Segregation of the genus Parahypoxylon (Hypoxylaceae, Xylariales) from Hypoxylon by a polyphasic taxonomic approach

During a mycological survey of the Democratic Republic of the Congo, a fungal specimen that morphologically resembled the American species Hypoxylon papillatum was encountered. A polyphasic approach including morphological and chemotaxonomic together with a multigene phylogenetic study (ITS, LSU, tub2, and rpb2) of Hypoxylon spp. and representatives of related genera revealed that this strain represents a new species of the Hypoxylaceae. However, the multi-locus phylogenetic inference indicated that the new fungus clustered with H. papillatum in a separate clade from the other species of Hypoxylon. Studies by ultrahigh performance liquid chromatography coupled to diode array detection and ion mobility tandem mass spectrometry (UHPLC-DAD-IM-MS/MS) were carried out on the stromatal extracts. In particular, the MS/MS spectra of the major stromatal metabolites of these species indicated the production of hitherto unreported azaphilone pigments with a similar core scaffold to the cohaerin-type metabolites, which are exclusively found in the Hypoxylaceae. Based on these results, the new genus Parahypoxylon is introduced herein. Aside from P. papillatum, the genus also includes P. ruwenzoriensesp. nov., which clustered together with the type species within a basal clade of the Hypoxylaceae together with its sister genus Durotheca.

[1]  M. Stadler,et al.  Multiformin-Type Azaphilones Prevent SARS-CoV-2 Binding to ACE2 Receptor , 2022, Cells.

[2]  M. Stadler,et al.  New polyketides from the liquid culture of Diaporthebreyniae sp. nov. (Diaporthales, Diaporthaceae) , 2022, MycoKeys.

[3]  Y. Li,et al.  Multi-Gene Phylogeny and Taxonomy of Hypoxylon (Hypoxylaceae, Ascomycota) from China , 2022, Diversity.

[4]  Roger G. Linington,et al.  An Isotopic Labeling Approach Linking Natural Products with Biosynthetic Gene Clusters , 2021, Nature Chemical Biology.

[5]  D. Wishart,et al.  CFM-ID 4.0: More Accurate ESI-MS/MS Spectral Prediction and Compound Identification. , 2021, Analytical chemistry.

[6]  R. Cox,et al.  Secondary metabolite biosynthetic diversity in the fungal family Hypoxylaceae and Xylaria hypoxylon , 2021, Studies in mycology.

[7]  Sudhir Kumar,et al.  MEGA11: Molecular Evolutionary Genetics Analysis Version 11 , 2021, Molecular biology and evolution.

[8]  S. Rogers,et al.  Spec2Vec: Improved mass spectral similarity scoring through learning of structural relationships. , 2021, PLoS computational biology.

[9]  T. Stradal,et al.  Resolution of the Hypoxylon fuscum Complex (Hypoxylaceae, Xylariales) and Discovery and Biological Characterization of Two of Its Prominent Secondary Metabolites , 2021, Journal of fungi.

[10]  A. Alves,et al.  Diversity of fungi associated with macroalgae from an estuarine environment and description of Cladosporium rubrum sp. nov. and Hypoxylon aveirense sp. nov. , 2021, International journal of systematic and evolutionary microbiology.

[11]  Abdoulaye Baniré Diallo,et al.  TOUCAN: a framework for fungal biosynthetic gene cluster discovery , 2020, NAR genomics and bioinformatics.

[12]  M. Stadler,et al.  Recent progress in biodiversity research on the Xylariales and their secondary metabolism , 2020, The Journal of antibiotics.

[13]  M. Stadler,et al.  Phylogenetic Assignment of the Fungicolous Hypoxylon invadens (Ascomycota, Xylariales) and Investigation of its Secondary Metabolites , 2020, Microorganisms.

[14]  J. Kalinowski,et al.  High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa , 2020, Fungal Diversity.

[15]  M. Stadler,et al.  Discovery of a new species of the Hypoxylon rubiginosum complex from Iran and antagonistic activities of Hypoxylon spp. against the Ash Dieback pathogen, Hymenoscyphus fraxineus, in dual culture , 2020, MycoKeys.

[16]  J. Kalinowski,et al.  Intragenomic polymorphisms in the ITS region of high-quality genomes of the Hypoxylaceae (Xylariales, Ascomycota) , 2020, Mycological Progress.

