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Phylogenetic Placement of Hanseniaspora– Kloeckera Species

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Phylogenetic Placement of Hanseniaspora– Kloeckera Species International Journal of Systematic and Evolutionary Microbiology (2006), 56, 1157–1165 DOI 10.1099/ijs.0.64052-0 Phylogenetic placement of Hanseniaspora– Kloeckera species using multigene sequence analysis with taxonomic implications: descriptions of Hanseniaspora pseudoguilliermondii sp. nov. and Hanseniaspora occidentalis var. citrica var. nov. Neza Cadez,1 Peter Raspor1 and Maudy Th. Smith2 Correspondence 1University of Ljubljana, Biotechnical Faculty, Department of Food Science and Technology, Neza Cadez Jamnikarjeva 101, 1000 Ljubljana, Slovenia [email protected] 2Centraalbureau voor Schimmelcultures, PO Box 85167, 3508 AD Utrecht, The Netherlands Two protein-coding genes, actin and translation elongation factor-1a (EF-1a), as well as two ribosomal gene regions, D1/D2 domains of the large subunit and both internal transcribed spacers including the 5?8S gene region, were evaluated regarding their usefulness for reconstruction of phylogenetic relationships in the Hanseniaspora–Kloeckera species group. This included analyses of sequence divergence values, heterogeneity of evolutionary rates and the reliability of the inferred trees. Both protein-coding genes showed greater capacities to resolve at the strain level and between the closely related species of Hanseniaspora–Kloeckera, compared with the ribosomal gene regions. However, to obtain a fully resolved and reliable phylogenetic tree that reflected the biological relationships it was necessary to combine three congruent sequence datasets. The novel species Hanseniaspora pseudoguilliermondii sp. nov. (type strain CBS 8772T) is described as a result of the application of various molecular approaches to delimit species. Furthermore, incongruent gene genealogies of genetically divergent strains of Hanseniaspora occidentalis, as determined by amplified fragment length polymorphism analysis and DNA–DNA reassociation measurements, indicated the presence of two novel varieties, H. occidentalis var. occidentalis (type strain CBS 2592T) and H. occidentalis var. citrica var. nov. (type strain CBS 6783T), which could be distinguished by habitat preference. INTRODUCTION Saccharomyces apiculatus (Reess, 1870). The unstable ability of these yeasts to form ascospores contributed to several The name Hanseniaspora was proposed for ascosporo- changes in nomenclature and definition of the genus genous apiculate yeasts by Zikes (1911), although their (Lodder & Kreger-van Rij, 1952). With the introduction common presence in fruit juices and fermenting musts of molecular taxonomy, relationships between the species had already led to the description of the apiculate species of Hanseniaspora and of the anamorphic genus Kloeckera were established on the basis of DNA base composition (Nakase & Komagata, 1970) and DNA–DNA relatedness Abbreviations: AFLP, amplified fragment length polymorphism; EF-1a, (Meyer et al., 1978). The latter study represents the basis for translation elongation factor-1a; ITS, internal transcribed spacer; LSU, the current classification, which was confirmed by several large subunit; RAPD, randomly amplified polymorphic DNA. phylogenetic studies based on different parts of the ribo- The GenBank/EMBL/DDBJ accession numbers for the gene somal gene and two protein-coding genes (Yamada et al., sequences determined in this study are listed in Table 1. 1992a; Boekhout et al., 1994; Esteve-Zarzoso et al., 2001; Figures showing saturation plots and phylogenetic analyses of Kurtzman & Robnett, 2003). The genus Hanseniaspora cur- sequences of actin and EF-1a genes and the D1/D2 regions of the rently comprises ten species, four of which (Hanseniaspora Hanseniaspora–Kloeckera LSU rDNA and ITS regions of strains, and meyeri, Hanseniaspora clermontiae, Hanseniaspora lachancei tables comparing dataset characteristics and characteristics inferred from the datasets using maximum-parsimony analyses and DNA–DNA and Hanseniaspora opuntiae) were recently circumscribed relatedness values among strains of Hanseniaspora occidentalis are on the basis of DNA–DNA reassociation data (Smith, 1998; available as supplementary material in IJSEM Online. Cadez et al., 2003). 64052 G 2006 IUMS Printed in Great Britain 1157 N. Cadez, P. Raspor and M. Th. Smith Phylogenetic placement of members of Hanseniaspora DNA extraction, amplification and sequencing. DNA was iso- within the Saccharomyces clade revealed that the genus is lated from cultures grown on yeast-malt agar (0?3 % yeast extract, divided into two clusters (Kurtzman & Robnett, 1998, 0?3 % malt extract, 0?5 % peptone, 1 % glucose, 2 % agar), according to the method of Mo¨ller et al. (1992). 