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Use of Conventional Taxonomy, Electrophoretic Karyotyping and DNA–DNA Hybridization for the Classification of Fermentative Apiculate Yeasts

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Use of Conventional Taxonomy, Electrophoretic Karyotyping and DNA–DNA Hybridization for the Classification of Fermentative Apiculate Yeasts International Journal of Systematic and Evolutionary Microbiology (2000), 50, 1665–1672 Printed in Great Britain Use of conventional taxonomy, electrophoretic karyotyping and DNA–DNA hybridization for the classification of fermentative apiculate yeasts Ann Vaughan-Martini, Paola Angelini and Gianluigi Cardinali Author for correspondence: Ann Vaughan-Martini. Tel: j39 075 585 6479. Fax: j39 075 585 6470. e-mail: avaughan!unipg.it Industrial Yeasts Collection A taxonomic study was conducted that considered strains of the genera (DBVPG), Dipartimento di Hanseniaspora/Kloeckera held in the Industrial Yeasts Collection (DBVPG) of Biologia Vegetale, ' Universita' di Perugia, Sez. the Dipartimento di Biologia Vegetale of the Universita di Perugia, Italy. Microbiologia Applicata, Standard phenotypic as well as molecular criteria were considered in a effort Borgo XX Giugno 74, to revisit the classification of these strains, some of which have been in the 06121 Perugia, Italy collection for about 50 years. Results of salient physiological tests showed that some of the DBVPG and type strains could not be identified by current taxonomic keys. Electrophoretic karyotypes were identical for some species, with the type strains of the seven accepted species showing only five distinct chromosomal patterns. DNA–DNA hybridization analyses, using a non- radioactive dot-blot technique, allowed for the distinction of taxa. The taxonomic implications of these results are discussed. Keywords: Hanseniaspora, conventional and molecular taxonomy, non-radioactive dot-blot DNA reassociation, pulsed-field gel electrophoresis INTRODUCTION confirm sporulation in some strains of Hansenia and therefore assigned it to an anamorphic taxon of The genus Hanseniaspora was created when Klo$ cker fermenting, apiculate yeasts. He then proposed the (1912) described the species Hanseniaspora valbyensis, generic name Hanseniaspora for the perfect taxa. although studies of fermenting, apiculate yeasts began Finally, after a series of incongruences in nomencla- much earlier, in 1870, when Reess designated a non- ture, Hansenia was replaced by the generic name sporulating strain as Saccharomyces apiculatus (Reess, Kloeckeria and then Kloeckera (Janke, 1928). 1870). The years that followed saw many different Over the years, additional apiculate yeasts were de- treatments of the classification and nomenclature of scribed and Hanseniaspora has grown from the original this group of yeasts due to problems experienced by single species described in the first edition of the investigators in the perception of a sexual cycle. monograph The Yeasts: a Taxonomic Study (Lodder In spite of the absence of sporulation, Reess (1870) & Kreger-van Rij, 1952) to the present six recognized probably included S. apiculatus in a perfect genus taxa in the fourth edition (Smith, 1998a). Over the because of its ability to ferment grape must, a trait far same time-period, the genus Kloeckera has been from universal in yeasts. It would not be until 28 years reduced to a single species, Kloeckera lindneri later that Beijerinck (1898) observed sporulation, with (Kloecker) Janke (Janke, 1928; Smith, 1998b), since a direct transformation of the vegetative cell into an studies of molecular taxonomy have demonstrated a ascus containing, according to the author, between high genomic relationship between all of the teleo- four and six ascospores. At that time, it was also morphic and anamorphic forms (Smith et al., 1977; pointed out that S. apiculatus tended to lose sexual Meyer et al., 1978) except for Kloeckera lindneri. capacity with prolonged cultivation. Lindner (1903) The present study set out to reinvestigate some strains also observed a sexual cycle for this species and of the DBVPG Industrial Yeasts Collection classified designated the genus Hansenia, for apiculate yeasts as the most common species of Hanseniaspora\ that form spores. Zikes (1911), however, was unable to Kloeckera involved in grape-must fermentation in ................................................................................................................................................. Italy: Hanseniaspora guilliermondii with its imperfect Abbreviation: PFGE, pulsed-field gel electrophoresis. form Kloeckera apis, Hanseniaspora osmophila (ana- 01388 # 2000 IUMS 1665 A. Vaughan-Martini, P. Angelini and G. Cardinali morphs Kloeckera corticis and Kloeckera magna), 1% peptone, 2% glucose) equilibrated in a water bath. An Hanseniaspora uvarum (Kloeckera apiculata) and effort to induce a sexual cycle was made following current Hanseniaspora vineae with Kloeckera