Antonie van Leeuwenhoek (2014) 106:67–84
`DOI 10.1007/s10482-014-0170-z
`
`I N I V I T E D R E V I E W
`
`Antonie van Leeuwenhoek 80th Anniversary Issue
`
`On the reclassification of species assigned to Candida
`and other anamorphic ascomycetous yeast genera
`based on phylogenetic circumscription
`
`Heide-Marie Daniel • Marc-Andre´ Lachance •
`Cletus P. Kurtzman
`
`Received: 14 February 2014 / Accepted: 4 April 2014 / Published online: 19 April 2014
`Ó Springer International Publishing Switzerland 2014
`
`Abstract Multigene phylogenies have been instru-
`mental in revising the classification of ascosporic
`(teleomorph) yeasts in a natural system based on lines
`of descent. Although many taxonomic changes have
`already been implemented for teleomorph taxa, this is
`not yet the case for the large genus Candida and
`smaller anascosporic (anamorph) genera. In view of
`the recently introduced requirement
`that a fungal
`species or higher taxon be assigned only a single valid
`name under the new International Code of Nomen-
`clature for algae, fungi, and plants (Melbourne Code),
`the current species of Candida and other anamorph
`yeast genera must undergo revision to make genus
`membership consistent with phylogenetic affinities. A
`review of existing data and analyses shows that certain
`Candida species may be assigned to teleomorph
`
`H.-M. Daniel (&)
`Mycothe`que de l’Universite´ catholique de Louvain
`(BCCM/MUCL), Earth and Life Institute, Mycology
`Laboratory, Universite´ catholique de Louvain, Croix du
`Sud 2 bte L7.05.06, 1348 Louvain-la-Neuve, Belgium
`e-mail: heide-marie.daniel@uclouvain.be
`
`M.-A. Lachance
`Department of Biology, University of Western Ontario,
`London, ON N6A 5B7, Canada
`
`C. P. Kurtzman
`Bacterial Foodborne Pathogens and Mycology Research
`Unit, National Center for Agricultural Utilization
`Research, Agricultural Research Service, U.S.
`Department of Agriculture, Peoria, IL 61604, USA
`
`genera with high confidence using multigene phylog-
`enies. Candida species that form well-circumscribed
`phylogenetic clades without any teleomorph member
`justify the creation of new genera. However, a
`considerable number of Candida species sit at the
`end of isolated and often long branches, and hence
`cannot be assigned to larger species groups. They
`should be maintained in Candida sensu lato until
`studied by multigene analyses in datasets with com-
`prehensive taxon sampling. The principle of name
`stability has to be honoured to the largest extent
`compatible with a natural classification of Candida
`species.
`
`Keywords Candida Reclassification
`Ascomycetous yeasts Dual nomenclature
`
`Melbourne Code
`
`Introduction
`
`Ascomycetous yeasts without known sexual states
`have been classified according to mode of cell division
`and occurrence of unique cellular morphologies.
`Three types of cell division have been observed;
`bipolar, with budding only at the poles of the cell (e.g.,
`Kloeckera, Schizoblastosporion); multipolar or multi-
`lateral, in which budding occurs at many sites on the
`cell wall (e.g., Botryozyma, Candida, Myxozyma,
`Saitoella, Trigonopsis); and fission,
`in which the
`new cell wall develops without constriction of the
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`68
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`Antonie van Leeuwenhoek (2014) 106:67–84
`
`parent cell wall as in bud formation (e.g., Schizosac-
`charomyces). Distinctive cell morphologies occur in
`several genera, such as Brettanomyces (ogival-shaped
`cells) and one species of Trigonopsis (triangular cells).
`Presence or absence of pseudohyphae or true hyphae
`has also been used to define genera. Asexual yeasts
`that divide by multilateral budding but have no
`distinctive cellular morphology have been assigned
`to the genus Candida. This system of classification
`allowed morphologically indistinguishable species to
`be grouped in a single genus, in parallel to the more
`intricate system used for sexually reproducing species,
`which were assigned to genera based primarily on
`ascus and ascospore morphology.
`DNA-based studies showed that phenotypic char-
`acteristics alone are inadequate in building a stable,
`informative, and emendable classification system,
`likely due to evolutionary parallelisms and reversals
`(Kurtzman and Robnett 1994; Guzma´n et al. 2013).