[17]  M. Stadler,et al.  Natonodosa speciosa gen. et sp. nov. and rediscovery of Poroisariopsis inornata: neotropical anamorphic fungi in Xylariales , 2020, Mycological Progress.

[18]  Simon Rogers,et al.  Feature-Based Molecular Networking in the GNPS Analysis Environment , 2019, Nature Methods.

[19]  K. Hyde.  Refined families of Sordariomycetes , 2020 .

[20]  M. Cedeño-Sanchez.  Three new species of Hypoxylon and new records of Xylariales from Panama , 2020, Mycosphere.

[21]  Olga Chernomor,et al.  IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era , 2019, bioRxiv.

[22]  C. Lambert,et al.  Observations on Texas hypoxylons, including two new Hypoxylon species and widespread environmental isolates of the H. croceum complex identified by a polyphasic approach , 2019, Mycologia.

[23]  Joe Wandy,et al.  MolNetEnhancer: Enhanced Molecular Networks by Integrating Metabolome Mining and Annotation Tools , 2019, bioRxiv.

[24]  G. Cardinali,et al.  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 , 2018, Studies in mycology.

[25]  Kazutaka Katoh,et al.  MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization , 2017, Briefings Bioinform..

[26]  K. Hyde,et al.  Contributions to species of Xylariales in China-1. Durotheca species , 2019, Mycological Progress.

[27]  Jin Zhang,et al.  PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies , 2018, bioRxiv.

[28]  M. Stadler,et al.  Hypomontagnella (Hypoxylaceae): a new genus segregated from Hypoxylon by a polyphasic taxonomic approach , 2018, Mycological Progress.

[29]  M. Rohde,et al.  Identification of fungal fossils and novel azaphilone pigments in ancient carbonised specimens of Hypoxylon fragiforme from forest soils of Châtillon-sur-Seine (Burgundy) , 2018, Fungal Diversity.

[30]  M. Stadler,et al.  Minutellins A - D, azaphilones from the stromata of Annulohypoxylon minutellum (Xylariaceae). , 2017, Phytochemistry.

[31]  Thomas K. F. Wong,et al.  ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates , 2017, Nature Methods.

[32]  Robert Lanfear,et al.  PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. , 2016, Molecular biology and evolution.

[33]  K. Hyde,et al.  Towards a natural classification and backbone tree for Graphostromataceae, Hypoxylaceae, Lopadostomataceae and Xylariaceae , 2017, Fungal Diversity.

[34]  M. Stadler,et al.  Resurrection and emendation of the Hypoxylaceae, recognised from a multigene phylogeny of the Xylariales , 2017, Mycological Progress.

[35]  M. Rohde,et al.  Phylogenetic and chemotaxonomic resolution of the genus Annulohypoxylon (Xylariaceae) including four new species , 2017, Fungal Diversity.

[36]  Kristian Fog Nielsen,et al.  Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking , 2016, Nature Biotechnology.

[37]  G. WendelinI.Friebes.  Studies on Hypoxylon ferrugineum (Xylariaceae), a rarely reported species collected in the urban area of Graz (Austria) , 2016 .

[38]  Jolanta Miadlikowska,et al.  Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota). , 2016, Molecular phylogenetics and evolution.

[39]  Olga Chernomor,et al.  Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices , 2016, Systematic biology.

[40]  M. Stadler,et al.  New species and reports of Hypoxylon from Argentina recognized by a polyphasic approach , 2016, Mycological Progress.

[41]  Anna Lechner,et al.  Molecular networking and pattern-based genome mining improves discovery of biosynthetic gene clusters and their products from Salinispora species. , 2015, Chemistry & biology.

[42]  K. Hyde,et al.  Anthostomella is polyphyletic comprising several genera in Xylariaceae , 2015, Fungal Diversity.

[43]  K. Hyde,et al.  Discovery of new mitorubrin derivatives from Hypoxylon fulvo-sulphureum sp. nov. (Ascomycota, Xylariales) , 2015, Mycological Progress.

[44]  Ondřej Koukol,et al.  Recent observations of sooty bark disease of sycamore maple in Prague (Czech Republic) and the phylogenetic placement of Cryptostroma corticale , 2015 .

[45]  K. Hyde,et al.  Lenormandins A—G, new azaphilones from Hypoxylon lenormandii and Hypoxylon jaklitschii sp. nov., recognised by chemotaxonomic data , 2015, Fungal Diversity.

