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Draft Genome Analysis of Trichosporonales Species That Contribute to the Taxonomy of the Genus Trichosporon and Related Taxa

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Draft Genome Analysis of Trichosporonales Species That Contribute to the Taxonomy of the Genus Trichosporon and Related Taxa Med. Mycol. J. Vol.Med. 60, Mycol.51-57, 2019 J. Vol. 60 (No. 2) , 2019 51 ISSN 2185-6486 Review Draft Genome Analysis of Trichosporonales Species That Contribute to the Taxonomy of the Genus Trichosporon and Related Taxa Masako Takashima1 and Takashi Sugita2 1 Japan Collection of Microorganisms, RIKEN BioResource Research Center 2 Department of Microbiology, Meiji Pharmaceutical University ABSTRACT Many nomenclatural changes, including proposals of new taxa, have been carried out in fungi to adapt to the “One fungus = One name” (1F = 1N) principle. In yeasts, while some changes have been made in response to 1F = 1N, most have resulted from two other factors: i) an improved understanding of biological diversity due to an increase in number of known species, and ii) progress in the methods for analyzing and evaluating biological diversity. The method for constructing a backbone tree, which is a basal tree used to infer phylogeny, has also progressed from single-gene trees to multi-locus trees and further, to genome trees. This paper describes recent advances related to the contribution of genomic data to taxonomy, using the order Trichosporonales as an example. Key words : backbone tree, classification, identification, Trichosporon, Trichosporonales (formerly Trichosporon vanderwaltii)andHaglerozyma Introduction (formerly Trichosporon chiarellii). Cryptococcus curvatus and C. humicola were transferred to Cutaneotrichosporon and In The Yeasts, A Taxonomic Study, 5 th ed., which was Vanrija, respectively. According to the classification proposed published in 2011, the genus Trichosporon (Trichosporonales, by Lui et al. (2015), species formerly identified as Basidiomycota) included 37 species1). Some species of the Trichosporon belonged to one family, the Trichosporonaceae. highly polyphyletic genus Cryptococcus (10 of 70 species Sugita et al.3) summarized this reclassification, focusing on listed in The Yeasts, A Taxonomic Study, 5 th ed.) were found medically important yeast species. among Trichosporon species upon construction of a phy- In the light of the recent advances in sequencing techniques, logenetic tree. The clinically important species, Cryptococcus namely, next-generation sequencing, the importance of correct curvatus (present name, Cutaneotrichosporon curvatum)and classification has increased greatly because it represents the Cryptococcus humicola (present name, Vanrija humicola), foundation for the correct assignment of taxa for which were two of these. genomic information becomes available. Accordingly, a In 2015, Liu et al.2) reclassified species assigned to the robust backbone tree and the identification of phenotypic traits genus Trichosporon, resulting in an increase from 37 to 45. In that can be used to distinguish taxa are required to build a their paper, species formerly assigned to the genus Trichos- taxonomic system that takes full advantage of genomic data. poron were divided into five genera, Apiotrichum (21 species), In this paper, we introduce the contributions of genomic data Cutaneotrichosporon (10 species), Effuseotrichosporon (1 to taxonomy, using our data from the Trichosporonales as an species), Haglerozyma (1 species), and Trichosporon (12 example. species). Most of the species formerly assigned to Trichospo- Single-gene tree, multigene tree, and draft genome ron were reclassified into three genera, Apiotrichum, Cutaneo- tree trichosporon,andTrichosporon, while two species were each assigned to the monotypic genera, Effuseotrichosporon Most Trichosporonales species can be identified using one Address for correspondence: Masako Takashima Japan Collection of Microorganisms, RIKEN BioResource Research Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan Received: 21, January 2019, Accepted: 21, February 2019 E-mail: [email protected] 52 Medical Mycology Journal Volume 60, Number 2, 2019 Fig. 1. Phylogenetic tree of Trichosporon and related taxa based on the D1/D2 domain of LSU rRNA gene. The tree was constructed using the maximum likelihood method based on the Tamura-Nei model5). All positions with less than 90% site coverage were eliminated, i.e., fewer than 10% alignment gaps, missing data, and ambiguous bases were allowed at any position. There were a total of 594 positions in the final dataset. Numerals on each node represent the percentages from 100 replicating bootstrap samplings (frequencies of less than 50% are not shown)6). Evolutionary analyses were conducted in MEGA77). The numerals represent the percentages from 100 replicate bootstrap samplings (frequencies of less than 50% are not shown). Sequences were retrieved