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Intraspecific Variation and Emendation of Hannaella Kunmingensis

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Intraspecific Variation and Emendation of Hannaella Kunmingensis Mycol Progress DOI 10.1007/s11557-012-0846-6 SHORT COMMUNICATION Intraspecific variation and emendation of Hannaella kunmingensis Ifeloju Dayo-Owoyemi & Andre Rodrigues & Melissa F. Landell & Patricia Valente & Ulrich G. Mueller & Jesus Pais Ramos & Fernando C. Pagnocca Received: 13 December 2011 /Revised: 17 July 2012 /Accepted: 19 July 2012 # German Mycological Society and Springer 2012 Abstract In order to investigate the intraspecific variability differences in 31 out of 64 phenotypic characteristics exam- in Hannaella kunmingensis, 11 isolates, including the type ined, including growth in lactose, vitamin free medium, strain, were analyzed for their morphological and biochem- xylitol, L-arabinitol, and nitrite. Growth in the presence of ical traits. The combined internal transcribed spacer region 0.1 % cycloheximide was also highlighted in H. kunmin- (ITS), D1/D2 domains of the large subunit rDNA (LSU), gensis. All the 11 strains were conspecific in the LSU; and cytochrome b gene were examined using phylogenetic however, variations of about 2.5 % were found in the ITS and parsimony network analyses. Our investigations while isolate CBS 8356 exhibited a 27.3 % divergence from revealed differences in colony morphology as well as the other strains in the cytochrome b gene. Parsimony net- work analysis revealed the existence of three haplotypes among the H. kunmingensis strains studied but excluded Electronic supplementary material The online version of this article CBS 8356 from the network connecting these haplotypes. (doi:10.1007/s11557-012-0846-6) contains supplementary material, which is available to authorized users. This study contributes to the knowledge of the intraspecific diversity of H. kunmingensis. To accommodate such intra- I. Dayo-Owoyemi : A. Rodrigues : F. C. Pagnocca Centro de Estudo de Insetos Sociais, Instituto de Biociências, specific variations, an emendation of the species diagnosis is UNESP—Univ Estadual Paulista, proposed. Rio Claro, SP 13506-900, Brasil * : : I. Dayo-Owoyemi ( ) A. Rodrigues F. C. Pagnocca Introduction Departamento de Bioquímica e Microbiologia, Instituto de Biociências, UNESP—Univ Estadual Paulista, Rio Claro, SP 13506-900, Brasil Long before the current era of species identification by e-mail: [email protected] DNA comparisons, yeasts were delineated based on differences in morphological and phenotypic attributes M. F. Landell : P. Valente Centro de Biotecnologia, (Kurtzman 2011). Most of these characteristics are variable, UFRGS—Universidade Federal do Rio Grande do Sul, hence, the need for more accurate diagnostic tools for yeast Porto Alegre, RS 91501-970, Brasil species identification soon became apparent (Kurtzman and Fell 2006;Kurtzman2011). The use of DNA sequence M. F. Landell : P. Valente Departamento de Microbiologia, Imunologia e Parasitologia, comparisons for yeast identification was widely embraced UFRGS—Universidade Federal do Rio Grande do Sul, after Kurtzman and Robnett (1998) predicted that strains Porto Alegre, RS 90050-170, Brasil showing six or more nucleotide differences (1 % substitu- tion) in the D1/D2 domains of the large subunit rDNA U. G. Mueller Section of Integrative Biology, University of Texas at Austin, (LSU) are likely to represent different species particularly Austin, TX 78712, USA for ascomycetous yeasts. Complementary D1/D2 (Fell et al. 2000) and internal transcribed spacer (ITS) databases J. P. Ramos (Sugita et al. 1999, 2000; Scorzetti et al. 2002) were estab- Laboratório de Referência Nacional para Tuberculose, Centro de Referência Prof. Hélio Fraga, ENSP/FIOCRUZ, lished for basidiomycetous yeasts and are continually being Rio de Janeiro, RJ 22780-192, Brasil updated by describers of new taxa. Mycol Progress The extent of phenotypic and genetic variations among Phytophthora cinnamomi Rands (Martin and Coffey 2012) basidiomycetous yeast strains that share a common gene as well as species boundaries in cephalotrichid nemerteans pool have been continuously revealed by several studies (Chen et al. 2010). According to Kurata et al. (2008) parsi- (Scorzetti et al. 2002;Kurtzmanetal.2011a). Typical mony analysis of the chloroplast DNA of the pitcher plant examples include intraspecific diversity exhibited by some Nepenthes vieillardii Hook. F. (Nepenthaceae) in New Cryptococcus species. Based on their serological variances, Caledonia revealed the presence of 17 haplotypes within strains of C. neoformans (San Felice) Vuill. and C. gattii this species. (Vanbreus. & Takashio) Kwon-Chung & Boekhout have Recent phylogenetic revision of the Luteolus lineage been classified into serotypes A, D and AD for the former, in Tremelalles based on sequences