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Wood Staining Fungi Revealed Taxonomic Novelties in Pezizomycotina: New Order Superstratomycetales and New Species Cyanodermella Oleoligni

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Wood Staining Fungi Revealed Taxonomic Novelties in Pezizomycotina: New Order Superstratomycetales and New Species Cyanodermella Oleoligni Wood staining fungi revealed taxonomic novelties in Pezizomycotina: new order Superstratomycetales and new species Cyanodermella oleoligni Citation for published version (APA): van Nieuwenhuijzen, E. J., Miadlikowska, J. M., Houbraken, J. A. M. P., Adan, O. C. G., Lutzoni, F. M., & Samson, R. A. (2016). Wood staining fungi revealed taxonomic novelties in Pezizomycotina: new order Superstratomycetales and new species Cyanodermella oleoligni. Studies in Mycology, 85, 107-124. https://doi.org/10.1016/j.simyco.2016.11.008 Document license: CC BY-NC-ND DOI: 10.1016/j.simyco.2016.11.008 Document status and date: Published: 01/09/2016 Document Version: Publisher’s PDF, also known as Version of Record (includes final page, issue and volume numbers) Please check the document version of this publication: • A submitted manuscript is the version of the article upon submission and before peer-review. There can be important differences between the submitted version and the official published version of record. People interested in the research are advised to contact the author for the final version of the publication, or visit the DOI to the publisher's website. • The final author version and the galley proof are versions of the publication after peer review. • The final published version features the final layout of the paper including the volume, issue and page numbers. Link to publication General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal. If the publication is distributed under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license above, please follow below link for the End User Agreement: www.tue.nl/taverne Take down policy If you believe that this document breaches copyright please contact us at: [email protected] providing details and we will investigate your claim. Download date: 07. Oct. 2021 available online at www.studiesinmycology.org STUDIES IN MYCOLOGY 85: 107–124. Wood staining fungi revealed taxonomic novelties in Pezizomycotina: New order Superstratomycetales and new species Cyanodermella oleoligni E.J. van Nieuwenhuijzen1, J.M. Miadlikowska2*, J.A.M.P. Houbraken1*, O.C.G. Adan3, F.M. Lutzoni2, and R.A. Samson1 1CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; 2Department of Biology, Duke University, Durham, NC 27708, USA; 3Department of Applied Physics, Eindhoven University of Technology, P.O. Box 513, 5600 MB Eindhoven, The Netherlands *Correspondence: J.M. Miadlikowska, [email protected]; J.A.M.P. Houbraken, [email protected] Abstract: A culture-based survey of staining fungi on oil-treated timber after outdoor exposure in Australia and the Netherlands uncovered new taxa in Pezizomycotina. Their taxonomic novelty was confirmed by phylogenetic analyses of multi-locus sequences (ITS, nrSSU, nrLSU, mitSSU, RPB1, RPB2, and EF-1α) using multiple reference data sets. These previously unknown taxa are recognised as part of a new order (Superstratomycetales) potentially closely related to Trypetheliales (Dothideomycetes), and as a new species of Cyanodermella, C. oleoligni in Stictidaceae (Ostropales) part of the mostly lichenised class Lecanoromycetes. Within Superstratomycetales a single genus named Superstratomyces with three putative species: S. flavomucosus, S. atroviridis, and S. albomucosus are formally described. Monophyly of each circumscribed Superstratomyces species was highly supported and the intraspecific genetic variation was substantially lower than interspecific differences detected among species based on the ITS, nrLSU, and EF-1α loci. Ribosomal loci for all members of Superstratomyces were noticeably different from all fungal sequences available in GenBank. All strains from this genus grow slowly in culture, have darkly pigmented mycelia and produce pycnidia. The strains of C. oleoligni form green colonies with slimy masses and develop green pycnidia on oatmeal agar. These new taxa could not be classified reliably at the class and lower taxonomic ranks by sequencing from the substrate directly or based solely on culture-dependent morphological investigations. Coupling phenotypic observations with multi-locus sequencing of fungi isolated in culture enabled these taxonomic discoveries. Outdoor situated timber provides a great potential for culturable undescribed fungal