from the DDBJ/GenBank/EMBL databases under the indicated accession numbers. or a combination of the sequences of the D1/D2 domain of the Table 1. In addition, some species, such as C. curvatus, could LSU rRNA gene (hereafter, D1/D2) and the internal not be positioned with confidence in phylogenetic trees using transcribed spacer (ITS) region (Fig. 1)1, 4). However, these regions, as in our previous studies8, 9). delineation based on the D1/D2 and ITS region is sometimes Liu et al.10) used seven genes to construct a backbone tree of not possible in the case of closely related species, as shown in tremellomycetous yeasts. Construction of backbone trees Med. Mycol. J. Vol. 60 (No. 2) , 2019 53 Table 1. Pairs of species that cannot be differentiated with a simple combination of sequences of the D1/D2 domain of LSU rRNA and the ITS region* Base differences in Recommended method for differentiation D1/D2 domain ITS region Trichosporon asahii, T. coremiiforme, 1–2 1–2 Sequencing of IGS region** (> 10% divergence) and T. faecale Trichosporon caseorum and T. lactis 2 1 Assimilation tests with melezitose and ribitol Apiotrichum domesticum and 2 0 Sequencing of IGS region** (> 5% divergence) A. montevideense *, Data from Sugita1) **, Intergenic spacer region Table 2. Internode certainty (IC) for three genera, Apiotrichum, Cutaneotrichosporon,andTrichosporon, in the genome tree Clade Number of species used IC Apiotrichum 8(A. brassicae, A. domesticum gamsii, A. gracile, A. laibachii, 0.619 A. montevideense, A. porosum, A. veenhuisii) Cutaneotrichosporon clade for whole Cutaneotrichosporon 8(C. arboriforme, C. curvatum, C. cutaneum, C. cyanovorans, 0.552 species including C. curvatum C. daszewskae, C. dermatis, C. mucoides, C. oleaginosus) clade for formerly identified as 5(C. arboriforme, C. cutaneum, C. dermatis, C. mucoides, 0.804 Trichosporon + C. arboriforme C. oleaginosus) Trichosporon 5(T. asahii, T. coremiiforme, T. faecale, T. inkin, T. ovoides) 0.982 Data from Takashima et al.15) *, Cutaneotrichosporon guehoae is not included in this table as it did not cluster with Cutaneotrichosporon species. based on the concatenation of six to seven genes (combining such as phosphatidylinositol 3-kinase TOR1 and glutamate partial rRNA gene sequences and protein-coding genes) has synthase (NADH), provided good resolution even when used been frequently used in the classification of fungi, including alone13). yeasts11, 12). Such trees generally exhibit better resolution than Further analysis was performed using 30 species (27 single-gene trees, but unfortunately show insufficient resolu- Trichosporonales species and 3 Tremellales species as an tion at some nodes. For example, the phylogenetic position of outgroup)15). The strains added were the type strains of several C. curvatus remained unstable in the seven-gene tree, leading species for which the phylogenetic position had not yet been the authors to treat C. curvatus as a clade of its own. We clarified, in particular those at the base of the published extracted the same regions of the RPB1, RPB2, and TEF1-α phylogenetic trees1, 2, 4, 9). The genome tree showed good genes from genomic data and constructed a phylogenetic tree resolution, with 100% bootstrap support for all branches, with other Trichosporonales species. The position of C. evidence that the topology is not affected by the sampling curvatus was not clarified13) in this three-gene tree, indicating error associated with smaller sequences. Internode certainty that the concatenation of these three genes is insufficient to was analyzed using Randomized Axelerated Maximum resolve its phylogenetic position. Likelihood (RAxML)16), which showed that the tree, for the Following the guidelines of Rokas et al.14), we determined most part, is well-supported by the majority of ortholog the draft genomes of 15 Trichosporonales species, extracted groups15) (The internode certainty of clades of the genera 30 protein-coding DNA sequences from the genomic data, and Apiotrichum, Cutaneotrichosporon,andTrichosporon are generated a phylogenetic tree based on a concatenated shown in Table 2). Notably, although Trichosporon guehoae alignment of 30 orthologous genes13). Trees inferred from was transferred to Cutaneotrichosporon by Liu et al.2),itdid concatenated alignments based on 72,531 nucleotide and 24, not cluster with other Cutaneotrichosporon species in the 173 amino acid sequences showed the same topology. C. genome tree. Middelhoven et al.17) described C. guehoae as T. curvatus formed a clade with C. cutaneum and C. dermatis guehoae and positioned it between Trichosporon loubieri (100% bootstrap support in both trees, based on nucleotides (present name, Apiotrichum loubieri)andTrichosporon and amino acids). In addition, we found that several genes, asahii, although this arrangement lacked bootstrap support. In 54 Medical Mycology Journal Volume 60, Number 2, 2019 Table 3. The
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