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Limtongia gen. nov. for Zygozyma smithiae (Lipomycetaceae)

Limtongia gen. nov. for Zygozyma smithiae (Lipomycetaceae) Ann Microbiol (2011) 61:689–693 DOI 10.1007/s13213-010-0182-5 SHORT COMMUNICATION Sasitorn Jindamorakot & Somjit Am-in & Pattaraporn Yukphan & Yuzo Yamada Received: 8 November 2010 /Accepted: 3 December 2010 /Published online: 11 January 2011 Springer-Verlag and the University of Milan 2011 Abstract Teleomorphic species of the genus Zygozyma Introduction and anamorphic species of the genus Myxozyma were examined phylogenetically. In phylogenetic trees based on The genus Zygozyma van der Walt et von Arx was 18S rRNA-, 26S rRNA-, mitochondrial small subunit introduced with a single species, Zygozyma oligophaga rRNA- and EF-1α-gene sequences and concatenated van der Walt et von Arx (van der Walt et al. 1987). sequences of the latter four regions, derived from the Subsequently, the following three species were described: neighbor-joining method, the four species of the genus Zygozyma arxii van der Walt, Smith et Yamada (van der Zygozyma constituted four clusters, respectively, with low Walt et al. 1989), Zygozyma suomiensis Smith, van der bootstrap values, indicating that all four species can be Walt et Yamada (Smith et al. 1989) and Zygozyma smithiae distinguished from one another at the generic level. The van der Walt, Wingfield et Yamada (van der Walt et al. name of Limtongia was newly suggested for Zygozyma 1990). In total, four species have been proposed in the smithiae,and Limtongia smithiae wasproposedasnew Lipomycetaceous yeasts. combination. The genus Zygozyma was characterized morphologically by producing allantoid to cymbiform ascospores, and . . Keywords Lipomycetaceous yeast Limtongia gen. nov. physiologically by producing extracellular amyloid material . . Limtongia smithiae comb. nov. Phylogeny (Smith 1998b; van der Walt et al. 1987). Yamada and Zygozyma smithiae Nogawa (1990, 1995a) had already determined the partial sequences of 18S and 26S rRNAs of Lipomycetaceous yeasts, and found that Zygozyma oligophaga holds a unique : : : S. Jindamorakot S. Am-in P. Yukphan Y. Yamada (*) phylogenetic position in three regions of determined se- BIOTEC Culture Collection, quence within the 18S and 26S rRNAs. The results obtained National Center for Genetic Engineering and Biotechnology, suggested that the genus Zygozyma should be restricted to National Science and Technology Development Agency, 113 Thailand Science Park, Phaholyothin Road, only the species Zygozyma oligophaga, the type species of Klong 1, Klong Luang, the genus Zygozyma, and the remaining three species of the Pathumthani 12120, Thailand genus should be divided into two or more taxa. e-mail: yamada333@kch.biglobe.ne.jp This paper proposes Limtongia as a new genus for Y. Yamada Zygozyma smithiae, with the new combination of Limtongia JICA Senior Overseas Volunteer, smithiae by use of phylogenetic, genetic, chemotaxonomic Japan International Cooperation Agency, and phenotypic data. Shibuya-ku, Tokyo 151-8558, Japan Y. Yamada Materials and methods Professor Emeritus, Shizuoka University, All the sequence data used in this study were cited in Suruga-ku, Shizuoka 422-8529, Japan Kurtzman and Robnett (2003) and Kurtzman et al. (2007, 690 Ann Microbiol (2011) 61:689–693 Fig. 1 a–e Phylogenetic relationships of Zygozyma species. The 2008). The base sequences of 18S rRNA genes, 26S rRNA phylogenetic trees are based on 18S rRNA gene sequences of 1,622 genes, EF-1α genes and mitochondrial small subunit rRNA bases (a), 26S rRNA gene sequences of 3,013 bases (b), mitochon- drial small subunit rRNA gene sequences of 147 bases (c), EF-1α genes obtained were aligned either in pairs or as a group. gene sequences of 654 bases (d), and concatenated sequences of 18S Multiple alignments were performed with the program rRNA-, 26S rRNA-, EF-1α- and mitochondrial small subunit rRNA- Clustal X (version 1.8, Thompson et al. 1997). Alignment genes of 5,436 bases (e), and were constructed by the neighbor-joining gaps and unidentified bases were eliminated. Distance method. Numerals at nodes indicate bootstrap values (%) derived from 1,000 replications matrices for the aligned sequences were calculated by the two-parameter method of Kimura (1980). Phyloge- netic trees were constructed by the neighbor-joining Zygozyma oligophaga was connected to the cluster with a method (Saitou and Nei 1987). The robustness of bootstrap value of 83%. However, the phylogenetic branch individual branches was estimated by bootstrapping with of Zygozyma oligophaga was quite far from the type strain 1,000 replications (Felsenstein 1985)using theprogram of Zygozyma suomiensis. The type strains of Zygozyma MEGA (version 4.0, Tamura et al. 2007). Thetypestrains arxii and Zygozyma smithiae were connected to each other of Saccharomyces cerevisiae, Kluyveromyces polysporus with a bootstrap value of 69%. The results obtained suggest (= Vanderwaltozyma polysporus), Kuraishia capsulata that Zygozyma suomiensis is phylogenetically independent and Citeromyces matritensis were used as outgroups. from Zygozyma