responsible for 1,8-dihydroxynaphthalene-melanin pigment biosynthesis in Ascochyta rabiei. Curr Genet 56:349–360

    Article  CAS  Google Scholar 

  • Atherton NM, Willder JSS (1993) Epr and endor of free radicals formed during the aerobic oxidation of chlorogenic acid and of caffeic acid in strongly alkaline solution. Res Chem Intermed 19:787–795

    Article  CAS  Google Scholar 

  • Bárcena A, Petroselli G, Velasquez SM, Estévez JM, Erra-Balsells R, Balatti PA, Saparrat MCN (2015) Response of the fungus Pseudocercospora griseola f. mesoamericana to tricyclazole. Mycol Prog 14:76. https://doi.org/10.1007/s11557-015-1102-7

    Article  Google Scholar 

  • Bárcena A, Bruno M, Gennaro A, Rozas MF, Mirífico MV, Balatti PA, Saparrat MCN (2018) Melanins from two selected isolates of Pseudocercospora griseola grown in-vitro: chemical features and redox activity. J Photochem Photobiol B 186:207–215

    Article  Google Scholar 

  • Baschien C, Tsui CK, Gulis V, Szewzyk U, Marvanová L (2013) The molecular phylogeny of aquatic hyphomycetes with affinity to the Leotiomycetes. Fungal Biol 117:660–672

    Article  Google Scholar 

  • Beck J, Ripka S, Siegner A, Schiltz E, Schweizer E (1990) The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum. Its gene structure relative to that of other polyketide synthases. Eur J Biochem 192:487–498

    Article  CAS  Google Scholar 

  • Bien S, Kraus C, Damm U (2020) Novel collophorina-like genera and species from Prunus trees and vineyards in Germany. Persoonia 45:46–67

    Article  CAS  Google Scholar 

  • Bingle TJS, Lewis EH, Colin ML (1999) Ketosynthase domain probes identify two subclasses of fungal polyketide synthase genes. Fungal Genet Biol 26:209–223

    Article  CAS  Google Scholar 

  • Blehert DS, Hicks AC, Behr M et al (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227

    Article  CAS  Google Scholar 

  • Bogale M, Orr MJ, O’Hara MJ, Untereiner WA (2010) Systematics of Catenulifera (anamorphic Hyaloscyphaceae) with an assessment of the phylogenetic position of Phialophora hyalina. Fungal Biol 114:396–409

    Article  CAS  Google Scholar 

  • Cano J, Sole M, Pitarch LB, Guarro J (2002) Castanedomyces australiensis, gen. nov., sp. nov., a keratinophilic fungus from Australian Soil. Stud Mycol 47:165–172

    Google Scholar 

  • Chen C, Verkley GJ, Sun G, Groenewald JZ, Crous PW (2016) Redefining common endophytes and plant pathogens in Neofabraea, Pezicula, and related genera. Fungal Biol 120:1291–1322

    Article  Google Scholar 

  • Cooper LA, Gadd GM (1984) Differentiation and melanin production in hyaline and pigmented strains of Microdochium bolleyi. Antonie van Leeuwenhoek 50:53–62

    Article  CAS  Google Scholar 

  • Crous PW, Shivas RG, Wingfield MJ et al (2012) Fungal planet description sheets: 128–153. Persoonia 29:146–201

    Article  CAS  Google Scholar 

  • Crous PW, Quaedvlieg W, Hansen K, Hawksworth DL, Groenewald JZ (2014) Phacidium and Ceuthospora (Phacidiaceae) are congeneric: taxonomic and nomenclatural implications. IMA Fungus 5:173–193

    Article  Google Scholar 

  • Damm U, Fourie PH, Crous PW (2010) Coniochaeta (Lecythophora), Collophora gen. nov. and Phaeomoniella species associated with wood necroses of Prunus trees. Persoonia 24:60–80

    Article  CAS  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  Google Scholar 

  • de Beer ZW, Duong TA, Wingfield MJ (2016) The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 83:165–191

