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Multigene Phylogenetic Analysis of Pathogenic Candida Species in The 097 JOURNAL OF CLINICAL MICROBIOLOGY, Jan. 2005, p. 101-111 Vol. 43, o. 1 0095-1137/05/$08.00+0 doi:1O.1128/JCM.43.1.101-111.2005 Copyright © 2005, American Society for Microbiology. All Rights Reserved. Multigene Phylogenetic Analysis of Pathogenic Candida Species in the Kazachstania (Arxiozyma) telluris Complex and Description of Their Ascosporic States as Kazachstania bovina sp. nov., K. heterogenica sp. nov., K. pintolopesii sp. nov., and K. slooffiae sp. nov. Cletus P. Kurtzman/* Christie J. Robnett,! Jerrold M. Ward,2 Cory Brayton,3 Peter Gorelick,4 and Thomas J. Walsh2 Microbial Genomics and Bioprocessing Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, u.s. Department ofAgriculture, Peoria, Illinois!,' Immunocompromised Host Section, Pediatric Oncology Branch, National Cancer Institute, Bethesda, Marylanr£2; Center for Comparative Medicine, 3 The Baylor College ofMedicine, Houston, Texas ; and Animal Health Diagnostic Laboratory, National Cancer Institute at Frederick, SAIC Frederick, Frederick, Maryland4 Received 2 July 2004/Returned for modification 3 September 2004/Accepted 13 September 2004 A yeast causing widespread infection of laboratory mice was identified from 26S rRNA gene sequences as Candida pintolopesii. To determine the relationship of C. pintolopesii with other members of the Kazachstania (Arxiozyma) telluris species complex, nucleotide sequences from domains 1 and 2 of the 26S rRNA gene, the mitochondrial small-subunit rRNA gene, and the RNA polymerase II gene were phylogenetically analyzed. That analysis resolved the 48 strains examined into five closely related species: K. telluris, Candida bovina, C. pintolopesii, Candida sloojfiae, and a previously unknown species. One or more strains of each of the last four species formed an ascosporic state much like that of K. telluris. To place these ascosporogenous strains taxonomically, it is proposed that they be assigned to the teleomorphic genus Kazachstania as K. bovina (type strain NRRL Y-7283, CBS 9732, from the nasal passage of a pigeon), K. heterogenica (type strain NRRL Y-27499, CBS 2675, from rodent feces), K. pintolopesii (type strain NRRL Y-27500, CBS 2985, from the peritoneal fluid of a dead guinea pig), and K. sloojfiae (type strain NRRL YB-4349, CBS 9733, from the cecum of a horse). On the basis of multigene sequence analyses, K. heterogenica appears to be a hybrid ofK. pintolopesii and a presently unknown species. With the exception of K. bovina, the phylogenetically defined species show a moderate degree of host specificity. During 2002, laboratory mice received by the ational In­ represent the anamorphic states of this ascosporogenous spe­ stitutes of Health from several different suppliers were infected cies (4, 19, 20). Mendon~a-Hagler and Phaff (12) tested this with a yeast, which rendered the mice unsuitable for laboratory possibility by measuring the extent of nuclear DA comple­ use. Domains 1 and 2 (Dl and D2, respectively) of the large­ mentarity among the four taxa. All four were reported to share subunit (26S) rR A genes of isolates from seven mice were 80% or greater nuclear DA relatedness, leading Mendonc;a­ sequenced in our laboratory, and the sequences were identical Hagler and Phaff (12) to propose that the four taxa represent to one another and to that of the type strain of Candida the same species. Hurt (2) reexamined the nuclear DNA re­ pintolopesii. Strains of a species generally have the same Dl latedness among the four taxa using a free-solution reassocia­ and D2 rR A gene sequences, or the sequences may some­ tion method rather than the filter-binding technique of Men­ times vary by 1 to 3 nucleotides (10). Consequently, from these donc;a-Hagler and Phaff (12). In contrast to the earlier results, sequence comparisons, we concluded that the mice were in­ Hurt (2) found only 20 to 56% nuclear DNA relatedness fected with C. pintolopesii. among the various pairings, which would suggest that the taxa C. pintolopesii is a member of the Kazachstania (Arxiozyma) represent four separate, but closely related, species. James et telluris species complex. Arxiozyma telluris was first described as al. (3) compared the four taxa by phylogenetic analysis of the Saccharomyces tellustris by van der Walt (17). Because the nucleotide sequences of the 18S rR A gene, 26S Dl and D2 ascospore walls of this species are roughened as a result of rRNA genes, and the mitochondrially encoded cytochrome surface ornamentation (5), van der Walt and Yarrow (18) oxidase II gene. These results again suggested that the taxa concluded that S. tellustris was not typical of the smooth-spored represent four separate but closely related species, and in view Saccharomyces sensu stricto