`Multi-gene sequence analysis, such as for the Saccha-
`romycetaceae (Kurtzman and Robnett 2003), has
`shown that circumscription of yeast genera from
`phenotypic characters is often not congruent with their
`delineation based on molecular phylogenies. In con-
`trast, the classification of asexually reproducing yeasts
`was rarely addressed in molecular phylogenetic stud-
`ies because their inclusion in Candida and other
`anamorphic genera satisfied the requirements of
`longstanding rules under the International Code of
`Botanical Nomenclature. However, a recent change in
`the rules for naming pleomorphic fungi now requires
`that a fungal species or higher taxon be assigned only a
`single valid name under the new Code [International
`Code of Nomenclature for algae, fungi, and plants
`(Melbourne Code) (McNeill et al. 2012)]. As a
`the current species of Candida and
`consequence,
`other asexual yeast genera must undergo revision to
`make genus membership consistent with phylogenetic
`affinities. In the case of species that currently possess
`both anamorph and teleomorph names, a decision will
`be required regarding which name to retain. In the
`previous system, the teleomorph name had priority,
`but the new Code places both names on an equal
`footing and reaffirms instead the principles of histor-
`ical priority and common usage.
`In the discussion that follows, we examine anamor-
`phic ascomycetous yeast genera (Tables 1, 2) and
`consider the impact of phylogenetic circumscription
`and changes in the Code on their standing. The genus
`
`123
`
`Table 1 Anamorph-teleomorph connections among ascomy-
`cetous yeasts
`
`Anamorphic genus
`
`Teleomorphic genus
`
`Saccharomycotina
`
`Aciculoconidium
`
`Blastobotrys
`
`Botryozyma
`
`Brettanomyces
`
`Candida
`
`Geotrichum
`
`Kloeckera
`
`Macrorhabdus
`
`Myxozyma
`
`Saprochaete
`
`Unknown. Near Kodamaea.
`
`Trichomonascus
`
`Ascobotryozyma
`
`Dekkera
`
`Many genera
`
`Dipodascus and Galactomyces
`
`Hanseniaspora
`
`Unknown.
`
`Lipomyces
`
`Magnusiomyces
`
`Schizoblastosporion
`
`Nadsonia
`
`Trigonopsis
`
`Taphrinomycotina
`
`Lalaria
`
`Saitoella
`
`Unknown. Near Botryozyma
`and Tortispora.
`
`Taphrina
`
`Unknown. Near Taphrina
`and Protomyces.
`
`Candida is of major concern because it has experi-
`enced a disproportionate increase in size relative to
`other genera. The most recent treatment of the genus
`recognized 314 species of multiple phylogenetic
`affiliations and listed 51 additional species names
`without discussion (Lachance et al. 2011). Since then,
`the number of new species assigned to Candida has
`continued to increase. After consultation of the asco-
`mycetous yeast sequence database YeastIP (http://geno
`me.jouy.inra.fr/yeastip/) (Weiss et al. 2013), Mycobank
`(http://www.mycobank.org/) (Crous et al. 2004) on
`February 11 2014, and the SCOPUS literature database,
`we here account for 434 Candida species and discuss
`their classification. Importantly, the genus Candida and
`its many species have served as major vehicles for crucial
`information regarding treatment options for opportunistic
`pathogenic species, artisanal and industrial processes,
`food regulations, enzyme production, osmophily, ther-
`motolerance, substrate specificities, and possible eco-
`logical roles. The genus has been kept intact in line with
`Berkhout’s (1923) original intent to accommodate a
`variety of largely undifferentiated yeasts, while avoiding
`the creation of numerous phylogenetically circumscribed
`new genera that are impossible to recognize by phenotype
`(Kurtzman 2011). The new Code no longer allows
`
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`Antonie van Leeuwenhoek (2014) 106:67–84
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`69
`
`Table 2 Placement of selected anamorphic species in genera and undescribed clades of the Saccharomycotina
`
`Family/genus or clade
`
`Species
`
`Debaryomycetaceae