    Article  Google Scholar 

  • De Hoog GS, Gottlich E, Platas G, Genilloud O, Leotta G, van Brummelen J (2005) Evolution, taxonomy and ecology of the genus Thelebolus in Antarctica. Stud Mycol 51:33–76

    Google Scholar 

  • Ehrlich KC, Cotty PJ (2002) Variability in nitrogen regulation of aflatoxin production by Aspergillus flavus strains. Appl Microbiol Biotechnol 60:174–178

    Article  CAS  Google Scholar 

  • Ekanayaka AH, Hyde KD, Gentekaki E, McKenzie EHC, Zhao Q, Bulgakov TS, Camporesi E (2019a) Preliminary classification of Leotiomycetes. Mycosphere 10:310–489

    Article  Google Scholar 

  • Ekanayaka AH, Hyde KD, Jones EBG, Zhao Q, Bulgakov TS (2019b) New and known discolichens from Asia and eastern Europe. Asian J Mycol 2:48–86

    Article  Google Scholar 

  • Elíades LA, Cabello MN, Pancotto V, Moretto A, Rago MM, Saparrat MCN (2015) Preliminary data on growth and enzymatic abilities of soil fungus Humicolopsis cephalosporioides at different incubation temperatures. Revista Iberoamericana de Micología 32:40–45

    Article  Google Scholar 

  • Elíades LA, Cabello MN, Pancotto V, Moretto A, Ferreri N, Saparrat MCN, Barrera MD (2019) Soil mycobiota under managed forests of Nothofagus pumilio in Tierra del Fuego, Argentina. N Z J For Sci 49:7. https://doi.org/10.33494/nzjfs492019x53x

    Article  Google Scholar 

  • Fehrer J, Réblová M, Bambasová V, Vohník M (2019) The root-symbiotic Rhizoscyphus ericae aggregate and Hyaloscypha (Leotiomycetes) are congeneric: phylogenetic and experimental evidence. Stud Mycol 92:195–225

    Article  CAS  Google Scholar 

  • Feng GH, Leonard TJ (1995) Characterization of the polyketide synthase gene (pksL1) required for aflatoxin biosynthesis in Aspergillus parasiticus. J Bacteriol 177:6246–6254

    Article  CAS  Google Scholar 

  • Gernandt DS, Platt JL, Stone JK, Spatafora JW, Holst-Jensen A, Hamelin RC, Kohn LM (2001) Phylogenetics of Helotiales and Rhytismatales based on partial small subunit nuclear ribosomal DNA sequences. Mycologia 93:915–933

    Article  CAS  Google Scholar 

  • Griffiths SA, Cox RJ, Overdijk EJR, Mesarich CH, Saccomanno B, Lazarus CM, de Wit PJGM, Collemare J (2018) Assignment of a dubious gene cluster to melanin biosynthesis in the tomato fungal pathogen Cladosporium fulvum. PLoS One 13:e0209600. https://doi.org/10.1371/journal.pone.0209600

    Article  Google Scholar 

  • Guatimosim E, Schwartsburd PB, Crous PW, Barreto RW (2016) Novel fungi from an ancient niche: lachnoid and chalara-like fungi on ferns. Mycol Prog 15:1239–1267

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  Google Scholar 

  • Gutiérrez E, Vallejo VR, Romaña J, Fons J (1991) The subantarctic Nothofagus forests of Tierra del Fuego: distribution, structure and production. Oecol Aquat 10:351–366

    Google Scholar 

  • Hambleton S, Sigler L (2014) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (≡ Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 78:343–371

    Google Scholar 

  • Han JG, Hosoya T, Sung GH, Shin HD (2014) Phylogenetic reassessment of Hyaloscyphaceae sensu lato (Helotiales, Leotiomycetes) based on multigene analyses. Fungal Biol 118:150–167

    Article  CAS  Google Scholar 

  • Harrington TC, McNew D, Steimel J, Hofstra D, Farrell R (2001) Phylogeny and taxonomy of the Ophiostoma piceae complex and the Dutch elm disease fungi. Mycologia 93:111–136