oligophaga as well as Zygozyma arxii and Zygozyma smithiae. In the phylogenetic tree based on mitochondrial small Result and discussion subunit rRNA gene sequences (Fig. 1c), the type strains of Zygozyma suomiensis, Zygozyma arxii, Zygozyma smithiae Phylogenetic trees of Zygozyma and Myxozyma species and Zygozyma oligophaga constituted their respective based on 18S rRNA-, 26S rRNA-, mitochondrial small clusters with quite low bootstrap values of 16, 20, 48, subunit rRNA- and EF-1α-gene sequences, as well as 47% and so on. The phylogenetic branches among the concatenated sequences of the latter four regions, were resulting clusters of the respective Zygozyma species were constructed by the neighbor-joining method (Fig. 1). almost similar in length to that between the type strains of In the phylogenetic tree based on 18S rRNA gene Kuraishia capsulata and Citeromyces matritensis,and sequences (Fig. 1a), the type strain of Zygozyma suomiensis much longer than that between the type strains of (Q-8) and the type strains of some Myxozyma species Saccharomyces cerevisiae and Kluyveromyces polysporus. constituted a small cluster with a bootstrap value of 100%. In the phylogenetic tree based on EF-1α gene sequences On the other hand, the type strain of Zygozyma smithiae (Fig. 1d), the type strains of the four Zygozyma species (Q-9) was connected to the type strains of the Myxozyma constituted their respective clusters independently, with species with a bootstrap value of 48%, and the resulting calculated bootstrap values of 10, 18 and 100%. cluster was then connected to the type strain of Zygozyma In the phylogenetic tree based on the concatenated arxii (Q-9; = Kawasakia arxii) with a bootstrap value of sequences of 18S rRNA genes, 26S rRNA genes, the EF- 52%. Between the cluster containing Zygozyma suomien- 1α genes and mitochondrial small subunit rRNA genes sis and the clusters containing Zygozyma smithiae and (Fig. 1e), the type strains of Zygozyma oligophaga and Zygozyma arxii, the calculated bootstrap value was 59%. Zygozyma suomiensis were connected with a bootstrap The type strain of Zygozyma oligophaga (Q-8), the type value of 57%. The type strains of Zygozyma arxii and species of the genus Zygozyma, was located on outermost Zygozyma smithiae were connected to each other with a branch of the phylogenetic tree. The calculated bootstrap bootstrap value of 60%. values were 100 and 59%. The phylogenetic branches among In all the five kinds of phylogenetic trees constructed, it the resulting clusters of the respective Zygozyma species were is obvious that the four species of the genus Zygozyma were almost similar in length to that between the type strains of phylogenetically independent from one another and Zygo- Kuraishia capsulata and Citeromyces matritensis, and much zyma smithiae was distinguished phylogenetically from the longer than that between the type strains of Saccharomyces remaining three species of the genus Zygozyma. cerevisiae and Kluyveromyces polysporus (= Vanderwalto- Kurtzman et al. (2007) constructed a phylogenetic tree zyma polysporus). The results obtained suggest that all four based on the concatenated sequences from the nearly Zygozyma species can be distinguished from one another entire 18S rRNA, 26S rRNA, mitochondrial small subunit phylogenetically at the generic level. rRNA and the EF-1α genes and showed that the family In the phylogenetic tree based on 26S rRNA gene Lipomycetaceae, including the genera Lipomyces, Dipo- sequences (Fig. 1b), the type strain of Zygozyma suomiensis dascopsis, Zygozyma and Babjevia, has a monophyletic and the type strains of Myxozyma species constituted a lineage since the bootstrap value of 100% was calculated cluster with a bootstrap value of 100%. The type strain of between the cluster including Babjevia anomala and Ann Microbiol (2011) 61:689–693 691 Zygozyma suomiensis NRRL Y-17356 (DQ519000) Myxozyma sirexii NRRL- Y-27626 (DQ519025) 38 ab 70 T 80 Myxozyma sirexii NRRL- Y-27626 (DQ518994) Zygozyma suomiensi s NRRL Y-17356 (DQ519031) 49 T Myxozyyma geophila NRRL Y-17252 (DQ518985) Myxozyma melibiosi NRRL Y-11781 (DQ519019) 36 Myxozyma melibiosi NRRL Y-11781 (DQ518988) Myxozyyma geophila NRRL Y-17252 (DQ519016) Myxozyma neotropica NRRL Y-17859 (DQ518992) Myxozyma mucilagina NRRL Y-11823 (DQ519021) 100 99 57 Myxozyyma vanderwaltii NRRL Y-17727 (DQ518996) Myxozyma neglecta NRRL Y-27508 (DQ519022) Myxozyma mucilagina NRRL Y-11823 (DQ518990) 75 Myxozyma neotropica NRRL Y-17859 (DQ519023) 83 44 Myxozyma neglecta NRRL Y-27508 (DQ518991) Myxozyyma vanderwaltii NRRL Y-17727 (DQ519027) Myxozyma monticola NRRL Y-17726 (DQ518989) Myxozyma lipomycoides NRRL Y-17253 (DQ519018) 100 84 Zygozyma oligophaga NRRL Y-17247 (DQ518998) Myxozyma nipponensis NRRL Y-27625 (DQ519024) 59 Zygozyma arxii NRRL Y-17921 (DQ519028) Myxozyma lipomycoides NRRL Y-17253 (DQ518987) 31 93 T A Myxozyma nipponensis NRRL Y-27625 (DQ518993) Zygozyma smithiae NRRL Y-17922 (DQ519030) Myxozyma kluyveri NRRL Y-17277 (DQ519017) Myxozyma kluyveri NRRL Y-17277 (DQ518986) T T 85 Myxozyma udenii NRRL Y-17387 (DQ518995) Myxozyma udenii NRRL Y-17387 (DQ519026) Myxozyma monticola