`Lodderomyces/Candida albicans C. albicans, C. blackwelliaea,c, C. bohioensisc,
`C. buenavistaensis, C. chauliodes, C. corydali, C. dubliniensis,
`C. frijolesensis, C. gigantensis, C. hyderabadensisa,
`C. jiufengensisa, C. labiduridarum, C. maltosa, C. metapsilosisa,
`C. morakotiaea, C. neerlandica, C. orthopsilosis,
`C. oxycetoniaea, C. parapsilosis, C. prachuapensisa,
`C. pseudojiufengensisa, C. sakaeoensisa, C. sanyaensisa,
`C. saraburiensisa, C. sojae, C. tetrigidarum, C. theaea,
`C. tropicalis, C. verbasci, C. viswanathii
`
`Candida glaebosa clade
`
`Candida kruisii clade
`
`Candida tanzawaensis clade
`
`Hyphopichia
`
`Kurtzmaniella
`
`Yamadazyma
`
`Metschnikowiaceae
`
`Clavispora
`
`C. fluviatilis, C. glaebosa, C. manassasensis, C. palmioleophila,
`C. pseudoglaebosa, C. saitoana, C. sphagnicola
`C. aglyptinic, C. atbi, C. barrocoloradensis, C. cretensis,
`C. gatunensis, C. kruisii, C. lycoperdinae, C. pallodes,
`C. panamensis, C. stri, C. tritomae
`
`C. ambrosiae, C. anneliseae, C. atakaporum, C. bokatorum,
`C. bolitotheri, C. bribrorum, C. canberraensis,
`C. chickasaworum, C. choctaworum, C. emberorum,
`C. guaymorum, C. kunorum, C. maxii, C. panamericana,
`C. prunicola, C. pyralidae, C. taliae, C. tanzawaensis,
`C. terraborum, C. vadensisa, C. wounanorum, C. xylopsoci,
`C. yuchorum
`C. fennica, C. gotoi, C. homilentoma, C. khmerensisa,
`C. pseudorhagiia, C. rhagii, C. wangnamkhiaoensisa
`C. anglicaa, C. boleticola, C. fragi, C. oleophila, C. railenensisa,
`C. santamariae, C. schatavii, C. zeylanoides
`C. aaseri, C. amphicisa,c, C. andamanensisa, C. atlantica,
`C. atmosphaerica, C. blattariaea, C. buinensis,
`C. cerambycidaruma, C. conglobata, C. dendronema,
`C. diddensiae, C. diospyria, C. endomychidaruma,
`C. friederichii, C. germanicaa, C. gorgasiia, C. insectorum,
`C. jarooniia, C. kanchanaburiensisa, C. khao-thaluensisa,
`C. keroseneaea, C. koraticaa, C. lessepsiia, C. membranifaciens,
`C. michaeliia, C. naeodendraa, C. oceania, C. olivaea,
`C. pseudoaaseria, C. songkhlaensisa, C. spencermartinsiaea,
`C. takamatsuzukensisa, C. tallmaniaea, C. tayloriia,c,
`C. tammaniensisa, C. tenuis, C. trypodendronia, C. tumulicolaa,
`C. vaughaniaea, C. vrieseaea
`
`C. aechmeae, C. akabanensis, C. asparagi, C. aurisa,
`C. berkhoutiaea, C. blattae, C. bromeliacearum, C. carvajalisa,
`C. chanthaburiensisa, C. citria, C. dosseyi,
`C. duobushaemuloniia, C. ecuadorensisa, C. eppingiaea,
`C. ezoensisa, C. flosculorum, C. fructus, C. haemulonii,
`C. heveicolaa, C. intermedia, C. inulinophilaa, C. konsanensisa,
`C. kutaonensisa, C. middelhovenianaa, C. mogii, C. musae,
`C. oregonensis, C. phyllophilaa, C. pseudoflosculoruma,
`C. pseudohaemuloniia, C. pseudointermedia,
`C. rhizophorensisa,c, C. ruelliaea, C. sharkensisa,c,
`C. suratensisa, C. thailandica, C. tolerans, C. tsuchiyae,
`C. ubatubensis, C. vitiphilaa
`
`Genetic markers
`
`SSU, D1/D2 LSU
`
`SSU, D1/D2 LSU
`
`SSU, D1/D2 LSU
`
`SSU, D1/D2 LSU
`
`D1/D2 LSU
`
`SSU, D1/D2 LSU
`
`SSU, D1/D2 LSU
`
`ACT1, EF1, Mcm7, RPB2
`
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`70
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`Table 2 continued
`
`Family/genus or clade
`
`Species
`
`Antonie van Leeuwenhoek (2014) 106:67–84
`
`Genetic markers
`
`SSU, D1/D2 LSU
`
`Kodamaea
`
`C. alishanicaa, C. arcana, C. derodonti, C. fukazawae,
`C. fungicola, C. hsintzibuensisa, C. kaohsiungensisa,
`C. leandreaa, C. lidongshanicaa, C. loeiensisa, C. mesenterica,
`C. plutei, C. restingaea, C. sagamina, C. smagusaa, C. suecica,
`‘Endomyces scopularum’d
`
`Ogataea
`
`Pichiaceae, methanol-assimilating yeasts and near relatives
`C. arabinofermentans, C. boidinii, C. chumphonensisa,
`C. krabiensisa, C. maris, C. mattranensisa, C. methanosorbosa,
`C. nanaspora, C. nemodendra, C. nitratophila, C. ortoniia,
`C. ovalis, C. piceae, C. pini, C. rishiriensisa, c, C. sithepensisa,
`C. sonorensis, C. succiphila, C. suzukii, C. xyloterinib
`
`LSU, SSU, EF1a, mtSSU
`
`Phaffomycetaceae
`
`Cyberlindnera
`