    Article  CAS  Google Scholar 

  • Hausner G, Reid J, Klassen GR (1993) On the subdivision of Ceratocystis s.l., based on partial ribosomal DNA sequences. Can J Bot 71:52–63

    Article  CAS  Google Scholar 

  • Heeger F, Bourne EC, Baschien C, Yurkov A, Bunk B, Spröer C, Overmann J, Mazzoni CJ, Monaghan MT (2018) Long-read DNA metabarcoding of ribosomal RNA in the analysis of fungi from aquatic environments. Mol Ecol Resour 18:1500–1514

    Article  CAS  Google Scholar 

  • Hendrickson L, Davis CR, Roach C, Nguyen DK, Aldrich T, McAda PC, Reeves CD (1999) Lovastatin biosynthesis in Aspergillus terreus: characterization of blocked mutants, enzyme activities and a multifunctional polyketide synthase gene. Chem Biol 6:429–439

    Article  CAS  Google Scholar 

  • Hosoya T, Zhao Y-J, Degawa Y (2014) Poculum pseudosydowianum, sp. nov. (Rutstroemiaceae, Ascomycota) from Japan and its endophytic occurrence. Phytotaxa 175:216–224

    Article  Google Scholar 

  • Hoy MA, Jeyaprakash A (2005) Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biol Control 32:427–441

    Article  Google Scholar 

  • Hyde KD, Dong Y, Phookamsak R et al (2020) Fungal diversity notes 1151–1276: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers 100:5–277

    Article  Google Scholar 

  • Johnston PR, Park D (2013) The phylogenetic position of Lanzia berggrenii and its sister species. Mycosystema 32:366–385

    CAS  Google Scholar 

  • Johnston PR, Park D, Manning MA (2010) Neobulgaria alba sp. nov. and its Phialophora-like anamorph in native forests and kiwifruit orchards in New Zealand. Mycotaxon 113:385–396

    Article  Google Scholar 

  • Johnston PR, Quijada L, Smith CA et al (2019) A multigene phylogeny toward a new phylogenetic classification of Leotiomycetes. IMA Fungus 10:1. https://doi.org/10.1186/s43008-019-0002-x

    Article  CAS  Google Scholar 

  • Johnston PR, Park D, Smith ME, Mujic AB, May TW (2021) Brahmaculus gen. nov. (Leotiomycetes, Chlorociboriaceae). MycoKeys 80:19–43

    Article  Google Scholar 

  • Kalra R, Conlan XA, Goel M (2020) Fungi as a potential source of pigments: harnessing filamentous fungi. Front Chem 8:369. https://doi.org/10.3389/fchem.2020.00369

    Article  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  Google Scholar 

  • Kayatz P, Thumann G, Luther TT, Jordan JF, Bartz-Schmidt KU, Esser PJ, Schraermeyer U (2001) Oxidation causes melanin fluorescence. Invest Ophthalmol Vis Sci 42:241–246

    CAS  Google Scholar 

  • Klau LJ, Podell S, Creamer KE, Demko AM, Singh HW, Allen EE, Moore BS, Ziemert N, Letzel AC, Jensen PR (2022) The Natural Product Domain Seeker version 2 (NaPDoS2) webtool relates ketosynthase phylogeny to biosynthetic function. J Biol Chem 298:102480. https://doi.org/10.1016/j.jbc.2022.102480

    Article  CAS  Google Scholar 

  • Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci 100:15670–15675

    Article  CAS  Google Scholar 

  • Kumar CG, Mongolla P, Pombala S, Kamle A, Joseph J (2011) Physicochemical characterization and antioxidant activity of melanin from a novel strain of Aspergillus bridgeri ICTF-201. Lett Appl Microbiol 53:350–358

    Article  CAS  Google Scholar 

  • Li W-J, McKenzie EHC, Liu J-K et al (2020) Taxonomy and phylogeny of hyaline-spored coelomycetes. Fungal Divers 100:279–801

    Article  CAS  Google Scholar 

  • Lin X, Heitman J (2005) Chlamydospore formation during hyphal growth in Cryptococcus neoformans. Eukaryotic Cell 4:1746–1754