NRRL Y-17726 (DQ519020) Zygozyma arxii NRRL Y-17921 (DQ518997) T T 69 Zygozyma smithiae NRRL Y-17922 (DQ518999) Zygozyma oligophaga NRRL Y-17247 (DQ519029) Citeromyces matritensis NRRL Y-2407 (EF550484) Citeromyces matritensis NRRL Y-2407 (EF550346) 73 93 T T Kuraishia capsulata NRRL Y-1842 (EF550408) Kuraishia capsulata NRRL Y-1842 (EU011585) T T Kluyveromyces polysporus NRRL Y-8283 (AY046249) Kluyveromyces polysporus NRRL Y-8283 (AY048169) NT NT 100 100 Saccharomyces cerevisiae NRRL Y-12632 (Z75578) Saccharomyces cerevisiae NRRL Y-12632 (AY048154) nuc Knuc 0.01 0.01 cd Myxozyma mucilagina NRRL Y-11823 (DQ496139) Myxozyma mucilagina NRRL Y-11823 (DQ496161) 98 A 52 71 Myxozyma neglecta NRRL Y-27508 (DQ496140) Myxozyma neglecta NRRL Y-27508 (DQ496160) 59 T 76 T Myxozyyma vanderwaltii NRRL Y-17727 (DQ496138) Myxozyyma vanderwaltii NRRL Y-17727 (DQ496164) Myxozyma neotropica NRRL Y-17859 (DQ496137) 56 Myxozyma neotropica NRRL Y-17859 (DQ496165) Zygozyma suomiensis NRRL Y-17356 (DQ496120) Myxozyma sirexii NRRL- Y-27626 (DQ496169) Myxozyma melibiosi NRRL Y-11781 (DQ496143) 91 Zygozyma suomiensis NRRL Y-17356 (DQ496174) Myxozyma sirexii NRRL- -27626 (DQ496141) Myxozyyma geophila NRRL Y-17252 (DQ496162) T 28 Myxozyyma geophila NRRL Y-17252 (DQ496142) Myxozyma kluyveri NRRL Y-17277 (DQ496159) Myxozyma kluyveri NRRL Y-17277 (DQ496124) Myxozyma udenii NRRL Y-17387 (DQ496167) T 42 48 Myxozyma udenii NRRL Y-17387 (DQ496125) Zygozyma arxii NRRL Y-17921 (DQ496173) Myxozyma nipponensis NRRL Y-27625 (DQ496146) Myxozyma monticola NRRL Y-17726 (DQ496166) T 20 Zygozyma smithiae NRRL Y-17922 (DQ496119) 47 53 Zygozyma smithiae NRRL Y-17922 (DQ496172) Myxozyma lipomycoides NRRL Y-17253 (DQ496145) Myxozyma melibiosi NRRL Y-11781 (DQ496163) 53 Zygozyma oligophaga NRRL Y-17247 (DQ496118) Myxozyma lipomycoides NRRL Y-17253 (DQ496168) 10 Myxozyma monticola NRRL Y-17726 (DQ496144) Myxozyma nipponensis NRRL Y-27625 (DQ496170) T 22 Zygozyma arxii NRRL Y-17921 (DQ496117) Zygozyma oligophaga NRRL Y-17247 (DQ496171) Kuraishia capsulata NRRL Y-1842 (EU014694) Citeromyces matritensis NRRL Y-2407 (EF547718) Citeromyces matritensis NRRL Y-2407 (EU057544) Kuraishia capsulata NRRL Y-1842 (EU018489) Kluyveromyces polysporus NRRL Y-8283 (AF402047) Kluyveromyces polysporus NRRL Y-8283 (AF442315) 63 NT NT 100 Saccharomyces cerevisiae NRRL Y-12632 (AF402004) 96 Saccharomyces cerevisiae NRRL Y-12632 (AF442281) Knuc nuc 0.02 0.05 Myxozyma mucilagina NRRL Y-11823 e 100 Myxozyma neglecta NRRL Y-27508 100 T Myxozyyma vanderwaltii NRRL Y-17727 Myxozyma neotropica NRRL Y-17859 Myxozyma sirexii NRRL-Y-27626 Zygozyma suomiensis NRRL Y-17356 Myxozyyma geophila NRRL Y-17252 Myxozyma melibiosi NRRL Y-11781 Myxozyma monticola NRRL Y-17726 48 T Zygozyma oligophaga NRRL Y-17247 Myxozyma kluyveri NRRL Y-17277 Myxozyma udenii NRRL Y-17387 93 Zygozyma arxii NRRL Y-17921 Zygozyma smithiae NRRL Y-17922 Myxozyma lipomycoides NRRL Y-17253 Myxozyma nipponensis NRRL Y-27625 Citeromyces matritensis NRRL Y-2407 Kuraishia capsulata NRRL Y-1842 Kluyveromyces polysporus NRRL Y-8283 NT Saccharomyces cerevisiae NRRL Y-12632 nuc 0.01 692 Ann Microbiol (2011) 61:689–693 Dipodascopsis tothii and the cluster including Dipodas- Genetically, the range of DNA G+C content of the genus copsis uninucleata and Lipomyces and Zygozyma species. Zygozyma was 14.0 mol% from 41.7 to 55.7 mol% for the On the basis of these findings, the family Lipomycetaceae only four species, and Zygozyma smithiae is unique, which was monophyletic, and thus the genus Zygozyma was was 55.7 mol% G+C in the type strain and much higher transferred to the genus Lipomyces to construct the genus than those (41.7–47.4 mol% G+C) of the type strains of the Lipomyces Lodder et Kreger van-Rij emend. Kurtzman et remaining three species (Smith 1998b). Chemotaxonomi- al. However, the emended genus Lipomyces was in fact cally, Zygozyma smithiae is characterized by Q-9, which not monophyletic but polyphyletic, since the calculated was able to discriminate the species from the Q-8-equipped bootstrap values at the branching points in the phyloge- species, Zygozyma oligophaga and Zygozyma suomiensis. netic tree were quite low within the emended genus. For Morphologically, the Q-9-equipped Zygozyma smithiae is example, the type strain of Zygozyma arxii (= Kawasakia able to be discriminated from the Q-9-equipped Zygozyma arxii) showed an independent cluster, and the calculated arxii by the presence of plasmodesmal cannals in cells (van bootstrap value at the branching point was quite low, since der Walt et al. 1991). These genetic, chemotaxonomic and there was no indication of any numeral for the bootstrap morphological characteristics are enough to distinguish value, and the type strain of Zygozyma smithiae was quite Zygozyma smithiae at the generic level, and the species distant phylogenetically from the type strain of Zygozyma can appropriately be classified in a separate new genus. The arxii. These facts suggested that the taxonomic subdivi- name of the genus is Limtongia gen. nov. sion of the emended genus would be possible from the phylogenic point of view. The teleomorphic genus Lipomyces Lodder et