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Fungal Diversity in the Southwestern US

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Fungal Diversity in the Southwestern US Fungal Diversity in the Southwestern US Sco T. Bates Fierer Laboratory Cooperave Instute for Research in Environmental Sciences University of Colorado, Boulder, CO, USA International Journal of Systematic and Evolutionary Microbiology (2006), 56, 2697–2702 DOI 10.1099/ijs.0.64332-0 Exophiala crusticola anam. nov. (affinity Herpotrichiellaceae), a novel black yeast from biological soil crusts in the Western United States Scott T. Bates,3 Gundlapally S. N. Reddy3 and Ferran Garcia-Pichel Correspondence School of Life Sciences, Arizona State University, Main Campus, Tempe, AZ-85287-4501, Ferran Garcia-Pichel USA [email protected] A novel black yeast-like fungus, Exophiala crusticola, is described based on two closely related isolates from biological soil crust (BSC) samples collected on the Colorado Plateau (Utah) and in the Great Basin desert (Oregon), USA. Their morphology places them in the anamorphic genus Exophiala, having affinities to the family Herpotrichiellaceae (Ascomycota). Phylogenetic analysis of their D1/D2 large subunit nuclear ribosomal RNA (LSU nrRNA) gene sequences suggests that they represent a distinct species. The closest known putative relative to Exophiala crusticola is Capronia coronata Samuels, isolated from decorticated wood in Westland County, New Zealand. The holotype for Exophiala crusticola anam. nov. is UAMH 10686 and the type strain is CP141bT (=ATCC MYA-3639T=CBS 119970T=DSM 16793T). Dark-pigmented fungi appear to constitute an important heterotrophic component of soil crusts and Exophiala crusticola represents the first description of a dematiaceous fungus isolated from BSCs. Biological soil crusts (BSCs) are formed by communities of of BSCs or the contributions that they make to crust ecology. micro-organisms that bind together the upper strata of soil Here, two black yeast-like fungal strains (CP141bT and and are common in arid lands, such as those found in the OR302-3) isolated from BSCs are described as a novel Western United States (Belnap & Gardner, 1993). BSCs in species of the genus Exophiala within the family arid lands are predominantly composed of cyanobacteria, Herpotrichiellaceae. mosses and lichens. Recent culture-dependent and inde- pendent studies have demonstrated that heterotrophic bac- Members of the family Herpotrichiellaceae exhibit a diverse teria belonging to the phyla Actinobacteria, Proteobacteria polymorphic life cycle and, therefore, can be difficult to and Bacteroidetes are also major components of BSCs (Smith identify by morphology alone. However, the use of nuclear et al., 2004; Nagy et al., 2005; Gundlapally & Garcia-Pichel, ribosomal RNA (nrRNA) gene sequence data has facilitated 2006) and an effort has been made to culture and report on identification and classification of these organisms (see isolates from BSCs that are members of these phyla (Reddy Spatafora et al., 1995; Untereiner & Naveau, 1999; de Hoog & Garcia-Pichel, 2005; Reddy et al., 2006). Although fungi etal., 2003). The familyis representedbythe teleomorphgenus have been identified as components of BSCs (Belnap et al., Capronia and the anamorphic genera Cladophialophora, 2001; Fletcher & Martin, 1948; Garcia-Pichel, 2002; Galun & Exophiala, Fonsecaea, Phaeococcomyces, Phialophora, Rami- Garty, 2001), few studies (e.g. Grishkan et al., 2006; States & chloridium and Rhinocladiella (Untereiner & Naveau, 1999). Christensen, 2001) have investigated the fungal constituents These fungi, commonly called black yeasts, are characterized by the presence of melanin or melanin-like pigments in the cell walls and by a yeast-like growth during part of their life cycles 3These authors contributed equally to this work. (Haase et al., 1999). Exophiala is also characterized by an Abbreviations: BSC, biological soil crust; EPS, extracellular polysac- annellidic form of blastic conidiogenesis and by conidiogen- charides; LSU, large subunit; nrRNA, nuclear ribosomal RNA. ous cells that are often inconspicuously annellate (de Hoog & The GenBank/EMBL/DDBJ accession numbers for the D1/D2 large Hermanides-Nijhof,1977).TheDictionaryofFungi(Kirketal., T subunit nuclear ribosomal RNA gene sequences of strains CP141b 2001) cites twelve species in the genus Exophiala; however, and OR302-3 are AM048755 and DQ777875, respectively. The accession number for the sequence of the internal transcribed spacer additional species have been described more recently (e.g. de of the nuclear ribosomal RNA gene for strain CP141bT is AM048756. Hoog et al., 2003). Some species of the genus Exophiala are known as occasional opportunistic human pathogens (de Comparisons of the nucleotide sequences of the D1/D2 large subunit nuclear ribosomal RNA gene of Exophiala crusticola and related taxa, Hoog et al., 2003; Haase et al., 1999). details of the characteristics that distinguish strains CP141bT and OR302-3 and an additional phylogenetic tree are available as Capronia coronata Samuels, having an Exophiala anamorph supplementary material in IJSEM Online. and isolated from decorticated wood in the Westland 64332 G 2006 IUMS Printed in Great Britain 2697 Sonoran Desertscrub Arizona Bioc Communies • Alpine Tundra • Subalpine Grassland • Petran Subalpine • Plains & Great Basin Conifer Forest Grassland • Semidesert Grassland • Petran Montane • Great Basin Desertscrub Forest • Mojave Desertscrub • Great Basin Conifer • Chihuahuan Desertscrub Woodland • Sonoran Desertscrub • Madrean Evergreen – Lower Colorado R.V. – AZ Uplands Woodland • Interior Chaparral Fungal Biodiversity 6 fungal species per single plant species =1.5 million fungal species worldwide Hawksworth, D.L. (1991) The fungal dimension of biodiversity : magnitude, significance, and conservaHon. Mycological Research 95: 641-655 ----------------------------------------- 74,000 to120,000 fungi known 500,000 to 9.9 million esmated 0. 75% - 24% of total described Fungal Biodiversity in Arizona vascular plants = ~4000 species 4000 x 6 = 24,000 potenal species of fungi ----------------------------- Macrofungi ~1200 spp. (S.T. Bates 2006) Lichenized Fungi ~900 spp. (T.H. Nash III et al. 2002-2004) Soil Fungi and Fungi Associated w/ BSCs ~300 spp. Endophyc ~ 500 spp. (pers. comm. A.E. Arnold) ----------------------------- ~2900 fungal species known from Arizona 21,100 fungal species le to document Boletus pulchriceps Did sequencing reveal unexpected changes in idenficaon or unexpected diversity? Did examining specimens reveal previously undocumented fungal diversity? New Arizona records of gasteroid fungi • Bovista aesvalis • Disciseda verrucosa • Bovista dermoxantha • Holocotylon brandegeeanum • Bovista plumbea • Lycoperdon lividum • Calvaa bicolor • Lycoperdon marginatum • Calvaa booniana • Lycoperdon molle • Calvaa craniiformis • Lycoperdon perlatum • Calvaa cyathiformis • Lycoperdon pulcherrimum • Calvaa fragilis • Lycoperdon rimulatum • Calvaa cf. leiospora • Lycoperdon umbrinum • Calvaa pachyderma • Lycoperdon pyriforme • Calvaa rugosa • Mycenastrum corium • Disciseda candida • Vascellum intermedium • Disciseda cervina • Vascellum lloydianum • Disciseda hyalothrix • Vascellum texense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