    Article  CAS  Google Scholar 

  • Linnemannstöns P, Schulte J, del Mar PM, Proctor RH, Avalos J, Tudzynski B (2002) The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet Biol 37:134–148

    Article  Google Scholar 

  • Llorente C, Bárcena A, Vera Bahima J, Saparrat MCN, Arambarri AM, Rozas MF, Mirífico MV, Balatti PA (2012) Cladosporium cladosporioides LPSC 1088 produces the 1,8-dihydroxynaphthalene-melanin-like compound and carries a putative pks gene. Mycopathologia 174:397–408

    Article  CAS  Google Scholar 

  • Lutzoni F, Kauff F, Cox CJ et al (2004) Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. Am J Bot 91:1446–1480

    Article  Google Scholar 

  • Madrid H, Gené J, Cano J, Silvera C, Guarro J (2010) Sporothrix brunneoviolacea and Sporothrix dimorphospora, two new members of the Ophiostoma stenoceras-Sporothrix schenckii complex. Mycologia 102:1193–1203

    Article  CAS  Google Scholar 

  • Marchand S, Cabral D, Wright JE (1976) Tres nuevos géneros de hyphomycetes de Tierra del Fuego. Bol Soc Argent Bot 17:67–72

    Google Scholar 

  • Martin-Sanchez PM, Gorbushina AA, Kunte HJ, Toepel J (2016) A novel qPCR protocol for the specific detection and quantification of the fuel-deteriorating fungus Hormoconis resinae. Biofouling 32:635–644

    Article  CAS  Google Scholar 

  • Mayorga ME, Timberlake WE (1992) The developmentally regulated Aspergillus nidulans wA gene encodes a polypeptide homologous to polyketide and fatty acid synthases. Mol Gen Genet 235:205–212

    Article  CAS  Google Scholar 

  • Medina R, López SMY, Franco MEE, Rollan C, Ronco BL, Saparrat MCN, De Wit PJGM, Balatti PA (2015) A survey on occurrence of Cladosporium fulvum identifies race 0 and race 2 in tomato-growing areas of Argentina. Plant Dis 99:1732–1737

    Article  Google Scholar 

  • Medina R, Lucentini CG, Franco MEE, Petroselli G, Rosso JA, Erra-Balsells R, Balatti PA, Saparrat MCN (2018) Identification of an intermediate for 1,8-dihydroxynaphthalene-melanin synthesis in a race-2 isolate of Fulvia fulva (syn. Cladosporium fulvum). Heliyon 4:e01036. https://doi.org/10.1016/j.heliyon.2018.e01036

    Article  Google Scholar 

  • Mehrabi M, Asgari B, Wijayawardene NN, Hyde KD (2018) Description of Dermea persica (Dermateaceae, Helotiales), a new asexual ascomycete from Iran, and an updated key to Dermea species. Phytotaxa 367:25–37

    Article  Google Scholar 

  • Melo D, Sequeira SO, Lopes JA, Macedo MF (2019) Stains versus colourants produced by fungi colonising paper cultural heritage: a review. J Cult Herit 35:161–182

    Article  Google Scholar 

  • Mestre MC, Fontenla S (2021) Yeast communities associated with ectomycorrhizal fungi in different Nothofagus forests of northwestern Patagonia. Symbiosis 84:179–193

    Article  Google Scholar 

  • Minami A, Ugai T, Ozaki T, Oikawa H (2020) Predicting the chemical space of fungal polyketides by phylogeny-based bioinformatics analysis of polyketide synthase-nonribosomal peptide synthetase and its modification enzymes. Sci Rep 10:13556. https://doi.org/10.1038/s41598-020-70177-w

    Article  CAS  Google Scholar 

  • Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649

    Article  Google Scholar 

  • Moriwaki A, Kihara J, Kobayashi T, Tokunaga T, Arase S, Honda Y (2004) Insertional mutagenesis and characterization of a polyketide synthase gene (PKS1) required for melanin biosynthesis in Bipolaris oryzae. FEMS Microbiol Lett 238:1–8