Kreger-van Limtongia Jindamorakot, Am-in, Yukphan et Yamada Rij emend. Kurtzman et al. has an extremely wide range of gen. nov. DNA base composition. The calculated DNA G+C contents of the emended genus were estimated to be from 41.5 Genus ad Lipomycetaceae pertinens. Cellulae incapsulatae, to 55.7 mol%, with a range of 14.2 mol% (Smith globosae, ellipsoideae vel ovoideae, singularae vel binae, 1998a, b). AccordingtoNakase and Komagata (1970), gemmantes multilateraliter. Asci non juncti, affixi, glo- such an emended genus that is genetically diverse has a bosi, allantoideae amoeboidei, multispori, evanescentes, heterogeneous nature taxonomically. Chemotaxonomi- oriundi intercalaritaer vel terminariter per transformatio- cally, the emended genus has three kinds of isoprenoid nem directas cellularum singularum vegetativarum aggre- quinone homologs (Smith 1998a, b;Yamada 1986; gatarum. Ascosporae allantoideae vel cymbiformes, Yamada et al. 1986), suggesting that the emended genus glabrae, succinae, conglutinantes ubi liberatae. Fermentatio is also taxonomically heterogeneous, as found in the genus abest. D-Glucosum, D-xylosum, D-xylitolum, glycerolum, Pichia Hansen emend. Kurtzman (Kurtzman 1984; acidum 2-keto-D-gluconicum, acidum 5-keto-D-gluconicum Yamada and Kondo 1972; Yamada et al. 1973). These et sucrosum assimilantur. D-Galactosum, L-sorbosum, genetic and chemotaxonomic data indicated that the D-arabinosum, L-arabinosum, D-mannitolum, D-sorbitolum, emended genus Lipomyces is subject to be divided into L-arabitolum, D-ribitolum, maltosum, lactosum, melibiosum, several genera that have smaller generic circumscriptions, trehalosum et raffinosum non assimilantur. Nitras kali non as already performed in the genus Pichia Hansen emend. assimilatur. Systema coenzymatis Q-9 adest. Proportio Kurtzman (Billon-Grand 1989; Kurtzman and Suzuki guanini+cytosini deoxiribonucleati 55.3–55.7 mol%. 2010; Kurtzman et al. 2008). Species typica: Limtongia smithiae (van der Walt, Upon subdivision of the genus Lipomyces Lodder et Wingfield et Yamada) Jindamorakot, Am-in, Yukphan et Kreger-van Rij emend. Kurtzman et al., the genera Yamada comb. nov. Waltomyces Yamada et Nakase (Yamada and Nakase Genus belongs to Lipomycetaceae. Cells are encap- 1985), Babjevia van der Walt et Smith (Smith et al. sulated, globose, ellipsoid or ovoid, occurring singly or 1995), Smithiozyma van der Walt, Kock et Yamada (Kock in pairs, budding multilaterally. Asci are unconjugated, et al. 1995) and Kawasakia Yamada et Nogawa (Yamada attached, globose, allantoid or amoeboid, multispored, and Nogawa 1995b)—all names that were not accepted by evanescent, arising by direct transformation of single Kurtzman et al. (2007)—should be retained. And additional vegetative cells aggregated. Ascospores are allantoid to new genera can be proposed. cymbiform, glabrous, amber-coloured and conjugated when The four species of the genus Zygozyma that were proved liberated. Fermentation is absent. D-Glucose, D-xylose, D- to have long phylogenetic distances and low bootstrap values xylitol, glycerol, 2-keto-D-gluconic acid, 5-keto-D-gluconic at the branching points, respectively, in the phylogenetic acid and sucrosum are assimilated. D-Galactose, L-sorbose, trees are enough to constitute respective genera, as suggested D-arabinose, L-arabinose, D-mannitol, D-sorbitol, L-arabitol, previously (Yamada and Nogawa 1995a)(Fig. 1). D-ribitol, maltose, lactose, melibiose, trehalose and raffinose Ann Microbiol (2011) 61:689–693 693 Smith MTh (1998a) Lipomyces Lodder & Kreger-van Rij. In: are not assimilated. Potassium nitrate is not assimilated. Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study, 4th Coenzyme Q-9 system is present. Guanine+cytosine con- edn. Elsevier, Amsterdam, pp 248–253 tents of DNA are 55.3–55.7 mol%. Smith MTh (1998b) Zygozyma van der Walt & von Arx. In: Kurtzman Type species: Limtongia smithiae (van der Walt, CP, Fell JW (eds) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 433–436 Wingfield et Yamada) Jindamorakot, Am-in, Yukphan et Smith MTh, van der Walt JP, Yamada Y, Batenburg-van der Vegte WH Yamada comb. nov. (1989) Zygozyma suomiensis sp. nov. (Lipomycetaceae), a new Basionym: Zygozyma smithiae van der Walt, Wingfield species from Finland. Antonie van Leeuwenhoek 56:283–288 et Yamada, Antonie van Leeuwenhoek 58: 96, 1990. Smith MTh, van der Walt JP, Batenburg-van der Vegte WH (1995) Babjevia gen. nov. - a new genus of the Lipomycetaceae. 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Bull Fac Agric Shizuoka Univ 45:31–34 ces gen. nov. FEMS Yeast Res 8:939–954 Yamada Y, Okada T, Ueshima O, Kondo K (1973) Coenzyme Q Nakase T, Komagata K (1970) Significance of DNA base composition system in the classification of the ascosporogenous yeast genera in the classification of the yeast genus Pichia. J Gen Appl Hansenula and Pichia. J Gen Appl Microbiol 19:189–208 Microbiol 16:511–521 Yamada Y, Nakase T, van der Walt JP (1986) The coenzyme Q system Saitou N, Nei M (1987) The neighbor-joining method: a new in strains of species in ascosporogenous yeast genera Lipomyces method for reconstructing phylogenetic trees. Mol Biol Evol and Waltomyces. Trans Mycol Soc Japan 27:313–319 4:406–425 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Microbiology Springer Journals

