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Minutisphaerales (Dothideomycetes, Ascomycota): a New Order of Freshwater Ascomycetes Including a New Family, Minutisphaeraceae

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Minutisphaerales (Dothideomycetes, Ascomycota): a New Order of Freshwater Ascomycetes Including a New Family, Minutisphaeraceae Minutisphaerales (Dothideomycetes, Ascomycota): a new order of freshwater ascomycetes including a new family, Minutisphaeraceae, and two new species from North Carolina, USA By: Huzefa A. Raja, Tamam El-Elimat, Nicholas H. Oberlies, Carol A. Shearer, Andrew N. Miller, Kazuaki Tanaka, Akira Hashimoto, Jacques Fournier Raja, H.A., El-Elimat, T., Oberlies, N.H., Shearer, C.A., Miller, A.N., Tanaka, K., Hashimoto, A., Fournier, J. 2015. Minutisphaerales (Dothideomycetes, Ascomycota): a new order of freshwater ascomycetes including a new family, Minutisphaeraceae, and two new species from North Carolina, USA. Mycologia. 107,4: 845-62. doi: 10.3852/15-013. Made available courtesy of Mycological Society of America: http://dx.doi.org/10.3852/15- 013 ***© Mycological Society of America. Reprinted with permission. No further reproduction is authorized without written permission from Mycological Society of America. This version of the document is not the version of record. Figures and/or pictures may be missing from this format of the document. *** Abstract: Minutisphaera is a recently established genus of freshwater Dothideomycetes characterized by small, globose to subglobose or apothecioid, erumpent to superficial, brown ascomata; fissitunicate, eight-spored, ovoid to obclavate asci; and 1–2-septate, clavate to broadly fusiform, hyaline to pale brown ascospores with or without a gelatinous sheath and filamentous appendages. The genus currently contains two species: M. fimbriatispora, the type species, and M. japonica. The higher-level phylogenetic relationship of Minutisphaerawithin the Dothideomycetes currently is unresolved. To establish the phylogenetic position of Minutisphaera within the Dothideomycetes and evaluate the phylogenetic affinities of newly collected Minutisphaera-like taxa, we sequenced three rDNA regions—18S, ITS1-5.8SITS2 (ITS) and 28S nuc rDNA, and a protein-coding gene, MCM7, for newly collected strains of Minutisphaera.Based on maximum likelihood and Bayesian analyses of a combined dataset (18S and 28S) composed of 167 taxa, a more refined dataset (28S and MCM7) comprising 52 taxa and a separate ITS dataset, and an examination of morphology, we describe and illustrate two new species of Minutisphaera. TheMinutisphaera clade was strongly supported within the Dothideomycetes with likelihood and Bayesian statistics but did not share phylogenetic affinities with any existing taxonomic group within the Dothideomycetes. We therefore establish a new order, Minutisphaerales, and new family, Minutisphaeraceae, for this monophyletic clade of freshwater ascomycetes. Chemical analysis of the organic extract M. aspera (G427) resulted in isolation and characterization of five known secondary metabolites, of which four were dipeptides (1–4) and one an aromatic polyketide (5). Conversely, two aromatic polyketides (5, 6) were isolated and identified from the organic extract of M. parafimbriatispora(G156-4). The isolated compounds were tested for their antimicrobial activity against an array of bacteria and fungi. Compound 6 showed promising activity against Staphylococcus aureus and Mycobacterium smegmatis with minimal inhibitory concentration values of 30 and 60 μg/mL, respectively. Keywords: Aquatic | microfungi | submerged wood | systematics Article: ***Note: Full text of article below Mycologia, 107(4), 2015, pp. 845–862. DOI: 10.3852/15-013 # 2015 by The Mycological Society of America, Lawrence, KS 66044-8897 Minutisphaerales (Dothideomycetes, Ascomycota): a new order of freshwater ascomycetes including a new family, Minutisphaeraceae, and two new species from North Carolina, USA Huzefa A. Raja1 and MCM7) comprising 52 taxa and a separate ITS Tamam El-Elimat dataset, and an examination of morphology, we Nicholas H. Oberlies describe and illustrate two new species of Minuti- Department of Chemistry and Biochemistry, University sphaera. The Minutisphaera clade was strongly sup- of North Carolina, Greensboro, North Carolina 27402 ported within the Dothideomycetes with likelihood Carol A. Shearer and Bayesian statistics but did not share phylogenetic Department of Plant Biology, University of Illinois, affinities with any existing taxonomic group within Urbana, Illinois 61801 the Dothideomycetes. We therefore establish a new order, Minutisphaerales, and new family, Minuti- Andrew N. Miller sphaeraceae, for this monophyletic clade of freshwa- Illinois Natural History Survey, University of Illinois, ter ascomycetes. Chemical analysis of the organic Champaign, Illinois 61820 extract M. aspera (G427) resulted in isolation and Kazuaki Tanaka characterization of five known