`Wickerhamomyces
`
`Trichomonascaceae and Starmerella
`
`Starmerella
`
`Trichomonascus
`
`Wickerhamiella
`
`C. adriatica, C. easanensisa, C. hungchunanaa, C. maesaa,
`C. maritima, C. mengyuniaea, C. mycetangii,
`C. nakhonratchasimensisa, C. pattaniensisa, C. stauntonicaa,
`C. takataa, C. taoyuanicaa, C. variovaarae
`C. dajiaensisa, C. jianshihensisa, C. namnaoensis, C. odintsovae,
`C. peoriensis, C. ponderosae, C. quercuum, C. silvicultrix,
`C. ulmi, C. yuanshanicaa,c
`
`LSU, SSU, EF1a
`
`LSU, SSU, EF1a
`
`C. apicola, C. apis, C. batistae, C. bombi, C. cellae,
`C. davenportii, C. etchellsii, C. floricola, C. floris,
`C. geochares, C. gropengiesseri, C. khaoyaiensis, C. kuoi,
`C. lactis-condensi, C. magnoliae, C. potachaoreniae,
`C. powellii, C. ratchasimensis, C. riodocensis, C. sirachaensis,
`C. sorbosivorans, C. stellata, C. stigmatis, C. tilneyi, C. vaccinii
`C. allociferriia, C. muciferaa, Blastobotrys adeninivorans,
`B. attinoruma, B. americana, B. arbuscula, B. aristata,
`B. capitulata, B. chiropterorum, B. elegans, B. illinoiensis,
`B. indianensis, B. malaysiensis, B. mokoenaii, B. muscicola,
`B. nivea, B. parvus, B. peoriensis, B. proliferans,
`B. raffinosifermentans, B. robertiia, B. serpentisa, B. terrestris
`C. alocasiicolaa, C. azyma, C. azymoidesa, C. bombiphilaa,
`C. drosophilae, C. galacta, C. hasegawaea, C. infanticola,
`C. jalapaonensisa, C. kazuoia, C. musiphilaa, C. pararugosa,
`C. parazymaa, C. sergipensisa, C. sorbophila, C. spandovensis,
`C. vanderwaltii
`
`D1/D2 LSU
`
`LSU, mtSSU, COX2
`
`LSU, mtSSU, COX2
`
`Additional groupings are discussed in the text. Genetic markers used to circumscribe the genera or clades are mentioned
`a Placement by D1/D2 LSU sequence analyses
`b Placement by SSU and D1/D2 LSU sequence analyses
`c Spelling corrected according to www.indexfungorum.org
`d Among the only three available cultures of E. scopularum, one was attributed to Pezizomycotina (Euascomycetes) (CBS 131.86)
`while two (CBS 154.92, CBS 155.92) clustered with Candida species that belong to the Kodamaea clade in analyses of SSU and D1/
`D2 LSU sequences (Suh et al. 2001), and represent a Kodamaea species
`
`maintenance of the status quo and implementation of the
`new rules is underway, as exemplified in the reclassifi-
`cation of anamorphic species in teleomorph-typified
`genera such as Alloascoidea (Kurtzman and Robnett
`2013b), Ambrosiozyma (Kurtzman and Robnett, 2013c),
`Diddensiella (Pe´ter et al. 2012), Scheffersomyces (Urbina
`
`and Blackwell 2012a, b), Starmerella (Duarte et al.
`2012), and Yarrowia (Groenewald and Smith 2013; Nagy
`et al. 2013), and the reclassification of ascosporic Asco-
`botryozyma species into the anamorphic genus Bot-
`ryozyma (Lachance and Kurtzman 2013). When newly
`discovered asexual species are described as members of
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`71
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`teleomorphic genera or former anamorphs are reassigned
`to them, authors increasingly add the mention of f.a.,
`forma asexualis, to draw attention to the fact that the
`sexual state is unknown, as suggested by Lachance
`(2012).
`In this review, we discuss the placement of
`anamorphic species in currently recognized genera
`and consider assignment of divergent species to new
`phylogenetically circumscribed genera. As part of this
`analysis, we shall also examine assignment of genera
`to families. Although family-level classification in
`ascomycetous yeasts is not completely resolved, a
`phylogenetic analysis using small (SSU) and large
`subunit (LSU) rRNA, translation elongation factor
`(EF1a), RNA polymerase II, subunits B1 and B2
`(RPB1, RPB2) gene sequences (referred to as ‘five-
`gene analysis’) that included representatives of almost
`all known genera lends support to the backbone of a
`phylogenetic tree (Fig. 1, Kurtzman and Robnett
`2013a) that reflects the family classification proposed
`by Kurtzman (2011).