Limtongia gen. nov. for Zygozyma smithiae (Lipomycetaceae)

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Springer Journals
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Copyright © 2011 by Springer-Verlag and the University of Milan
Subject
Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
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1590-4261
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1869-2044
DOI
10.1007/s13213-010-0182-5
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Abstract

Ann Microbiol (2011) 61:689–693 DOI 10.1007/s13213-010-0182-5 SHORT COMMUNICATION Sasitorn Jindamorakot & Somjit Am-in & Pattaraporn Yukphan & Yuzo Yamada Received: 8 November 2010 /Accepted: 3 December 2010 /Published online: 11 January 2011 Springer-Verlag and the University of Milan 2011 Abstract Teleomorphic species of the genus Zygozyma Introduction and anamorphic species of the genus Myxozyma were examined phylogenetically. In phylogenetic trees based on The genus Zygozyma van der Walt et von Arx was 18S rRNA-, 26S rRNA-, mitochondrial small subunit introduced with a single species, Zygozyma oligophaga rRNA- and EF-1α-gene sequences and concatenated van der Walt et von Arx (van der Walt et al. 1987). sequences of the latter four regions, derived from the Subsequently, the following three species were described: neighbor-joining method, the four species of the genus Zygozyma arxii van der Walt, Smith et Yamada (van der Zygozyma constituted four clusters, respectively, with low Walt et al. 1989), Zygozyma suomiensis Smith, van der bootstrap values, indicating that all four species can be Walt et Yamada (Smith et al. 1989) and Zygozyma smithiae distinguished from one another at the generic level. The van der Walt, Wingfield et Yamada (van der Walt et al. name of Limtongia was newly suggested for Zygozyma 1990). In total, four species have been proposed in the smithiae,and Limtongia smithiae wasproposedasnew Lipomycetaceous yeasts. combination. The genus Zygozyma was characterized morphologically by producing allantoid to cymbiform ascospores, and . . Keywords Lipomycetaceous yeast Limtongia gen. nov. physiologically by producing extracellular amyloid material . . Limtongia smithiae comb. nov. Phylogeny (Smith 1998b; van der Walt et al. 1987). Yamada and Zygozyma smithiae Nogawa (1990, 1995a) had already determined the partial sequences of 18S and 26S rRNAs of Lipomycetaceous yeasts, and found that Zygozyma oligophaga holds a unique : : : S. Jindamorakot S. Am-in P. Yukphan Y. Yamada (*) phylogenetic position in three regions of determined se- BIOTEC Culture Collection, quence within the 18S and 26S rRNAs. The results obtained National Center for Genetic Engineering and Biotechnology, suggested that the genus Zygozyma should be restricted to National Science and Technology Development Agency, 113 Thailand Science Park, Phaholyothin Road, only the species Zygozyma oligophaga, the type species of Klong 1, Klong Luang, the genus Zygozyma, and the remaining three species of the Pathumthani 12120, Thailand genus should be divided into two or more taxa. e-mail: yamada333@kch.biglobe.ne.jp This paper proposes Limtongia as a new genus for Y. Yamada Zygozyma smithiae, with the new combination of Limtongia JICA Senior Overseas Volunteer, smithiae by use of phylogenetic, genetic, chemotaxonomic Japan International Cooperation Agency, and phenotypic data. Shibuya-ku, Tokyo 151-8558, Japan Y. Yamada Materials and methods Professor Emeritus, Shizuoka University, All the sequence data used in this study were cited in Suruga-ku, Shizuoka 422-8529, Japan Kurtzman and Robnett (2003) and Kurtzman et al. (2007, 690 Ann Microbiol (2011) 61:689–693 Fig. 1 a–e Phylogenetic relationships of Zygozyma species. The 2008). The base sequences of 18S rRNA genes, 26S rRNA phylogenetic trees are based on 18S rRNA gene sequences of 1,622 genes, EF-1α genes and mitochondrial small subunit rRNA bases (a), 26S rRNA gene sequences of 3,013 bases (b), mitochon- drial small subunit rRNA gene sequences of 147 bases (c), EF-1α genes obtained were aligned either in pairs or as a group. gene sequences of 654 bases (d), and concatenated sequences of 18S Multiple alignments were performed with the program rRNA-, 26S rRNA-, EF-1α- and mitochondrial small subunit rRNA- Clustal X (version 1.8, Thompson et al. 1997). Alignment genes of 5,436 bases (e), and were constructed by the neighbor-joining gaps and unidentified bases were eliminated. Distance method. Numerals at nodes indicate bootstrap values (%) derived from 1,000 replications matrices for the aligned sequences were calculated by the two-parameter method of Kimura (1980). Phyloge- netic trees were constructed by the neighbor-joining Zygozyma oligophaga was connected to the cluster with a method (Saitou and Nei 1987). The robustness of bootstrap value of 83%. However, the phylogenetic branch individual branches was estimated by bootstrapping with of Zygozyma oligophaga was quite far from the type