secondary metabolites, Faculty of Agriculture and Life Sciences, Hirosaki of which four were dipeptides (1–4) and one an University, Bunkyo-cho, Hiroskaki, Aomori 036-8561, aromatic polyketide (5). Conversely, two aromatic Japan polyketides (5, 6) were isolated and identified from Akira Hashimoto the organic extract of M. parafimbriatispora (G156-4). The United Graduate School of Agricultural Sciences, The isolated compounds were tested for their Iwate University, 18-8 Ueda 3 chome, Morioka 020- antimicrobial activity against an array of bacteria 8550, Japan and fungi. Compound 6 showed promising activity Jacques Fournier against Staphylococcus aureus and Mycobacterium Las Muros, 09420 Rimont, France smegmatis with minimal inhibitory concentration values of 30 and 60 mg/mL, respectively. Key words: Aquatic, microfungi, submerged Abstract: Minutisphaera is a recently established wood, systematics genus of freshwater Dothideomycetes characterized by small, globose to subglobose or apothecioid, INTRODUCTION erumpent to superficial, brown ascomata; fissituni- cate, eight-spored, ovoid to obclavate asci; and 1–2- The freshwater Dothideomycetes currently comprises septate, clavate to broadly fusiform, hyaline to pale 200 taxa (32%) of ca. 622 ascomycetes reported from brown ascospores with or without a gelatinous sheath freshwater habitats (Shearer et al. 2014). In the past and filamentous appendages. The genus currently few years molecular phylogenetic studies have ad- contains two species: M. fimbriatispora,thetype vanced our understanding of the systematics of species, and M. japonica. The higher-level phyloge- freshwater Dothideomycetes (Inderbitzin et al. 2001, netic relationship of Minutisphaera within the Dothi- Schoch et al. 2009, Shearer et al. 2009, Hirayama et al. deomycetes currently is unresolved. To establish the 2010, Ferrer et al. 2011, Suetrong et al. 2011, Hyde et phylogenetic position of Minutisphaera within the al. 2013, Shearer et al. 2014). These studies have Dothideomycetes and evaluate the phylogenetic indicated that members of freshwater Dothideomy- affinities of newly collected Minutisphaera-like taxa, cetes are (i) distinct from terrestrial Dothideomycete we sequenced three rDNA regions—18S, ITS1-5.8S- lineages, (ii) have adapted to freshwater habitats ITS2 (ITS) and 28S nuc rDNA, and a protein-coding numerous times and (iii) most have phylogenetic gene, MCM7, for newly collected strains of Minuti- affinites to the subclass Pleosporomycetidae. Only sphaera. Based on maximum likelihood and Bayesian one taxon was described originally from freshwater analyses of a combined dataset (18S and 28S) (e.g. Mycosphaerella aquatica, Capnodiales) from composed of 167 taxa, a more refined dataset (28S submerged wood in a water cooling tower. Three other Mycosphaerella spp. reported from freshwater Submitted 20 Jan 2015; accepted for publication 23 Apr 2015. are related to the Dothideomycetidae (Shearer and 1 Corresponding author. E-mail: [email protected] Raja 2014), whereas only a few taxa are related to the 845 846 MYCOLOGIA Tubeufiales, Pleosporomycetidae (Boonmee et al. The goals of this study were to: (i) describe and 2014). Despite the progress in our understanding of illustrate the newly collected Minutisphaera spp. from the systematics of Dothideomycetes (Hyde et al. 2013) freshwater habitats in the Piedmont region; (ii) place and specifically freshwater Dothideomycetes (Shearer these newly collected taxa into a molecular phyloge- et al. 2009, Shearer et al. 2014) a number of newly netic framework by constructing a molecular phylog- described and/or previously reported taxa from eny of Minutisphaera spp. using partial 18S, internal freshwater are currently incertae sedis and their transcribed spacer regions (ITS) and partial 28S family and ordinal level positions within the Dothi- rDNA sequences, as well as the minichromosome deomycetes remain obscure (Hyde et al. 2013). One maintenance protein complex 7 gene (MCM7), to such freshwater dothideomycete genus is Minuti- better understand both the species as well as higher- sphaera. level relationships of Minutisphaera spp. within the Minutisphaera Shearer, A.N. Mill & Ferrer, typified Dothideomycetes; and (iii) screen isolates of newly by M. fimbriatispora Shearer, A.N. Mill & Ferrer collected species for secondary metabolites to de- originally was described from submerged wood in termine the relationships between secondary prod- freshwater habitats from USA (Ferrer et al. 2011). ucts of both screened and unscreened isolates. More recently a new species of Minutisphaera, M. japonica, was described and illustrated from Japan. MATERIALS AND METHODS This species is phylogenetically related to M. fimbria- tispora based on rDNA sequence comparisons (Raja et Collection, morphological examination and fungal isolates.— al. 2013b). In addition to the newly found M. Methods of collection, isolation and morphological
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