2003). The first cluster contains the species Hanseniaspora vineae, Hanseniaspora osmophila and Hanseniaspora occi- PCR primers for the amplification of actin and EF-1a protein-coding dentalis. Strains belonging to the latter species were found to regions were designed based on sequences of Saccharomyces cerevisiae be heterogeneous with respect to their randomly amplified (GenBank accession numbers NC_001138 and U51033, respectively). polymorphic DNA (RAPD) profiles, electrophoretic karyo- Additional primers were designed from generated sequences of the types and restriction patterns of the internal transcribed actin gene of H. vineae (Act-HV) and the EF-1a gene of H. meyeri (EF1- HM). Primer sequences, annealing temperatures and annealing sites spacer (ITS) regions (Cadez et al., 2002). The second cluster and references are given in Table 2. comprises Hanseniaspora valbyensis and four recently described species that are closely related to Hanseniaspora Amplifications were performed under the following conditions: an uvarum and Hanseniaspora guilliermondii (Cadez et al., initial denaturing step of 5 min at 94 uC, followed by 35 cycles of 30 s at 2003). The poorly resolved rDNA-based phylogenetic tree 94 uC, 30 s at primer-pair-specific annealing temperatures (Table 2), 2 min at 72 C and termination with a final extension step of 7 min at suggested that there were very close relationships among u 72 uC. The PCR products were purified using GenElute PCR Clean-up species of the H. uvarum–H. guilliermondii complex, which (Sigma–Aldrich), according to the manufacturer’s instructions. The was not in agreement with the genetic relatedness deter- pGEM-T vector system was used to clone the PCR products of the mined by DNA–DNA reassociation analyses (Cadez et al., protein-coding genes, following the procedure described in the manual 2003). This supports the observation that the relationships (Promega). Plasmid DNA was isolated and purified for subsequent between recently diverged species complexes are difficult to sequencing by using GenElute Plasmid Minipreps (Sigma–Aldrich). resolve on the basis of a single gene only (Rokas et al., 2003). Nucleotide sequences were determined in both directions by using a Thermo Sequenase Primer Cycle sequencing kit (Amersham Bio- Several studies have demonstrated the phylogenetic useful- sciences) and labelled universal primers M13(210) or M14R with an ALFexpress II Automatic DNA Sequencer (Amersham Pharmacia ness of protein-coding genes for inferring relationships Biotech). The D1/D2 regions of the large subunit (LSU) rDNA and ITS among different taxonomic units (Baldauf et al., 2000; regions were sequenced as described previously (Cadez et al., 2003). Daniel et al., 2001; Belloch et al., 2000; O’Donnell et al., Sequences of both strands were aligned and edited with the ALFwin 1998). Housekeeping genes such as translation elongation Sequence Analyser 2.10.06 software (Amersham Pharmacia Biotech). factor-1a (EF-1a) and actin are frequently used as indepen- dently evolving markers because they do not appear to Phylogenetic analyses. The number of variable and parsimony- have undergone horizontal transfer or gene duplication. informative sites, the genomic DNA G+C contents and the mean Moreover, the rates of sequence substitutions in exons are uncorrected sequence divergences between the groups of taxa were constrained by codon positions, which may determine the calculated using the computer program MEGA 2.1 (Kumar et al., taxonomic level of analysis (Baldauf & Palmer, 1993; Kretzer 2001). & Bruns, 1999). Sequences were aligned automatically using the multiple sequence alignment program CLUSTAL X version 1.83 (Thompson et al., 1997). Because the species of Hanseniaspora–Kloeckera fall into Positions where gaps existed in one of the sequences were manually several groups of closely related taxa separated by large excluded using BioEdit (Hall, 1999). All subsequent phylogenetic phylogenetic distances (Cadez et al., 2003), the phylogenetic analyses employed the PAUP* 4.0b10 software package (Swofford, marker for resolving Hanseniaspora–Kloeckera species 2002). Most-parsimonious trees were generated by a heuristic search should have both the capacity to resolve the sister species procedure with 1000 random addition replicates and tree bisection– and the potential to realistically reconstruct the phylogeny reconnection branch swapping. Nucleotide sites were equally weighted. between the divergent lineages. Consequently, the aim of The stability of the branches was assessed by bootstrap analysis (Felsenstein, 1985) in which 1000 replicates were used. The homo- the study was to assess the phylogenetic usefulness of four geneity of the signal from the four datasets was tested with partition- phylogenetic markers by describing sequence divergence homogeneity tests (Farris et al., 1995) implemented in PAUP* 4.0b10 and by comparing the inter- and intraspecific
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