Abstract
Yeasts of the Pichia genus have been isolated from different natural environments. Phylogenies based on multigene sequence analysis have shown that the genus is polyphyletic. Some species of this genus are member of the CTG group. In order to have a better insight into the relationship among species assigned to the yeast genera Pichia into the CTG group, we first sequenced the mitochondrial genome of the osmotolerant yeast Pichia farinosa. We then compared this genome with mitochondrial genomes of yeasts of the CTG group. The P. farinosa mitochondrial DNA is a circular-mapping genome of 32,065 bp, which contains 43 genes transcribed from both strands. It contains a complete set of tRNAs, the small and the large rRNAs, as well as 14 protein-coding genes. Yeasts of the CTG group contain the same core of mitochondrial genes. Phylogenetic analysis based on mitochondrial sequences clearly shows that the CTG group is divided into two distinct clades: the first one contains diploid Candida species, whereas the second mainly contains haploid Pichia species. Moreover, this analysis provides clear evidence that Pichia farinosa and Pichia sorbitophila, which were known to be unique species, are two distinct species.
Similar content being viewed by others
Abbreviations
- Mt:
-
Mitochondrial
References
Adler A, Hidalgo-Grass C, Boekhout T, Theelen B, Sionov E, Polacheck I (2007) Pichia farinosa bloodstream infection in a lymphoma patient. J Clin Microbiol 45:3456–3458
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anderson JB, Wickens C, Khan M, Cowen LE, Federspiel N, Jones T, Kohn LM (2001) Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J Bacteriol 183:865–872
Bakir M, Cerikcioğlu N, Tirtir A, Berrak S, Ozek E, Canpolat C (2004) Pichia anomala fungaemia in immunocompromised children. Mycoses 47:231–235
Butler G, Rasmussen MD, Lin MF, Santos MAS, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy J-L, Agrafioti I, Arnaud M-B, Bates S, Brown AJP, Brunke S, Costanzo MC, Fitzpatrick DA, de Groot PWJ, Harris D, Hoyer LL et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657–662
Chevalier BS, Stoddard BL (2001) Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Res 29:3757–3774
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J, Guindon S, Lefort V, Lescot M et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469
Dujon B (2010) Yeast evolutionary genomics. Nat Rev Genet 11:512–524
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113
Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99
Foury F, Roganti T, Lecrenier N, Purnelle B (1998) The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett 440:325–331
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Haugen P, Simon DM, Bhattacharya D (2005) The natural history of group I introns. Trends Genet 21:111–119
Jacquier A, Dujon B (1983) The intron of the mitochondrial 21S rRNA gene: distribution in different yeast species and sequence comparison between Kluyveromyces thermotolerans and Saccharomyces cerevisiae. Mol Gen Genet 192:487–499
Jeffries TW (2006) Engineering yeasts for xylose metabolism. Curr Opin Biotechnol 17:320–326
Jeffries TW, Grigoriev IV, Grimwood J, Laplaza JM, Aerts A, Salamov A, Schmutz J, Lindquist E, Dehal P, Shapiro H, Jin Y, Passoth V, Richardson PM (2007) Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis. Nat Biotechnol 25:319–326
Jung PP, Schacherer J, Souciet JL, Potier S, Wincker P, de Montigny J (2009) The complete mitochondrial genome of the yeast Pichia sorbitophila. FEMS Yeast Res 9:903–910
Kerscher S, Durstewitz G, Casaregola S, Gaillardin C, Brandt U (2001) The complete mitochondrial genome of Yarrowia lipolytica. Comp Funct Genomics 2:80–90
Knight RD, Landweber LF, Yarus M (2001) How mitochondria redefine the code. J Mol Evol 53:299–313
Kosa P, Valach M, Tomaska L, Wolfe KH, Nosek J (2006) Complete DNA sequences of the mitochondrial genomes of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis: insight into the evolution of linear DNA genomes from mitochondrial telomere mutants. Nucleic Acids Res 34:2472–2481