africana. The recommendations (Smith, 1998a). DBVPG collection holds over 150 strains belonging to Preparation and analysis of nuclear DNA this group that have been isolated from various Pulsed-field gel electrophoresis (PFGE). Intact chromosomal substrates over a period of about 50 years. Since the DNA for PFGE was prepared as reported previously separation of these taxa is sometimes difficult, es- (Cardinali et al., 1995). Gels composed of 1% agarose (type pecially in the absence of a sexual cycle, it was deemed II-A, medium EEO; Sigma) were analysed using a CHEF necessary to confirm the original designations of some Mapper or DRII (Bio-Rad) with 0n5iTBE buffer. A of these strains by employing the most recent con- temperature of 12–15 mC was maintained throughout the ventional criteria (Smith, 1998a, b) together with runs and the parameters of the electrophoresis are described methods of molecular taxonomy. in the figure legends. Hybridization experiments. DNA extraction and hydroxy- METHODS apatite (HTP; Bio-Rad) purification were performed ac- cording to the protocol proposed by Cardinali et al. (2000). Organisms. The strains studied are listed in Table 1. Type DNA–DNA hybridization experiments were performed strains of the perfect and imperfect species were kindly using a dot-blot procedure where probe DNA was labelled provided by the yeast division of the Centraalbureau voor using the ECL-Direct non-radioactive procedure (Amer- Schimmelcultures (CBS), Delft, The Netherlands. sham) following the manufacturer’s instructions. Pre- Physiological studies. Growth responses on sole carbon and hybridization, hybridization and high-stringency washes nitrogen sources, as well as resistance to cycloheximide (0n5% NaCl) were all carried out at 42 mC. (actidione), were determined in liquid medium on a roller Densitometric analysis of the DNA–DNA hybridizations. X-ray film drum at 25 mC by using the methods described by Yarrow (Kodak X-OMAT; Sigma) was exposed for 1, 2, 5 or 15 min (1998). Maximum growth temperatures were determined by according to the intensity of the signal. Only non-saturated using static cultures containing YEPG (1% yeast extract, films were subjected to further analysis. Table 1. DBVPG isolates examined in the present study Strain Species or original epithet Source Date of deposit 3062 Hanseniaspora apuliensis Castelli Grape must; Israel 1950 3094 Kloeckera apiculata Wine; Trentino, Italy 1951 3096 Kloeckera magna Sweet filtered wine; Brindisi, Italy 1951 3272 Kloeckera apiculata Grape must; Calabria, Italy 1952 3280 Kloeckera apiculata Soil; The Netherlands 1952 3298 Kloeckera africana Wine; Capoterra (Sardinia), Italy 1952 3447 Kloeckera apiculata Milk; Perugia, Italy 1955 3539 Kloeckera apiculata Flowers; Perugia, Italy 1955 3542 Kloeckera apiculata Soil; Puerto Lapiche, Spain 1955 3543 Kloeckera magna Grapes; Cerro del Moro (La 1955 Mancha), Spain 3582 Kloeckera apiculata Grapes; Fuen Mayor (Rioja), Spain 1956 4033 Kloeckera magna Cavern; Italy 1963 4059 Kloeckera magna Grape must; Slovenia 1968 4159 Kloeckera magna Grape must; Slovenia 1968 4160 Kloeckera magna Grape must; Slovenia 1968 4351 Kloeckera apiculata Sea water; Italy 1994 6717T Pseudosaccharomyces apiculatus (Reess) Klo$ cker Unknown 1993 6718T Hanseniaspora uvarum (Niehaus) Shehata et al. Muscatelle grapes; Ukraine 1990 6774T Hanseniaspora valbyensis Klo$ cker Soil; Denmark 1993 6790T Kloeckera apis Lavie ex M. T. Smith et al. Trachea of bee; France 1993 6791T Kloeckera corticis (Klo$ cker) Janke Bark of tree; Denmark 1993 6792T Kloeckera africana (Klo$ cker) Janke Soil; Algeria 1993 6793T Kloeckera japonica Saito & Otani Sap of tree; Japan 1993 6794T Pseudosaccharomyces javanicus Klo$ cker Soil; Java 1993 6795T Hanseniaspora osmophila (Niehaus) Phaff et al. ex M. Th. Smith Ripe Reisling grapes; Germany 1993 6796T Hanseniaspora guilliermondii Pijper Infected nail; South Africa 1993 6797T Hanseniaspora vineae van der Walt & Tscheuschner Soil of vineyard; South Africa 1993 6798T Hanseniaspora occidentalis M. T. Smith Soil; West Indies 1993 7132T Kloeckera lindneri (Klo$ cker) Janke Soil; Java 1998 1666 International Journal of Systematic and Evolutionary Microbiology 50 A taxonomic treatment of fermentative apiculate yeasts A calibration curve was obtained by plotting the values of repeated the assimilative patterns observed at the time serial probe dilutions against the corresponding signals of the original species designation. According to the expressed as grey levels (according to a 256-level system). A most recent criteria for the classification of the genera regression equation was used to calculate the reassociation Hanseniaspora\Kloeckera (Smith, 1998a, b), all strains level of each sample. Video densitometric analysis was originally classified as Kloeckera apiculata, as well as carried out using the free-domain software NIH 1.62b and densitometric data were processed with the type strains of Hanseniaspora
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