    CAS  Google Scholar 

  • Narsing Rao MP, Xiao M, Li WJ (2017) Fungal and bacterial pigments: secondary metabolites with wide applications. Front Microbiol 8:1113. https://doi.org/10.3389/fmicb.2017.01113

    Article  Google Scholar 

  • Nasr S, Bien S, Soudi MR et al (2018) Novel Collophorina and Coniochaeta species from Euphorbia polycaulis, an endemic plant in Iran. Mycol Prog 17:755–771

    Article  Google Scholar 

  • Nekoduka S, Tanaka K, Harada Y, Sano T (2010) Phylogenetic affinity of Mycochaetophora gentianae, the causal fungus of brown leaf spot on gentian (Gentiana triflora), to Pseudocercosporella-like hyphomycetes in Helotiales. Mycoscience 51:123–133

    Article  Google Scholar 

  • Nicholson TP, Rudd BA, Dawson M et al (2001) Design and utility of oligonucleotide gene probes for fungal polyketide synthases. Chem Biol 8:157–178

    Article  CAS  Google Scholar 

  • Nikoh N, Fukatsu T (2000) Interkingdom host jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. Mol Biol Evol 17:629–638

    Article  CAS  Google Scholar 

  • Nitiu DS, Mallo AC, Saparrat MCN (2020) Fungal melanins that deteriorate paper cultural heritage: an overview. Mycologia 112:859–870

    Article  CAS  Google Scholar 

  • Ohm RA, Feau N, Henrissat B et al (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8:e1003037. https://doi.org/10.1371/journal.ppat.1003037

    Article  CAS  Google Scholar 

  • Okada G, Jacobs K, Kirisits T, Louis-Seize GW, Seifert KA, Sugita T, Takematsu A, Wingfield MJ (2000) Epitypification of Graphium penicillioides Corda, with comments on the phylogeny and taxonomy of Graphium-like synnematous fungi. Stud Mycol 45:169–186

    Google Scholar 

  • Pal AK, Gajjar DU, Vasavada AR (2014) DOPA and DHN pathway orchestrate melanin synthesis in Aspergillus species. Med Mycol 52:10–18

    CAS  Google Scholar 

  • Palige K, Linde J, Martin R et al (2013) Global transcriptome sequencing identifies chlamydospore specific markers in Candida albicans and Candida dubliniensis. PLoS ONE 8:e61940. https://doi.org/10.1371/journal.pone.0061940

    Article  CAS  Google Scholar 

  • Pärtel K, Baral HO, Tamm H, Põldmaa K (2017) Evidence for the polyphyly of Encoelia and Encoelioideae with reconsideration of respective families in Leotiomycetes. Fungal Divers 82:183–219

    Article  Google Scholar 

  • Puel O, Tadrist S, Delaforge M, Oswald IP, Lebrihi A (2007) The inability of Byssochlamys fulva to produce patulin is related to absence of 6-methylsalicylic acid synthase and isoepoxydon dehydrogenase genes. Int J Food Microbiol 115:131–139

    Article  CAS  Google Scholar 

  • Réblová M, Gams W, Štěpánek V (2011) The new hyphomycete genera Brachyalara and Infundichalara, the similar Exochalara and species of ‘Phialophora sect. Catenulatae’ (Leotiomycetes). Fungal Divers 46:67–86

    Article  Google Scholar 

  • Rehner SA, Samuels GJ (1995) Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs. Can J Bot 73:816–823

    Article  Google Scholar 

  • Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073

    Article  Google Scholar 

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Rossman AY, Cathie Aime M, Farr DF et al (2004) The coelomycetous genera Chaetomella and Pilidium represent a newly discovered lineage of inoperculate discomycetes. Mycol Prog 3:275–290

    Article  Google Scholar 

  • Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Saparrat MCN, Balatti PA, Martínez MJ, Jurado M (2010) Differential regulation of laccase gene expression in Coriolopsis rigida LPSC No. 232. Fungal Biol 114:999–1006

  • Sauer M, Ping L, Sangari R et al (2002) Estimating polyketide metabolic potential among non-sporulating fungal endophytes of Vaccinium macrocarpon. Mycol Res 106:460–470