`
`Debaryomycetaceae
`
`Ascosporic genera that are presently assigned to the
`Debaryomycetaceae include Debaryomyces, Kurtz-
`maniella, Lodderomyces, Meyerozyma, Millerozyma,
`Priceomyces,
`Scheffersomyces,
`Schwanniomyces,
`Spathaspora, Wickerhamia, and Yamadazyma (Kurtz-
`man 2011). Hyphopichia was placed among these
`genera by the five-gene analysis (Fig. 1, Clade 6) in
`contrast to its earlier classification in the Metschnik-
`owiaceae. Yeasts in this family are characterized by
`ubiquinone Q-9, but at present, most species relation-
`ships in this family have only been analyzed using D1/
`D2 LSU and SSU sequence data (Kurtzman and
`Suzuki 2010) and branch support is oftentimes weak.
`Candida, the most prominent genus in the Debary-
`omycetaceae, is typified by C. vulgaris, a synonym of
`C. tropicalis, and will be restricted to the monophy-
`letic group that includes C. tropicalis, C. albicans, the
`ascosporic species Lodderomyces elongisporus, and
`28 additional species (Ji et al. 2009; Lachance et al.
`2011; Nitiyon et al. 2011; Chang et al. 2012a; Limtong
`et al. 2012b; Hui et al. 2013; Sipiczki 2013) (Table 2).
`Consistent with the Code, the genus name for species
`in this clade should be Candida as it is widely used, in
`contrast to Lodderomyces, which is encountered only
`
`infrequently. Numerous new species have been added
`to this clade and the expansion suggests that C. trop-
`icalis and C. albicans might occupy distinct sister
`clades. This prospect argues strongly for the retypifi-
`cation of Candida on the widely recognized species
`C. albicans.
`Many Candida species can be assigned to presently
`described genera, but the genus also contains species
`with no known phylogenetic affinities in existing
`genera. Among these are the C. glaebosa clade, which
`includes
`seven described species
`(Table 2) and
`the C.
`tropicalis,
`appears to be a neighbor of
`Spathaspora, and Scheffersomyces clades (Kurtzman
`and Suzuki 2010; Kachalkin and Yurkov 2012; Suh
`et al. 2013). Members of the C. glaebosa clade appear
`similar in their responses on common growth tests and
`sugar fermentation is often slow, weak or absent.
`Candida ascalaphidarum was most similar
`to C.
`palmioleophila, a member of this clade based on D1/
`D2 LSU sequences, although of uncertain affiliation
`when adding SSU sequences to the analysis (Nguyen
`et al. 2007).
`The C. kruisii clade includes 11 species (Suh et al.
`2006; Lachance et al. 2011) (Table 2), all of which are
`associated with mushrooms and the beetles feeding on
`them. The species belong to three subclades, two of
`which differ in growth reaction to cycloheximide, but
`the subclades appear to represent a single genus. The
`large C. tanzawaensis clade, which presently includes
`23 species (Kurtzman 2001; Suh et al. 2004; Lachance
`et al. 2011) (Table 2), is also associated with beetles
`and wood-decaying mushrooms. The species assimi-
`late xylose, which suggests an ecological role in the
`decomposition of wood-derived carbohydrates. Basal
`to the C. tanzawanaensis clade are C. caryicola and
`C. tibetensis with the even more distant neighbors
`C. linzhiensis and C. sequanensis (Lachance et al.
`2011). The assignment of these four species to two or
`more separate genera should await additional gene
`sequences to confirm their phylogenetic position.
`Candida sake and C. alai also represent monotypic
`lineages that may represent separate genera (Lachance
`et al. 2011), but their placement also must await
`additional gene sequence analyses.
`Placement of the ascosporic genus Hyphopichia is
`weakly supported in the Debaryomycetaceae from the
`five-gene analysis (Fig. 1, Clade 6). The Hyphopichia
`clade includes seven Candida species (Limtong et al.
`2012a) (Table 2), most of which are on long branches
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`Antonie van Leeuwenhoek (2014) 106:67–84
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`Fig. 1 Phylogenetic
`relationships among type
`species of ascomycetous
`yeast genera and reference
`taxa determined from
`maximum likelihood
`analysis using concatenated
`gene sequences for SSU
`rRNA, LSU rRNA, EF-1a,
`RPB1 and RPB2 (from
`Kurtzman and Robnett
`2013a). Filobasidiella
`neoformans was the
`designated outgroup species
`in the analysis. Names in
`bold font are type species of
`currently recognized genera,
`whereas names in standard
`font are not type species.
`Bootstrap values (1,000
`replicates) [50 % are given
`at branch nodes. Strain
`accession numbers are
`NRRL unless otherwise
`indicated. Designations in
`brackets indicate the
`coenzyme Q value for each
`species. Alloascoidea,
`Diddensiella and Tortispora
`are newly described
`ascosporic genera
`(Kurtzman and Robnett
`2013b; Lachance and
`Kurtzman 2013; Pe´ter et al.