strain 1,000 replications (Felsenstein 1985)using theprogram of Zygozyma suomiensis. The type strains of Zygozyma MEGA (version 4.0, Tamura et al. 2007). Thetypestrains arxii and Zygozyma smithiae were connected to each other of Saccharomyces cerevisiae, Kluyveromyces polysporus with a bootstrap value of 69%. The results obtained suggest (= Vanderwaltozyma polysporus), Kuraishia capsulata that Zygozyma suomiensis is phylogenetically independent and Citeromyces matritensis were used as outgroups. from Zygozyma oligophaga as well as Zygozyma arxii and Zygozyma smithiae. In the phylogenetic tree based on mitochondrial small Result and discussion subunit rRNA gene sequences (Fig. 1c), the type strains of Zygozyma suomiensis, Zygozyma arxii, Zygozyma smithiae Phylogenetic trees of Zygozyma and Myxozyma species and Zygozyma oligophaga constituted their respective based on 18S rRNA-, 26S rRNA-, mitochondrial small clusters with quite low bootstrap values of 16, 20, 48, subunit rRNA- and EF-1α-gene sequences, as well as 47% and so on. The phylogenetic branches among the concatenated sequences of the latter four regions, were resulting clusters of the respective Zygozyma species were constructed by the neighbor-joining method (Fig. 1). almost similar in length to that between the type strains of In the phylogenetic tree based on 18S rRNA gene Kuraishia capsulata and Citeromyces matritensis,and sequences (Fig. 1a), the type strain of Zygozyma suomiensis much longer than that between the type strains of (Q-8) and the type strains of some Myxozyma species Saccharomyces cerevisiae and Kluyveromyces polysporus. constituted a small cluster with a bootstrap value of 100%. In the phylogenetic tree based on EF-1α gene sequences On the other hand, the type strain of Zygozyma smithiae (Fig. 1d), the type strains of the four Zygozyma species (Q-9) was connected to the type strains of the Myxozyma constituted their respective clusters independently, with species with a bootstrap value of 48%, and the resulting calculated bootstrap values of 10, 18 and 100%. cluster was then connected to the type strain of Zygozyma In the phylogenetic tree based on the concatenated arxii (Q-9; = Kawasakia arxii) with a bootstrap value of sequences of 18S rRNA genes, 26S rRNA genes, the EF- 52%. Between the cluster containing Zygozyma suomien- 1α genes and mitochondrial small subunit rRNA genes sis and the clusters containing Zygozyma smithiae and (Fig. 1e), the type strains of Zygozyma oligophaga and Zygozyma arxii, the calculated bootstrap value was 59%. Zygozyma suomiensis were connected with a bootstrap The type strain of Zygozyma oligophaga (Q-8), the type value of 57%. The type strains of Zygozyma arxii and species of the genus Zygozyma, was located on outermost Zygozyma smithiae were connected to each other with a branch of the phylogenetic tree. The calculated bootstrap bootstrap value of 60%. values were 100 and 59%. The phylogenetic branches among In all the five kinds of phylogenetic trees constructed, it the resulting clusters of the respective Zygozyma species were is obvious that the four species of the genus Zygozyma were almost similar in length to that between the type strains of phylogenetically independent from one another and Zygo- Kuraishia capsulata and Citeromyces matritensis, and much zyma smithiae was distinguished phylogenetically from the longer than that between the type strains of Saccharomyces remaining three species of the genus Zygozyma. cerevisiae and Kluyveromyces polysporus (= Vanderwalto- Kurtzman et al. (2007) constructed a phylogenetic tree zyma polysporus). The results obtained suggest that all four based on the concatenated sequences from the nearly Zygozyma species can be distinguished from one another entire 18S rRNA, 26S rRNA, mitochondrial small subunit phylogenetically at the generic level. rRNA and the EF-1α genes and showed that the family In the phylogenetic tree based on 26S rRNA gene Lipomycetaceae, including the genera Lipomyces, Dipo- sequences (Fig. 1b), the type strain of Zygozyma suomiensis dascopsis, Zygozyma and Babjevia, has a monophyletic and the type strains of Myxozyma species constituted a lineage since the bootstrap value of 100% was calculated cluster with a bootstrap value of 100%. The type strain of between the cluster including Babjevia anomala and Ann Microbiol (2011) 61:689–693 691 Zygozyma suomiensis NRRL Y-17356 (DQ519000) Myxozyma sirexii NRRL- Y-27626 (DQ519025) 38 ab 70 T 80 Myxozyma sirexii NRRL- Y-27626 (DQ518994) Zygozyma suomiensi s NRRL Y-17356 (DQ519031) 49 T Myxozyyma geophila NRRL Y-17252 (DQ518985) Myxozyma melibiosi NRRL Y-11781 (DQ519019) 36 Myxozyma melibiosi NRRL Y-11781 (DQ518988) Myxozyyma geophila NRRL Y-17252 (DQ519016) Myxozyma neotropica NRRL Y-17859 (DQ518992) Myxozyma mucilagina NRRL Y-11823 (DQ519021) 100 99 57 Myxozyyma vanderwaltii NRRL Y-17727 (DQ518996) Myxozyma neglecta NRRL Y-27508 (DQ519022) Myxozyma mucilagina NRRL Y-11823 (DQ518990) 75 Myxozyma neotropica NRRL Y-17859 (DQ519023) 83 44 Myxozyma neglecta NRRL Y-27508 (DQ518991) Myxozyyma vanderwaltii NRRL Y-17727 (DQ519027) Myxozyma monticola NRRL Y-17726 (DQ518989) Myxozyma