of the nuclear rRNA and B and C for the latter (Boekhout et al. 2001; Kwon- (18S rDNA, ITS and LSU) and mitochondrial cytochrome Chung et al. 2002; Bovers et al. 2006, 2008). Although with b genes led to the creation of two genera, namely no genetic variation, heterogeneity in colony morphology Derxomyces and Hannaella (Wang and Bai 2008). While and physiological characteristics were observed in species the genus Derxomyces (type species: Derxomyces mrakii of C. victoriae M.J. Montes et al., with the color ranging (Hamam. & Nakase) F.Y. Bai & Q.M. Wang) was proposed from cream, pale yellowish-brown to pinkish and the sur- to accommodate species in the Bullera mrakii Hamam. & face ranging from smooth, somewhat warty or reticulate Nakase clade, the genus Hannaella accommodates species (Montes et al. 1999; Thomas-Hall et al. 2002). Rhode in the Bullera sinensis M.X. Li clade (formerly classified in (2006) reported differences in the carbon assimilation pro- Bullera and Cryptococcus). Therefore, yeast species formerly files and growth temperature requirements of 35 strains of classified in the genera Cryptococcus and Bullera within these C. laurentii (Kuff.) C.E. Skinner isolated from a soil sample clades have been re-classified as Derxomyces or Hannaella while Sugita et al. (2000) also reported intraspecific ITS (Wang and Bai 2008). diversity among some other strains of this species. Here we report results of intraspecific diversity within the Intraspecific variations have also been reported for taxon Hannaella kunmingensis F.Y. Bai, M. Takash. & mating strains of the same species. For example, sexually Nakase ex F.Y. Bai & Q.M. Wang, anamorphic basidiomy- compatible strains of the heterothallic species Sporidiobolus cetous yeast formerly described as Bullera kunmingensis salmonicolor Fell & Tallman (CBS 490 and CBS 2630) F.Y. Bai, M. Takash. & Nakase. We subjected 11 strains were found to differ by seven and 26 nucleotide positions (including the type strain CBS 8960T) isolated from different in the LSU and ITS, respectively (Sampaio 2011). substrates and geographic locations, to detailed physiological Inference of evolutionary relationships between different tests and genetic characterization using phylogenetic and par- yeasts has, over the years, relied mostly on trees derived simony network analysis (TCS). Based on our findings, an from phylogenetic analyses of rDNA sequence data. emendation of Hannaella kunmingensis is proposed. However, studies have revealed that phylogenetic trees sometimes do not accurately measure gene genealogies of haplotypes resulting from intraspecific polymorphisms Materials and methods (Clement et al. 2000; Posada and Crandall 2001). Parsimony network analysis (TCS) on the other hand provides the Strains used advantage of a network that discriminates better among haplotypes than a tree with dichotomic splits (Hart and A total of 11 strains of H. kunmingensis were used in this Sunday 2007). Studies applying parsimony network study (Table S1). Strains ATT 066, ATT 082 and ATT 265 analysis for the estimation of gene genealogies in basidio- were isolated from fungus gardens of the leafcutter ant Atta mycetous yeasts are scanty. However, by analyzing the LSU texana Buckley at Hornsby Bend Environmental Research and ITS of multiple isolates of the ascomycetous yeast Center, Austin, Texas, USA. Two strains, ATT 082 and ATT Candida apicola (Hajsig) S. A. Mey. & Yarrow, 28 out of 066, were isolated during the winter season from nests at 30 strains which could have otherwise been classified into two different locations (30°13′97″N, 97°39′10″W and 30° separate species if the criterion predicted by Kurtzman and 13′94″N, 97°39′18″W for nests UGM060121-01 and Robnett (1998) were adopted, were retained in this species UGM060121-02, respectively); while strain ATT 265 was (Lachance et al. 2010). Applying similar analysis to 81 isolated during fall season from nest UGM060121-01. For strains formerly classified in Candida azyma (van der Walt, yeast isolation, 1 g of each garden sample was initially diluted Johannsen & Yarrow) S.A. Mey. & Yarrow, Lachance et al. ten-fold in 0.05 % Tween 80 and 0.2 % peptone water and (2010) reassigned 57 isolates to the new species C. para- plated in YMA with antibiotic (Rodrigues et al. 2009). zyma Lachance while only 18 isolates were retained in C. Five strains originating from Brazil (BI 96, BI 203, BI azyma. Besides yeast taxonomy, parsimony network analy- 254, BI 279 and BI 319) were isolated from three bromeliad sis has been used to determine mitochondrial haplotypes in plants (Landell et al. 2006). Leaves and flowers of the Mycol Progress bromeliads were collected in May and November 2004, and primers ITS1 and ITS4 for the ITS (White et al. 1990). January 2005 and August 2006 in Itapuã Park, South of Mitochondrial cytochrome b gene amplification was
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