    Article  CAS  Google Scholar 

  • Schmitt I, Martín MP, Kautz S, Lumbsch HT (2005) Diversity of non-reducing polyketide synthase genes in the Pertusariales (lichenized Ascomycota): a phylogenetic perspective. Phytochemistry 66:1241–1253

    Article  CAS  Google Scholar 

  • Schoch CL, Sung GH, López-Giráldez F et al (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239

    Article  CAS  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241–6246

    Article  CAS  Google Scholar 

  • Schoch CL, Robbertse B, Robert V et al (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. Database 2014:bau061. https://doi.org/10.1093/database/bau061

    Article  Google Scholar 

  • Scorsetti AC, Elíades LA, Stenglein SA, Cabello MN, Pelizza SA, Saparrat MCN (2012) Pathogenic and enzyme activities of the entomopathogenic fungus Tolypocladium cylindrosporum (Ascomycota: Hypocreales) from Tierra del Fuego, Argentina. Rev Biol Trop 60:833–841

    Article  Google Scholar 

  • Shoemaker RA, Hambleton S, Lacroix M, Tesolin M, Coulombe J (2002) Fungi Canadenses No. 344: Rhexocercosporidium carotae. Can J Plant Pathol 24:359–362

    Article  Google Scholar 

  • So K-K, Kim J-M, Nguyen N-L et al (2012) Rapid screening of an ordered fosmid library to clone multiple polyketide synthase genes of the phytopathogenic fungus Cladosporium phlei. J Microbiol Methods 91:412–419

    Article  CAS  Google Scholar 

  • Sogonov MV, Schroers HJ, Gams W, Dijksterhuis J, Summerbell RC (2005) The hyphomycete Teberdinia hygrophila gen. nov., sp. nov. and related anamorphs of Pseudeurotium species. Mycologia 97:695–709

    Article  CAS  Google Scholar 

  • Somrithipol S, Gareth Jones EB, Bahkali AH et al (2017) Lauriomyces, a new lineage in the Leotiomycetes with three new species. Cryptog Mycolog 38:259–273

    Article  Google Scholar 

  • Spatafora JW, Sung GH, Johnson D et al (2006) A five-gene phylogeny of Pezizomycotina. Mycologia 98:1018–1028

    Article  CAS  Google Scholar 

  • Sri-indrasutdhi V, Tsui CKM, Chuaseeharonnachai C et al (2015) Helicocentralis hyalina gen. et sp. nov., an aero-aquatic helicosporous fungus (Leotiomycetes, Ascomycota) in Thailand. Mycol Prog 14:81. https://doi.org/10.1007/s11557-015-1103-6

    Article  Google Scholar 

  • Sugiyama M, Ohara A, Mikawa T (1999) Molecular phylogeny of onygenalean fungi based on small subunit ribosomal DNA (SSU rDNA) sequences. Mycoscience 40:251–258

    Article  CAS  Google Scholar 

  • Suh S-O, Blackwell M (1999) Molecular phylogeny of the cleistothecial fungi placed in Cephalothecaceae and Pseudeurotiaceae. Mycologia 91:836–848

    Article  CAS  Google Scholar 

  • Sung G-H, Spatafora JW, Zare R, Hodge KT, Gams W (2001) A revision of Verticillium Sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72:311–328

    Article  Google Scholar 

  • Takano Y, Kubo Y, Shimizu K et al (1995) Structural analysis of PKS1, a polyketide synthase gene involved in melanin biosynthesis in Colletotrichum lagenarium. Mol Gen Genet 249:162–167

    Article  CAS  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Toledo AV, Franco MEE, Lopez SMY, Troncozo MI, Saparrat MCN, Balatti PA (2017) Melanins in fungi: types, localization and putative biological roles. Physiol Mol Plant Pathol 99:2–6

    Article  CAS  Google Scholar 

  • Tominaga M, Lee YH, Hayashi R, Suzuki Y, Yamada O, Sakamoto K, Gotoh K, Akita O (2006) Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains. Appl Environ Microbiol 72:484–490