`2012) and
`Middelhovenomyces is a
`newly described
`anamorphic genus
`(Kurtzman and Robnett
`2014). The new anamorphic
`genera Danielozyma (near
`Kodamaea) and Deakozyma
`(near Yarrowia) (Kurtzman
`and Robnett 2014) are not
`included in this analysis
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`73
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`when analyzed from D1/D2 LSU sequences. The
`Kurtzmaniella clade includes eight species of Candida
`(Kurtzman 2011; Lachance et al. 2011) (Table 2).
`Other species that may be members or neighbors of
`this clade include C. aurita, C. natalensis, C. quer-
`citrusa, C. multigemmis and C. sophiae-reginae. Can-
`dida pseudofarinosa is to be assigned to Millerozyma
`based on ACT1, RPB1 and RPB2 sequences (Mallet
`et al. 2012) and C. psychrophila to Debaryomyces
`based on high D1/D2 LSU similarity (Kurtzman
`2011).
`Candida athensensis, C. carpophila, C. neuston-
`ensis, and C. smithsonii are assigned to the Meyer-
`ozyma clade based on D1/D2 LSU sequences, although
`with high bootstrap support (Chang et al. 2010;
`Lachance et al. 2011). The rarely isolated C. elateri-
`darum and the osmophilic C. glucosophila join the
`clade on long, unsupported branches. Candida fer-
`menticarens and C. northwykensis appear to be mem-
`bers of Priceomyces based on D1/D2 LSU, supported
`by SSU sequence analysis for the former species
`(Kurtzman and Suzuki 2010; Ravella et al. 2011).
`The genus Scheffersomyces has been revised and
`Candida species were included based on a multilocus
`phylogenetic analysis (Urbina and Blackwell 2012a, b).
`An analysis with extended taxon sampling indicated
`polyphyly of the genus, also reflected by either xylose or
`cellobiose fermenting ability, calling for a limitation of
`Schefferomyces to the clade comprising the type species
`Sch. stipitis as well as Sch. cryptocercus, Sch. illinoi-
`ensis, Sch. insectosa, Sch. lignosus, Sch. parashehatae,
`Sch. quercinus, Sch. segobiensis, Sch. shehatae, Sch.
`virginianus, andSch. xylosifermentans (Suh et al. 2013).
`The species C. broadrunensis, C. thasaenensis, Sch.
`amazonensis, Sch. coipomoensis, Sch. ergatensis, Sch.
`gosingicus, Sch. lignicola, Sch. queiroziae, andSch.
`spartinae need to be reclassified.
`The genus Spathaspora is composed of a core
`group that is well supported by phylogenetic analyses
`of D1/D2 LSU sequences and includes C. jeffriesii,
`C. materiae, Sp. arborariae, Sp. brasiliensis, Sp.
`passalidarum, and Sp. suhii (Cadete et al. 2013).
`Spathaspora xylofermentans and Sp. roraimanensis
`share the unique ascospore morphology of this group,
`but form variable associations with species such as
`C. sake or C. alai and C. insectamans, all likely to
`represent independent genera because of long branch
`lengths. Other weakly associated species include
`C. lyxosophila, C. xylanilytica,
`and C. subhashii
`
`(Boonmak et al. 2011). The redefinition of Spathas-
`pora requires the use of gene sequences providing
`higher resolution than D1/D2 LSU.
`The genus Yamadazyma presently has 11 assigned
`species. However, sequence analysis has identified 40
`phylogenetically related Candida species (Burgaud
`et al. 2011; Groenewald et al. 2011a; Junyapate et al.
`2014; Lachance et al. 2011; Nagatsuka et al. 2009)
`(Table 2), which will expand Yamadazyma into one of
`the larger genera of the Debaryomycetaceae.
`
`Metschnikowiaceae
`
`Most genera in the Metschnikowiaceae clade (Acicu-
`loconidium, Clavispora, Kodamaea, Metschnikowia)
`resemble those of Debaryomycetaceae in ubiquinone
`Q-9 formation and both families were placed in the
`same large Clade 6 by the five-gene analysis (Fig. 1).
`The Metschnikowiaceae form a well-supported cluster
`with exclusion of Hyphopichia. Clavispora is an
`exception in possessing ubiquinone Q-8. The genera
`Metschnikowia and Clavispora are distinguished by
`their
`ubiquinones
`and
`ascospore morphology,
`although these traits are not known for all members.