taxa, including higher rank lineages as revealed by this study, and therefore, should be further explored. Key words: Classification of Pezizomycotina, Cyanodermella oleoligni, Dothideomycetes, Fungal cultures, Multi-locus phylogeny, Oil-treated wood, Ostropales, Superstratomycetales. Taxonomic novelties: New order: Superstratomycetales van Nieuwenhuijzen, Miadlikowska, Lutzoni & Samson, New family: Superstratomycetaceae van Nieuwenhuijzen, Miadlikowska, Lutzoni & Samson, New genus: Superstratomyces van Nieuwenhuijzen, Miadlikowska & Samson, New species: Cyanodermella oleoligni van Nieuwenhuijzen & Samson, Superstratomyces albomucosus van Nieuwenhuijzen & Samson, S. atroviridis van Nieuwenhuijzen & Samson, S. flavomucosus van Nieuwenhuijzen & Samson. Available online 27 November 2016; http://dx.doi.org/10.1016/j.simyco.2016.11.008. INTRODUCTION fungus Aureobasidium (van Nieuwenhuijzen et al. 2016, unpubl. data). However, not all cultures, even if characterised with mo- Microbial community composition can be an informative char- lecular data, could be identified taxonomically. acteristic of an organism, substrate, or habitat. A distinction is Among the predominant cultured fungal colonies obtained made between desirable balanced microbial communities and from fungal stained wood surfaces, two types of coelomycetes unbalanced or disturbed communities, for example, in intestines remained unclassified (van Nieuwenhuijzen et al. unpubl. data). (Roeselers et al. 2011, Gouba et al. 2013) and on skin (Findley One type involved isolates with darkly coloured pycnidia et al. 2013, Lloyd-Price et al. 2016), as well as in tap water (referred here as the “dark” group) obtained from several oil- (Roeselers et al. 2015, Babic et al. 2016) soils (Barot et al. 2007, treated and untreated wood samples situated at an outdoor Creamer et al. 2016) or on wood (Sailer et al. 2010, Purahong test site in the Netherlands. Isolates of the other type had green et al. 2016). In order to broaden the understanding, and coloured pycnidia (referred here as the “green” group) and were improve applications, of beneficial microbial communities, it is obtained from a single oil-treated wood sample exposed to essential that all taxa in these communities are identified. outdoor conditions at a selected site in Australia. Neither As part of a study on natural fungal-based wood finishes morphological nor molecular data for these two fungal groups (biofinishes), fungal compositions on outdoor exposed wood matched currently known described species. samples were studied using a culture-based method. Fungi were The aim of this study was to further investigate the phylo- sampled from untreated and oil-treated wood that contained dark genetic affiliations and taxonomic identities of 26 pycnidia- fungal stains due to outdoor exposure. Several oil-treated wood producing fungi isolated from oil-treated wood exposed to out- samples had dense stained surfaces that met the desirable door conditions. We sequenced four ribosomal and three protein- biofinish criteria of surface coverage and pigmentation (van coding loci of representative fungal strains and inferred their Nieuwenhuijzen et al. 2015). DNA sequencing of the resulting phylogenetic relationships using multiple data sets including fungal cultures showed that these biofinishes were composed of kingdom-, subphylum-, class- and order-wide taxonomic con- multiple genera, always containing the common wood staining texts. Furthermore, we conducted a detailed morphological Studies in Mycology Peer review under responsibility of CBS-KNAW Fungal Biodiversity Centre. Copyright © 2016, CBS-KNAW Fungal Biodiversity Centre. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). 107 VAN NIEUWENHUIJZEN ET AL. investigation of these fungal isolates. As a result, a new mono- against the CBS-KNAW database. Based on this screening, strain generic order Superstratomycetales (Dothideomycetes) con- CBS 353.84 was added to the 22 fungal isolates of the “dark” group, taining three newly proposed species, and a new species subjected to morphological examination, and DNA was extracted Cyanodermella oleoligni (Ostropales, Lecanoromycetes) are from a fresh culture (Table 1). Subsequently, the translation elon- formally described here. gation factor 1 alpha (EF-1α) was obtained for all strains of the “dark” group. The nuclear ribosomal small subunit (nrSSU), the mitochondrial ribosomal small subunit (mitSSU), and two additional MATERIALS AND METHODS protein-coding genes, namely the largest and second largest subunits of RNA polymerase II (RPB1 and RPB2,
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