Phylogeny and Evolution of Medical Species of Candida and Related Taxa: a Multigenic Analysis

ABSTRACT Hemiascomycetes are species of yeasts within the order Saccharomycetales. The order encompasses disparate genera with a variety of life styles, including opportunistic human pathogens (e.g., Candida albicans), plant pathogens (e.g., Eremothecium gossypii), and cosmopolitan yeasts associated with water and decaying vegetation. To analyze the phylogeny of medically important species of yeasts, we selected 38 human pathogenic and related strains in the order Saccharomycetales. The DNA sequences of six nuclear genes were analyzed by maximum likelihood and Bayesian phylogenetic methods. The maximum likelihood analysis of the combined data for all six genes resolved three major lineages with significant support according to Bayesian posterior probability. One clade was mostly comprised of pathogenic species of Candida. Another major group contained members of the family Metschnikowiaceae as a monophyletic group, three species of Debaryomyces, and strains of Candida guilliermondii. The third clade consisted exclusively of species of the family Saccharomycetaceae. Analysis of the evolution of key characters indicated that both codon reassignment and coenzyme Q9 likely had single origins with multiple losses. Tests of correlated character evolution revealed that these two traits evolved independently.

[1]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[2]  R. Kuykendall,et al.  Nucleotide sequence analysis of the 5·8S rDNA and adjacent ITS2 region of Candida albicans and related species , 1993, Yeast.

[3]  K. Kjer,et al.  Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. , 1995, Molecular phylogenetics and evolution.

[4]  K. Kondo,et al.  Coenzyme Q system in the classification of the ascosporogenous yeast genera Debaryomyces, Saccharomyces, Kluyveromyces, and Endomycopsis. , 1976 .

[5]  P. Kozinn,et al.  Candida and candidiasis. , 1971, JAMA.

[6]  F. Kauff,et al.  Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. , 2002, Molecular phylogenetics and evolution.

[7]  C. Kurtzman.  Molecular taxonomy of the yeasts , 1994, Yeast.

[8]  T. Sugita,et al.  Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. , 1999, Systematic and applied microbiology.

[9]  K. Yokoyama,et al.  Identification and Phylogenetic Relationship of the Most Common Pathogenic Candida Species Inferred from Mitochondrial Cytochrome b Gene Sequences , 2000, Journal of Clinical Microbiology.

[10]  H. Nishida,et al.  Archiascomycetes: detection of a major new lineage within the Ascomycota , 1994 .

[11]  Joost A. Stalpers,et al.  Ainsworth and Bisby's dictionary of the fungi: 9th edition. , 1995 .

[12]  Pedro Beltrão,et al.  Comparative evolutionary genomics unveils the molecular mechanism of reassignment of the CTG codon in Candida spp. , 2003, Genome research.

[13]  Sudhir Kumar,et al.  MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers , 1994, Comput. Appl. Biosci..

[14]  B. Hall,et al.  Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. , 1999, Molecular biology and evolution.

[15]  P. Lewis.  A likelihood approach to estimating phylogeny from discrete morphological character data. , 2001, Systematic biology.

[16]  G. Serio,et al.  A new method for calculating evolutionary substitution rates , 2005, Journal of Molecular Evolution.

[17]  T. Jukes.  CHAPTER 24 – Evolution of Protein Molecules , 1969 .

[18]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[19]  D. Schluter,et al.  LIKELIHOOD OF ANCESTOR STATES IN ADAPTIVE RADIATION , 1997, Evolution; international journal of organic evolution.

[20]  T. Lott,et al.  Sequence Analysis of the Internal Transcribed Spacer 2 (ITS2) from Yeast Species Within the Genus Candida , 1998, Current Microbiology.

[21]  J. Oliver,et al.  The general stochastic model of nucleotide substitution. , 1990, Journal of theoretical biology.

[22]  M. Pagel.  Inferring the historical patterns of biological evolution , 1999, Nature.

[23]  K. Hazen,et al.  New and emerging yeast pathogens , 1995, Clinical microbiology reviews.

[24]  M. Pagel.  Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  M. Sogin,et al.  Evolutionary relationships among pathogenic Candida species and relatives , 1991, Journal of bacteriology.

[26]  J. W. Taylor,et al.  Detecting morphological convergence in true fungi, using 18S rRNA gene sequence data. , 1992, Bio Systems.

[27]  F. Corpet.  Multiple sequence alignment with hierarchical clustering. , 1988, Nucleic acids research.

[28]  Wayne P. Maddison,et al.  Macclade: Analysis of Phylogeny and Character Evolution/Version 3 , 1992 .

[29]  C. Kurtzman,et al.  Phylogenetic relationships among yeasts of the 'Saccharomyces complex' determined from multigene sequence analyses. , 2003, FEMS yeast research.

[30]  C. Kurtzman,et al.  Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5' end of the large-subunit (26S) ribosomal DNA gene , 1997, Journal of clinical microbiology.

[31]  T. Bruns,et al.  ITS primers with enhanced specificity for basidiomycetes ‐ application to the identification of mycorrhizae and rusts , 1993, Molecular ecology.

[32]  T. Kanbe,et al.  Phylogenetic relationship and mode of evolution of yeast DNA topoisomerase II gene in the pathogenic Candida species. , 2001, Gene.

[33]  Gabriela R. Moura,et al.  Yeast as a model organism for studying the evolution of non-standard genetic codes. , 2004, Briefings in functional genomics & proteomics.

[34]  Hiroshi Honda,et al.  The codon CUG is read as serine in an asporogenic yeast Candida cylindracea , 1989, Nature.

[35]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[36]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[37]  T. White.  Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[38]  C. Kurtzman,et al.  Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences , 1998, Antonie van Leeuwenhoek.

[39]  J. Felsenstein.  Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[40]  H. Kishino,et al.  Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea , 1989, Journal of Molecular Evolution.

[41]  R. Moore.  The Yeasts, A Taxonomic Study, 4th edn., C.P. Kurtzman, J.W. Fell (Eds.). Elsevier, Amsterdam (1998), xviii, Price Hfl 800 (Euros 363; $460). , 2000 .

[42]  M. Rinaldi,et al.  Three distinct genotypes within Candida parapsilosis from clinical sources , 1995, Journal of clinical microbiology.

[43]  H. Daniel,et al.  Partial sequence analysis of the actin gene and its potential for studying the phylogeny of Candida species and their teleomorphs. , 2001, International journal of systematic and evolutionary microbiology.

[44]  Thomas J. White,et al.  PCR protocols: a guide to methods and applications. , 1990 .

[45]  Nan Yu,et al.  The Comparative RNA Web (CRW) Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs , 2002, BMC Bioinformatics.

[46]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[47]  S. Tavaré.  Some probabilistic and statistical problems in the analysis of DNA sequences , 1986 .

[48]  M. Pagel.  The Maximum Likelihood Approach to Reconstructing Ancestral Character States of Discrete Characters on Phylogenies , 1999 .