`The evolutionary rates of D1/D2 LSU sequences are
`highly diverse in the Metschnikowia/Clavispora clade
`and phylogenetic analyses using housekeeping genes
`are required to circumscribe both genera reliably. An
`analysis using four coding genes confirmed some, but
`not all groups derived by D1/D2 LSU analysis,
`although some species placements still remain to be
`resolved (Guzma´n et al. 2013). The analysis delin-
`eated four groups, two of which comprised Metsch-
`nikowia species and included C. chrysomelidarum,
`C. gelsemii, C. golubevii, C. hawaiiana, C. ipomoeae,
`C. kipukae, C. kofuensis, C. picachoensis, C. pimen-
`sis, C. rancensis, and C. torresii with reasonable to
`high statistical support. Candida wancherniae could
`be assigned to one of these groups based on D1/D2
`LSU similarity to M. agaves (Nakase et al. 2009b).
`Candida danieliae and C. hainanensis were only
`loosely connected to members of these groups by
`long branches and their placement needs to be ascer-
`tained by multigene analysis (Wang et al. 2008;
`Groenewald et al. 2011b). A distinct group was formed
`by C. picinguabensis and C. saopaulonensis with
`C. melibiosica joined on a long branch, to which
`C. bambusicola, C. nongkhaiensis, C. robnettiae,
`
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`74
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`Antonie van Leeuwenhoek (2014) 106:67–84
`
`C. succicola, C. tocantinsensis, C. touchengensis, and
`C. baotianensis may potentially be added based on D1/
`D2 sequence similarity (Nakase et al. 2011a; Groene-
`wald et al. 2011b; Barbosa et al. 2012; Hui et al. 2012).
`Phylogenetic analyses identified 40 species of Candida
`as likely members of the Clavispora clade (Wang et al.
`2008; James et al. 2009; Satoh et al. 2009; Fell et al.
`2011; Groenewald et al. 2011b; Nakase et al. 2011b;
`Ribeiro et al. 2011; Yuan et al. 2012; Cendejas-Bueno
`et al. 2012; Sarawan et al. 2013; James et al. 2013;
`Limtong and Kaewwichian 2013) (Table 2).
`The Kodamaea clade is well recognizable from
`combined D1/D2 LSU and SSU analyses and 16
`species of Candida are members of this clade (Suh and
`Blackwell 2005; Hsieh et al. 2010; Lachance and
`Kurtzman 2011; Nakase et al. 2011c) (Table 2).
`Candida catenulata, C. mesorugosa, C. neorugosa,
`C.
`C. pseudorugosa,
`ranongensis,
`C. rugosa,
`C. savonica, C. scorzettiae, and C. tanticharoeniae
`were shown on common branches in different combi-
`nations based on D1/D2 LSU and these nine species
`may be either members or sisters of Kodamaea (Li
`et al. 2006; Nakase et al. 2010a; Am-In et al. 2011;
`Paredes et al. 2012; Chaves et al. 2013). A similar
`placement was shown for C. catenulata and C. rugosa
`by multigene phylogenetic analyses (Tsui et al. 2008)
`and needs confirmation by multigene analyses with an
`extended taxon sampling.
`The anamorphic genus Aciculoconidium is charac-
`terized by multilateral budding and branched septate
`hyphae that form needle-shaped blastoconidia (Smith
`2011a). The single known species, A. aculeatum, has
`been isolated from fruit flies but not from other
`substrates. An ascosporic state for Aciculoconidium is
`unknown, but phylogenetic analysis places it as a
`neighbor to the genus Kodamaea (Fig. 1, Clade 6).
`Candida litseae1 and C. ontarioensis represent an
`isolated lineage that
`initially appeared somewhat
`closely related to Sporopachydermia based on an
`analysis that included LSU, mtSSU and COX2 (Ku-
`rtzman and Robnett 2007). A new analysis based on
`SSU, D1/D2 LSU, EF1a, RPB1 and RPB2 confirms
`the isolation of these two species, which justified their
`placement in the new genus Danielozyma (Kurtzman
`and Robnett 2014), and also shows them somewhat
`related to Metschnikowiaceae.
`
`1 Spelling corrected according to www.indexfungorum.org
`
`123
`
`Pichiaceae, methanol-assimilating yeasts
`and near relatives
`
`the Pichiaceae (Kregervanrija,
`Three genera of
`Pichia, Saturnispora) form a well-supported group in
`the five-gene analysis, although Dekkera/Brettanomy-
`ces occur in the neighboring methanol-assimilating
`yeasts on a long branch (Fig. 1, Clade 5). The extended
`group of Pichiaceae, methanol-assimilating yeasts and
`their near relatives received variable support (Kurtzman
`and Robnett 2013a). Genera of this group were phylo-
`genetically circumscribed by SSU, LSU, and EF1a gene
`sequences (Kurtzman et al. 2008). The asexual genus
`Brettanomyces was described in 1921, but discovery of
`ascosporulation in certain species resulted in placement
`of those species in the teleomorphic genus Dekkera in
`1964 as dictated by the International Code of Botanical
`Nomenclature, then in force [see Smith (2011b) for
`species characteristics]. Species of Brettanomyces are
`noteworthy for production of acetic acid from glucose, a
`characteristic that markedly shortens longevity in
`culture. Species of the clade often spoil wine, beer,
`and soft drinks, but have more recently been regarded as
`contributors to diversified aromas. Because the name
`Brettanomyces is commonly used in the food and
`beverage industries, the genus name Brettanomyces
`should have priority over Dekkera.