Koszul R, Malpertuy A, Frangeul L, Bouchier C, Wincker P, Thierry A, Duthoy S, Ferris S, Hennequin C, Dujon B (2003) The complete mitochondrial genome sequence of the pathogenic yeast Candida (Torulopsis) glabrata. FEBS Lett 534:39–48
Kurtzman CP, Fell JW (1998) The yeasts, a taxonomic study, 4th edn. Elsevier, Amsterdam
Kurtzman CP, Robnett CJ (2003) Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Res 3:417–432
Kurtzman CP, Suzuki M (2010) Phylogenetic analysis of ascomycete yeasts that form coenzyme Q-9 and the proposal of the new genera Babjeviella, Meyerozyma, Millerozyma, Priceomyces, and Scheffersomyces. Mycoscience 51:2–14
Lang BF, Laforest M, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23:119–125
Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172–175
Leandro MJ, Gonçalves P, Spencer-Martins I (2006) Two glucose/xylose transporter genes from the yeast Candida intermedia: first molecular characterization of a yeast xylose-H+ symporter. Biochem J 395:543–549
Li R, Yu C, Li Y, Lam T, Yiu S, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Maresová L, Sychrová H (2003) Physiological characterization of osmotolerant yeast Pichia sorbitophila and comparison with a putative synonym Pichia farinosa. Folia Microbiol 48:211–217
Nobre A, Lucas C, Leão C (1999) Transport and utilization of hexoses and pentoses in the halotolerant yeast Debaryomyces hansenii. Appl Environ Microbiol 65:3594–3598
Nosek J, Novotna M, Hlavatovicova Z, Ussery DW, Fajkus J, Tomaska L (2004) Complete DNA sequence of the linear mitochondrial genome of the pathogenic yeast Candida parapsilosis. Mol Genet Genomics 272:173–180
Ohama T, Suzuki T, Mori M, Osawa S, Ueda T, Watanabe K, Nakase T (1993) Non-universal decoding of the leucine codon CUG in several Candida species. Nucleic Acids Res 21:4039–4045
Rodriques de Miranda L, Appel KR, Seyfarth H (1980) Pichia sorbitophila sp. nov. Antonie Van Leeuwenhoek 46:157–159
Sacerdot C, Casaregola S, Lafontaine I, Tekaia F, Dujon B, Ozier-Kalogeropoulos O (2008) Promiscuous DNA in the nuclear genomes of hemiascomycetous yeasts. FEMS Yeast Res 8:846–857
Santos MA, Tuite MF (1995) The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res 23:1481–1486
Schäfer B (2005) RNA maturation in mitochondria of S. pombe. Gene 354:80–85
Sekito T, Okamoto K, Kitano H, Yoshida K (1995) The complete mitochondrial DNA sequence of Hansenula wingei reveals new characteristics of yeast mitochondria. Curr Genet 28:39–53
Talla E, Anthouard V, Bouchier C, Frangeul L, Dujon B (2005) The complete mitochondrial genome of the yeast Kluyveromyces thermotolerans. FEBS Lett 579:30–40
Tsui CKM, Daniel H, Robert V, Meyer W (2008) Re-examining the phylogeny of clinically relevant Candida species and allied genera based on multigene analyses. FEMS Yeast Res 8:651–659
Valach M, Tomaska L, Nosek J (2008) Preparation of yeast mitochondrial DNA for direct sequence analysis. Curr Genet 54:105–109
Acknowledgments
We thank Thomas Jeffries for providing us the mitochondrial sequence of Pichia stipitis. We are very grateful to Irwin Davidson, Bernard Jost, and Stéphanie Legras from the IGBMC Microarray and Sequencing Platform. We also thank Jean-Marc Aury for assistance in computational analysis. This work was supported in part by the Génolevures Consortium GDR 2354. JPP is supported by a grant from the French “Ministère de l’Enseignement Supérieur et de la Recherche”. JS was supported by a CNRS PEPS 2009 grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L. Tomaska.
J. de Montigny and J. Schacherer contributed equally to this work.
Accession number: the sequence has been deposited in EMBL under accession number FN870377.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jung, P.P., Friedrich, A., Souciet, JL. et al. Complete mitochondrial genome sequence of the yeast Pichia farinosa and comparative analysis of closely related species. Curr Genet 56, 507–515 (2010). https://doi.org/10.1007/s00294-010-0318-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-010-0318-y