lipomycoides NRRL Y-17253 (DQ519018) 100 84 Zygozyma oligophaga NRRL Y-17247 (DQ518998) Myxozyma nipponensis NRRL Y-27625 (DQ519024) 59 Zygozyma arxii NRRL Y-17921 (DQ519028) Myxozyma lipomycoides NRRL Y-17253 (DQ518987) 31 93 T A Myxozyma nipponensis NRRL Y-27625 (DQ518993) Zygozyma smithiae NRRL Y-17922 (DQ519030) Myxozyma kluyveri NRRL Y-17277 (DQ519017) Myxozyma kluyveri NRRL Y-17277 (DQ518986) T T 85 Myxozyma udenii NRRL Y-17387 (DQ518995) Myxozyma udenii NRRL Y-17387 (DQ519026) Myxozyma monticola NRRL Y-17726 (DQ519020) Zygozyma arxii NRRL Y-17921 (DQ518997) T T 69 Zygozyma smithiae NRRL Y-17922 (DQ518999) Zygozyma oligophaga NRRL Y-17247 (DQ519029) Citeromyces matritensis NRRL Y-2407 (EF550484) Citeromyces matritensis NRRL Y-2407 (EF550346) 73 93 T T Kuraishia capsulata NRRL Y-1842 (EF550408) Kuraishia capsulata NRRL Y-1842 (EU011585) T T Kluyveromyces polysporus NRRL Y-8283 (AY046249) Kluyveromyces polysporus NRRL Y-8283 (AY048169) NT NT 100 100 Saccharomyces cerevisiae NRRL Y-12632 (Z75578) Saccharomyces cerevisiae NRRL Y-12632 (AY048154) nuc Knuc 0.01 0.01 cd Myxozyma mucilagina NRRL Y-11823 (DQ496139) Myxozyma mucilagina NRRL Y-11823 (DQ496161) 98 A 52 71 Myxozyma neglecta NRRL Y-27508 (DQ496140) Myxozyma neglecta NRRL Y-27508 (DQ496160) 59 T 76 T Myxozyyma vanderwaltii NRRL Y-17727 (DQ496138) Myxozyyma vanderwaltii NRRL Y-17727 (DQ496164) Myxozyma neotropica NRRL Y-17859 (DQ496137) 56 Myxozyma neotropica NRRL Y-17859 (DQ496165) Zygozyma suomiensis NRRL Y-17356 (DQ496120) Myxozyma sirexii NRRL- Y-27626 (DQ496169) Myxozyma melibiosi NRRL Y-11781 (DQ496143) 91 Zygozyma suomiensis NRRL Y-17356 (DQ496174) Myxozyma sirexii NRRL- -27626 (DQ496141) Myxozyyma geophila NRRL Y-17252 (DQ496162) T 28 Myxozyyma geophila NRRL Y-17252 (DQ496142) Myxozyma kluyveri NRRL Y-17277 (DQ496159) Myxozyma kluyveri NRRL Y-17277 (DQ496124) Myxozyma udenii NRRL Y-17387 (DQ496167) T 42 48 Myxozyma udenii NRRL Y-17387 (DQ496125) Zygozyma arxii NRRL Y-17921 (DQ496173) Myxozyma nipponensis NRRL Y-27625 (DQ496146) Myxozyma monticola NRRL Y-17726 (DQ496166) T 20 Zygozyma smithiae NRRL Y-17922 (DQ496119) 47 53 Zygozyma smithiae NRRL Y-17922 (DQ496172) Myxozyma lipomycoides NRRL Y-17253 (DQ496145) Myxozyma melibiosi NRRL Y-11781 (DQ496163) 53 Zygozyma oligophaga NRRL Y-17247 (DQ496118) Myxozyma lipomycoides NRRL Y-17253 (DQ496168) 10 Myxozyma monticola NRRL Y-17726 (DQ496144) Myxozyma nipponensis NRRL Y-27625 (DQ496170) T 22 Zygozyma arxii NRRL Y-17921 (DQ496117) Zygozyma oligophaga NRRL Y-17247 (DQ496171) Kuraishia capsulata NRRL Y-1842 (EU014694) Citeromyces matritensis NRRL Y-2407 (EF547718) Citeromyces matritensis NRRL Y-2407 (EU057544) Kuraishia capsulata NRRL Y-1842 (EU018489) Kluyveromyces polysporus NRRL Y-8283 (AF402047) Kluyveromyces polysporus NRRL Y-8283 (AF442315) 63 NT NT 100 Saccharomyces cerevisiae NRRL Y-12632 (AF402004) 96 Saccharomyces cerevisiae NRRL Y-12632 (AF442281) Knuc nuc 0.02 0.05 Myxozyma mucilagina NRRL Y-11823 e 100 Myxozyma neglecta NRRL Y-27508 100 T Myxozyyma vanderwaltii NRRL Y-17727 Myxozyma neotropica NRRL Y-17859 Myxozyma sirexii NRRL-Y-27626 Zygozyma suomiensis NRRL Y-17356 Myxozyyma geophila NRRL Y-17252 Myxozyma melibiosi NRRL Y-11781 Myxozyma monticola NRRL Y-17726 48 T Zygozyma oligophaga NRRL Y-17247 Myxozyma kluyveri NRRL Y-17277 Myxozyma udenii NRRL Y-17387 93 Zygozyma arxii NRRL Y-17921 Zygozyma smithiae NRRL Y-17922 Myxozyma lipomycoides NRRL Y-17253 Myxozyma nipponensis NRRL Y-27625 Citeromyces matritensis NRRL Y-2407 Kuraishia capsulata NRRL Y-1842 Kluyveromyces polysporus NRRL Y-8283 NT Saccharomyces cerevisiae NRRL Y-12632 nuc 0.01 692 Ann Microbiol (2011) 61:689–693 Dipodascopsis tothii and the cluster including Dipodas- Genetically, the range of DNA G+C content of the genus copsis uninucleata and Lipomyces and Zygozyma species. Zygozyma was 14.0 mol% from 41.7 to 55.7 mol% for the On the basis of these findings, the family Lipomycetaceae only four species, and Zygozyma smithiae is unique, which was monophyletic, and thus the genus Zygozyma was was 55.7 mol% G+C in the type strain and much higher transferred to the genus Lipomyces to construct the genus than those (41.7–47.4 mol% G+C) of the type strains of the Lipomyces Lodder et Kreger van-Rij emend. Kurtzman et remaining three species (Smith 1998b). Chemotaxonomi- al. However, the emended genus Lipomyces was in fact cally, Zygozyma smithiae is characterized by Q-9, which not monophyletic but polyphyletic, since the calculated was able to discriminate the species from the Q-8-equipped bootstrap values at the branching points in the phyloge- species, Zygozyma oligophaga and Zygozyma suomiensis. netic tree were quite low within the emended genus. For Morphologically, the Q-9-equipped Zygozyma smithiae is example, the type strain of Zygozyma arxii (= Kawasakia able to be discriminated from the Q-9-equipped Zygozyma arxii) showed an independent cluster, and the calculated arxii by the presence of plasmodesmal cannals in cells (van bootstrap value at the branching point was quite low, since der Walt et al. 1991). These genetic, chemotaxonomic and there was no indication of any numeral for the bootstrap