species and redescribed it as A. of this genetic divergence, James et al. (3) proposed reinstate­ telluris. Candida bovina, C. pintolopesii, and Candida slooffiae ment of pintolopesii and slooffiae as distinct species. are phenotypically much like A. telluris and were believed to C. C. More recently, Kurtzman and Robnett (11) examined genus boundaries in the Saccharomyces complex by multigene se­ *' Corresponding author. Mailing address: Microbial Genomics and quence analysis. The ca. 80 species resolved into 14 clades, Bioprocessing Research Unit, ational Center for Agricultural Utili­ which were interpreted as genera, resulting in redescriptions of zation Research, Agricultural Research Service, U.S. Department of Agriculture, 1815 . University St., Peoria, IL 61604. Phone: (309) some previously accepted genera and the proposal of five new 681-6561. Fax: (309) 681-6672. E-mail: [email protected]. genera (8). Clade 2 from the analysis included several species 101 102 KURTZM ET AL. J. eLi . MICROBIOL. of Saccharomyces and Kluyveromyces that were phylogeneti­ rection was used for neighbor-joining analyses. Bootstrap support for the phy­ cally unrelated to the type species of their respective genera, as logenetic trees was determined from 1,000 replications. well as species of the monotypic genera Arxiozyma, Kazach­ Nucleotide sequence accession numbers. The GenBank accession numbers of the sequences determined from the analysis of each gene, except for those of stania, and Pachytichospora. Of the last three genera, Kazach­ the RA polymerase II gene (GenBank accession numbers AY552467 to stania has taxonomic priority, resulting in the transfer of A. AY552472) and the mitochondrial small-subunit rRNA gene (GenBank acces­ telluris and other clade 2 species to Kazachstania. sion numbers AF442281 to AF442286), which were used for comparison with In the present study, we compared the mouse isolates with species in the Saccharomyces cerevisiae clade, are given on the phylogenetic trees. other strains of the K telluris complex and resolved five clades by Dl and D2 26S rR A gene sequence analysis, consistent RESULTS with the report of James et al. (3). We further compared these isolates by analysis of the mitochondrial small-subunit rR A Initial identification of yeasts from laboratory animals. In gene and RA polymerase II gene sequences. Analyses of the addition to the mice at the ational Cancer Institute that were last two data sets gave trees congruent with the tree con­ observed to have yeasts within the gastrointestinal tract, a line structed from the Dl and D2 sequences, supporting the con­ of knockout mice with a B6:129 background from that facility cept that C. pintolopesii, C. bovina, and C. slooffiae are distinct were shipped to another large research facility in another state species. The analyses also detected an additional, previously for rederivation and eventual research. The mice were rou­ unknown species. Microscopic examination of the cultures re­ tinely maintained in a receiving and quarantine room. The vealed that one or more strains from each of these four clades gastrointestinal infection had not been seen at that research formed ascospores. Consequently, we propose placement of facility for many years. The transported infected mice were the ascosporic states of C. pintolopesii, C. bovina, C. slooffiae, found to have gastric infection with chronic gastritis. DBN and the newly detected species in the teleomorphic genus 2 Cr mice placed in the same cage as infected null mice for 4 Kazachstania. months also developed gastric infection. Histopathology. The histopathological gastric changes con­ sisted of numerous but variable numbers of yeast-like organ­ MATERIALS AND METHODS isms in gastric epithelial surface debris and along the surfaces Initial identification of yeasts from laboratory animals. The yeast-like organ­ of epithelial cells throughout all regions of the glandular stom­ isms were first found during necropsy and by histopathology in sentinel and research mice of various strains and stocks from a facility where caging, food, and ach. Hematoxylin-eosin staining revealed that the organisms bedding were not autoclaved. These organisms were not observed in an adjacent were small, approximately 3 j.Lm in diameter, spherical to ovoid barrier facility where caging, food, and bedding were autoclaved. Similar organ­ yeast-like cells with a dark blue outer wall and some internal isms were found frequently in hamsters and sporadically in rat sentinels from the dot-like structures. These organisms were densely positive by same facility and in nude and heterozygous nude mice in a facility at an unrelated periodic acid-Schiff staining. Chronic inflammation with lym­ institu tion. Histology. Multiple tissues from
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