`The genus Nakazawaea is expected to be enlarged
`by C. anatomiae, C. ishiwadae, C. peltata, C. populi,
`and C. wickerhamii according to SSU, LSU, mtSSU,
`and EF1a analyses (Kurtzman 2011). The addition of
`C. laoshanensis, C. molendinolei, C. pomicola and
`C. wyomingensis
`is
`suggested by D1/D2 LSU
`sequences (Lachance et al. 2011). Following the
`genus concept applied by the transfer of various
`Pichia and Williopsis species to Ogataea, the transfer
`of 20 Candida species to Ogataea is expected (Nakase
`et al. 2010b; Kurtzman and Robnett 2010; Koo-
`wadjanakul et al. 2011; Lachance et al. 2011)
`(Table 2). However, the Ogataea clade that formed
`the base for the above genus circumscription was not
`statistically supported. Two supported subclades were
`formed at the exclusion of C. boidinii which had an
`isolated position that became more pronounced by
`using RPB1 and RPB2 instead of mtSSU sequences.
`The Ogataea clade and apparently related Candida
`species need further study before reclassification is
`done. Other Candida species that may be more
`distantly related to Ogataea and Kuraishia include
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`75
`
`C. borneonana, C. cidri, C. hungarica and C. ogatae
`(Pe´ter et al. 2009; Sipiczki 2012).
`In addition,
`C. cylindracea, C. floccosa, and C. pseudocylindra-
`cea are located on long branches basal to the Ogataea
`clade (Lachance et al. 2011; Wang et al. 2009a).
`Candida wuzhishanensis belongs to the Ambro-
`siozyma clade (Wang et al. 2009a).
`Multigene phylogenetic analysis of C. californica,
`C. ethanolica, C. inconspicua, C. pseudolambica, C.
`rugopelliculosa, and C. thaimueangensis placed these
`species in the Pichia clade (Kurtzman et al. 2008),
`whereas C. awuae,2 C. cabralensis, and C. phayaon-
`ensis were added by D1/D2 LSU analyses (Limtong
`et al. 2012c; Flo´rez et al. 2010; Nielsen et al. 2010).
`Candida diversa, C. halmiae, C. sekii, and C. siam-
`ensis appear to be members of the closely related
`genus Saturnispora while Candida sanitii, C. silvae,
`and C. suwanaritii occupied a more basal position in
`the Saturnispora clade (Nielsen et al. 2010; Limtong
`et al. 2010a; Boonmak et al. 2009). Two basal clades
`consisting of (1) C. abiesophila, C. asiatica and (2) C.
`ficus, C. silvatica might represent neighbouring genera
`(Limtong et al. 2010b; Kurtzman 2006).
`
`Phaffomycetaceae
`
`Genera of the Phaffomycetaceae (Komagataella, Pha-
`ffomyces) also include Barnettozyma, Cyberlindnera,
`Phaffomyces, Starmera and Wickerhamomyces based
`on the five-gene analysis (Fig. 1, Clades 2 and 3). The
`Barnettozyma clade
`includes C. norvegica and
`C. montana with minimal support, while D1/D2 LSU
`sequences also indicate C. qinlingensis and C. sanyi-
`ensis as possible members (Liu et al. 2008; Kurtzman
`2011; Lachance et al. 2011). Cyberlindnera includes
`the 13 species listed in Table 2 (Jindamorakot et al.
`2004; Kurtzman et al. 2008; Chang et al. 2012c).
`Phaffomyces includes C. orba and C. coquimbonensis,
`and Wickerhamomyces includes the 10 species listed in
`Table 2 (Cardinali et al. 2012; Nakase et al. 2012;
`Kurtzman et al. 2008; Liu et al. 2008). C. solani took
`different positions in and around the Wickerhamo-
`myces/Cyberlindnera clade depending on datasets.
`The Starmera clade appears to include C. berthetii,
`C. dendrica, C. laemsonensis, and C. stellimalicola
`
`2 Spelling corrected according to www.indexfungorum.org
`
`(Am-In et al. 2011; Kurtzman et al. 2008). Whether the
`basal species C. freyschussii and C. galis belong to the
`Phaffomycetaceae is uncertain (Lachance et al. 2011).
`
`Saccharomycodaceae
`
`Saccharomycodaceae