morphological characteristics are enough to distinguish value, and the type strain of Zygozyma smithiae was quite Zygozyma smithiae at the generic level, and the species distant phylogenetically from the type strain of Zygozyma can appropriately be classified in a separate new genus. The arxii. These facts suggested that the taxonomic subdivi- name of the genus is Limtongia gen. nov. sion of the emended genus would be possible from the phylogenic point of view. The teleomorphic genus Lipomyces Lodder et Kreger-van Limtongia Jindamorakot, Am-in, Yukphan et Yamada Rij emend. Kurtzman et al. has an extremely wide range of gen. nov. DNA base composition. The calculated DNA G+C contents of the emended genus were estimated to be from 41.5 Genus ad Lipomycetaceae pertinens. Cellulae incapsulatae, to 55.7 mol%, with a range of 14.2 mol% (Smith globosae, ellipsoideae vel ovoideae, singularae vel binae, 1998a, b). AccordingtoNakase and Komagata (1970), gemmantes multilateraliter. Asci non juncti, affixi, glo- such an emended genus that is genetically diverse has a bosi, allantoideae amoeboidei, multispori, evanescentes, heterogeneous nature taxonomically. Chemotaxonomi- oriundi intercalaritaer vel terminariter per transformatio- cally, the emended genus has three kinds of isoprenoid nem directas cellularum singularum vegetativarum aggre- quinone homologs (Smith 1998a, b;Yamada 1986; gatarum. Ascosporae allantoideae vel cymbiformes, Yamada et al. 1986), suggesting that the emended genus glabrae, succinae, conglutinantes ubi liberatae. Fermentatio is also taxonomically heterogeneous, as found in the genus abest. D-Glucosum, D-xylosum, D-xylitolum, glycerolum, Pichia Hansen emend. Kurtzman (Kurtzman 1984; acidum 2-keto-D-gluconicum, acidum 5-keto-D-gluconicum Yamada and Kondo 1972; Yamada et al. 1973). These et sucrosum assimilantur. D-Galactosum, L-sorbosum, genetic and chemotaxonomic data indicated that the D-arabinosum, L-arabinosum, D-mannitolum, D-sorbitolum, emended genus Lipomyces is subject to be divided into L-arabitolum, D-ribitolum, maltosum, lactosum, melibiosum, several genera that have smaller generic circumscriptions, trehalosum et raffinosum non assimilantur. Nitras kali non as already performed in the genus Pichia Hansen emend. assimilatur. Systema coenzymatis Q-9 adest. Proportio Kurtzman (Billon-Grand 1989; Kurtzman and Suzuki guanini+cytosini deoxiribonucleati 55.3–55.7 mol%. 2010; Kurtzman et al. 2008). Species typica: Limtongia smithiae (van der Walt, Upon subdivision of the genus Lipomyces Lodder et Wingfield et Yamada) Jindamorakot, Am-in, Yukphan et Kreger-van Rij emend. Kurtzman et al., the genera Yamada comb. nov. Waltomyces Yamada et Nakase (Yamada and Nakase Genus belongs to Lipomycetaceae. Cells are encap- 1985), Babjevia van der Walt et Smith (Smith et al. sulated, globose, ellipsoid or ovoid, occurring singly or 1995), Smithiozyma van der Walt, Kock et Yamada (Kock in pairs, budding multilaterally. Asci are unconjugated, et al. 1995) and Kawasakia Yamada et Nogawa (Yamada attached, globose, allantoid or amoeboid, multispored, and Nogawa 1995b)—all names that were not accepted by evanescent, arising by direct transformation of single Kurtzman et al. (2007)—should be retained. And additional vegetative cells aggregated. Ascospores are allantoid to new genera can be proposed. cymbiform, glabrous, amber-coloured and conjugated when The four species of the genus Zygozyma that were proved liberated. Fermentation is absent. D-Glucose, D-xylose, D- to have long phylogenetic distances and low bootstrap values xylitol, glycerol, 2-keto-D-gluconic acid, 5-keto-D-gluconic at the branching points, respectively, in the phylogenetic acid and sucrosum are assimilated. D-Galactose, L-sorbose, trees are enough to constitute respective genera, as suggested D-arabinose, L-arabinose, D-mannitol, D-sorbitol, L-arabitol, previously (Yamada and Nogawa 1995a)(Fig. 1). D-ribitol, maltose, lactose, melibiose, trehalose and raffinose Ann Microbiol (2011) 61:689–693 693 Smith MTh (1998a) Lipomyces Lodder & Kreger-van Rij. In: are not assimilated. Potassium nitrate is not assimilated. Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study, 4th Coenzyme Q-9 system is present. Guanine+cytosine con- edn. Elsevier, Amsterdam, pp 248–253 tents of DNA are 55.3–55.7 mol%. Smith MTh (1998b) Zygozyma van der Walt & von Arx. In: Kurtzman Type species: Limtongia smithiae (van der Walt, CP, Fell JW (eds) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 433–436 Wingfield et Yamada) Jindamorakot, Am-in, Yukphan et Smith MTh, van der Walt JP, Yamada Y, Batenburg-van der Vegte WH Yamada comb. nov. (1989) Zygozyma suomiensis sp. nov. (Lipomycetaceae), a new Basionym: Zygozyma smithiae van der Walt, Wingfield species from Finland. Antonie van Leeuwenhoek 56:283–288 et Yamada, Antonie van Leeuwenhoek 58: 96, 1990. Smith MTh, van der Walt JP, Batenburg-van der Vegte WH (1995) Babjevia gen. nov. - a new genus of the Lipomycetaceae. 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Annals of MicrobiologySpringer Journals

Published: Jan 11, 2011

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