    Article  CAS  Google Scholar 

  • Tsai HF, Chang YC, Washburn RG, Wheeler MH, Kwon-Chung KJ (1998) The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J Bacteriol 180:3031–3038

    Article  CAS  Google Scholar 

  • Untereiner WA, Yue Q, Chen L, Li Y, Bills GF, Štěpánek V, Réblová M (2019) Phialophora section Catenulatae disassembled: New genera, species, and combinations and a new family encompassing taxa with cleistothecial ascomata and phialidic asexual states. Mycologia 111:998–1027

    Article  CAS  Google Scholar 

  • Varga J, Rigó K, Kocsubé S, Farkas B (2003) Diversity of polyketide synthase gene sequences in Aspergillus species. Res Microbiol 154:593–600

    Article  CAS  Google Scholar 

  • Vu D, Groenewald M, de Vries M et al (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154

    Article  CAS  Google Scholar 

  • Wang Z, Binder M, Hibbett DS (2005) Life history and systematics of the aquatic discomycete Mitrula (Helotiales, Ascomycota) based on cultural, morphological, and molecular studies. Am J Bot 92:1565–1574

    Article  Google Scholar 

  • White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA, pp 315–322

    Google Scholar 

  • Ye X, Feng B, Szaniszlo PJ (1999) A color-selectable and site-specific integrative transformation system for gene expression studies in the dematiaceous fungus Wangiella (Exophiala) dermatitidis. Curr Genet 36:241–247

    Article  CAS  Google Scholar 

  • Zdybel M, Pilawa B, Buszman E, Witoszyńska T (2013) EPR studies of Cladosporium cladosporioides complexes with amphotericin B. Nukleonika 58:401–405

    CAS  Google Scholar 

  • Zhang R, Xia H, Xu Q et al (2013) Recombinational cloning of the antibiotic biosynthetic gene clusters in linear plasmid SCP1 of Streptomyces coelicolor A3(2). FEMS Microbiol Lett 345:39–48

    Article  CAS  Google Scholar 

  • Zheng H, Zhang ZN, Wen Z, Castañeda-Ruiz RF, Yu ZF (2019) Blastosporium persicolor gen. et sp. nov., a new helotialean fungus. MycoKeys 51:55–64

    Article  Google Scholar 

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Acknowledgements

We thank Ana M. Gennaro from the INTEC (CONICET-UNL, Santa Fe, Argentina) for performing the ESR analysis. AB, RM, LAE, and MCNS are members of the Carrera del Investigador Científico CONICET, Argentina. MNC and PAB are researchers of the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CICPBA), Argentina.

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Funding

This research was partially financed by the National Agency for Scientific and Technological Promotion (ANPCyT) of the Ministry of Science, Technology and Productive Innovation through the PICT 2018-3144 project (RM), PICT 2019-00207 project (MCNS), PICT 2020-02736 project (PAB), CONICET (PUE INFIVE and PIP 11220200100527CO) and UNLP, Argentina, and by the Secretary of Science and Technique of the National University of La Plata, through the R&D Projects A344 (MCNS).

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AB designed and performed experiments on biomass production, extraction, and characterization of pigments and melanin synthesis inhibition. RM analyzed data, provided funding acquisition, and co-wrote the paper. MEEF made DNA extraction, polymerase chain reactions, sequence alignments, and phylogenetic analyses. LAE helped performing different tasks in laboratory. MNC provided fungal strains and participated actively in species identification using morphological features. CPT contributed on the revision and conceptualization of this manuscript. PAB was involved in the analysis and discussion of the data obtained, provided funding acquisition and assisted with the writing of the paper. MCNS supervised the research, provided funding acquisition and co-wrote the paper.

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Correspondence to Mario Carlos Nazareno Saparrat.

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The authors declare no competing interests.

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Alejandra Bárcena and Rocío Medina are Co-first author.

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Bárcena, A., Medina, R., Franco, M.E.E. et al. Humicolopsis cephalosporioides synthesizes DHN-melanin in its chlamydospores. Mycol Progress 22, 4 (2023). https://doi.org/10.1007/s11557-022-01853-6

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