[46]  M. Stadler,et al.  A polyphasic taxonomy of Daldinia (Xylariaceae) , 2014, Studies in mycology.

[47]  M. Stadler,et al.  Hypoxyvermelhotins A-C, new pigments from Hypoxylon lechatii sp. nov. , 2014, Fungal biology.

[48]  M. Stadler,et al.  Cohaerins G-K, azaphilone pigments from Annulohypoxylon cohaerens and absolute stereochemistry of cohaerins C-K. , 2013, Phytochemistry.

[49]  M. Stadler,et al.  Theissenia reconsidered, including molecular phylogeny of the type species T. pyrenocrata and a new genus Durotheca (Xylariaceae, Ascomycota) , 2013, IMA fungus.

[50]  M. Stadler,et al.  New Hypoxylon species from Martinique and new evidence on the molecular phylogeny of Hypoxylon based on ITS rDNA and β-tubulin data , 2013, Fungal Diversity.

[51]  Jesús Martín,et al.  Hypoxylon pulicicidum sp. nov. (Ascomycota, Xylariales), a Pantropical Insecticide-Producing Endophyte , 2012, PloS one.

[52]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[53]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[54]  O. Gascuel,et al.  Survey of Branch Support Methods Demonstrates Accuracy, Power, and Robustness of Fast Likelihood-based Approximation Schemes , 2011, Systematic biology.

[55]  M. Stadler,et al.  Three new Xylaria species from southwestern Europe , 2011, Mycological Progress.

[56]  M. Stadler,et al.  New species of Hypoxylon from western Europe and Ethiopia. , 2010 .

[57]  M. Stadler,et al.  Lepraric acid derivatives as chemotaxonomic markers in Hypoxylon aeruginosum, Chlorostroma subcubisporum and C. cyaninum, sp. nov. , 2010, Fungal biology.

[58]  J. Rogers,et al.  Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily. , 2010, Molecular phylogenetics and evolution.

[59]  K. Hyde,et al.  The new genus Rostrohypoxylon and two new Annulohypoxylon species from Northern Thailand , 2010, Fungal Diversity.

[60]  R. Jeewon,et al.  A re-evaluation of the evolutionary relationships within the Xylariaceae based on ribosomal and protein-coding gene sequences , 2009 .

[61]  M. Stadler,et al.  The "red Hypoxylons" of the temperate and subtropical Northern hemisphere , 2008 .

[62]  M. Piepenbring,et al.  Affinities of Phylacia and the daldinoid Xylariaceae, inferred from chemotypes of cultures and ribosomal DNA sequences. , 2008, Mycological research.

[63]  Y. Ju,et al.  Theissenia rogersii sp. nov. and phylogenetic position of Theissenia , 2007 .

[64]  J. Rogers,et al.  An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny , 2006 .

[65]  M. Stadler,et al.  Cohaerins C–F, four azaphilones from the xylariaceous fungus Annulohypoxylon cohaerens , 2006 .

[66]  M. Stadler,et al.  Antimicrobial azaphilones from the fungus Hypoxylon multiforme. , 2005, Planta medica.

[67]  J. Rogers,et al.  Molecular phylogeny of Hypoxylon and closely related genera , 2005 .

[68]  M. Stadler,et al.  Cohaerins A and B, azaphilones from the fungus Hypoxylon cohaerens, and comparison of HPLC-based metabolite profiles in Hypoxylon sect. Annulata. , 2005, Phytochemistry.

[69]  M. Stadler,et al.  Phylogenetic relationships among Daldinia, Entonaema, and Hypoxylon as inferred from ITS nrDNA analyses of Xylariales , 2005 .

[70]  J. Rogers,et al.  The genus Theissenia: T. pyrenocrata, T. cinerea sp. nov., and T. eurima sp. nov , 2003, Mycologia.

[71]  Hidetoshi Shimodaira.  An approximately unbiased test of phylogenetic tree selection. , 2002, Systematic biology.

[72]  B. Hall,et al.  Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. , 1999, Molecular biology and evolution.

[73]  K. O’Donnell,et al.  Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. , 1997, Molecular phylogenetics and evolution.

[74]  R. Vilgalys,et al.  Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species , 1990, Journal of bacteriology.

[75]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[76]  J. Rogers.  Hypoxylon duranii sp. nov. and the anamorphs of H. caries, H. papillatum, and Rosellinia subiculata , 1985 .