Evolution of pathogenicity and sexual reproduction in eight Candida genomes

Geraldine Butler; Matthew D. Rasmussen; Michael F. Lin; Manuel A.S. Santos; Sharadha Sakthikumar; Carol A. Munro; Esther Rheinbay; Manfred Grabherr; Anja Forche; Jennifer L. Reedy; Ino Agrafioti; Martha B. Arnaud; Steven Bates; Alistair J.P. Brown; Sascha Brunke; Maria C. Costanzo; David A. Fitzpatrick; Piet W.J. De Groot; David Harris; Lois L. Hoyer; Bernhard Hube; Frans M. Klis; Chinnappa Kodira; Nicola Lennard; Mary E. Logue; Ronny Martin; Aaron M. Neiman; Elissavet Nikolaou; Michael A. Quail; Janet Quinn; Maria C. Santos; Florian F. Schmitzberger; Gavin Sherlock; Prachi Shah; Kevin A.T. Silverstein; Marek S. Skrzypek; David Soll; Rodney Staggs; Ian Stansfield; Michael P.H. Stumpf; Peter E. Sudbery; Thyagarajan Srikantha; Qiandong Zeng; Judith Berman; Matthew Berriman; Joseph Heitman; Neil A.R. Gow; Michael C. Lorenz; Bruce W. Birren; Manolis Kellis

doi:10.1038/nature08064

Evolution of pathogenicity and sexual reproduction in eight Candida genomes

Geraldine Butler, Matthew D. Rasmussen, Michael F. Lin, Manuel A.S. Santos, Sharadha Sakthikumar, Carol A. Munro, Esther Rheinbay, Manfred Grabherr, Anja Forche, Jennifer L. Reedy, Ino Agrafioti, Martha B. Arnaud, Steven Bates, Alistair J.P. Brown, Sascha Brunke, Maria C. Costanzo, David A. Fitzpatrick, Piet W.J. De Groot, David Harris, Lois L. HoyerBernhard Hube, Frans M. Klis, Chinnappa Kodira, Nicola Lennard, Mary E. Logue, Ronny Martin, Aaron M. Neiman, Elissavet Nikolaou, Michael A. Quail, Janet Quinn, Maria C. Santos, Florian F. Schmitzberger, Gavin Sherlock, Prachi Shah, Kevin A.T. Silverstein, Marek S. Skrzypek, David Soll, Rodney Staggs, Ian Stansfield, Michael P.H. Stumpf, Peter E. Sudbery, Thyagarajan Srikantha, Qiandong Zeng, Judith Berman, Matthew Berriman, Joseph Heitman, Neil A.R. Gow, Michael C. Lorenz, Bruce W. Birren, Manolis Kellis

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Abstract

Candida species are the most common cause of opportunistic fungal infection worldwide. Here we report the genome sequences of six Candida species and compare these and related pathogens and non-pathogens. There are significant expansions of cell wall, secreted and transporter gene families in pathogenic species, suggesting adaptations associated with virulence. Large genomic tracts are homozygous in three diploid species, possibly resulting from recent recombination events. Surprisingly, key components of the mating and meiosis pathways are missing from several species. These include major differences at the mating-type loci (MTL); Lodderomyces elongisporus lacks MTL, and components of the a1/α2 cell identity determinant were lost in other species, raising questions about how mating and cell types are controlled. Analysis of the CUG leucine-to-serine genetic-code change reveals that 99% of ancestral CUG codons were erased and new ones arose elsewhere. Lastly, we revise the Candida albicans gene catalogue, identifying many new genes.

Original language	English (US)
Pages (from-to)	657-662
Number of pages	6
Journal	Nature
Volume	459
Issue number	7247
DOIs	https://doi.org/10.1038/nature08064
State	Published - Jun 4 2009

Bibliographical note

Funding Information:
Acknowledgements We thank the US National Human Genome Research Institute (NHGRI) for support under the Fungal Genome Initiative at the Broad Institute. We thank C. Kurtzman for providing the sequenced strains of L. elongisporus, C. guilliermondii and C. lusitaniae, M. Koehrsen for Broad Institute website support, D. Park for informatics support and K. Wolfe and A. Regev for comments on the manuscript. We acknowledge the contributions of the Broad Institute Sequencing Platform and A. Barron, L. Clark, C. Corton, D. Ormond, D. Saunders, K. Seeger and R. Squares from the Wellcome Trust Sanger Institute for the C. parapsilosis sequencing and assembly. N.A.R.G., A.J.P.B., M.B. and co-workers were supported by the Wellcome Trust; M.G., S.S., Q.Z., C.K., B.W.B. and C.A.C. were supported by NHGRI and the National Institute of Allergy and Infectious Disease, US National Institutes of Health (NIH), Department of Health and Human Services; G.B. and co-workers were supported by Science Foundation Ireland; J.B., A.F., J.H., A.M.N. and co-workers were supported by the NIH; and M.K., M.D.R. and M.F.L. by the NIH, the US National Science Foundation and the Sloan Foundation.

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Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A. S., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., Agrafioti, I., Arnaud, M. B., Bates, S., Brown, A. J. P., Brunke, S., Costanzo, M. C., Fitzpatrick, D. A., De Groot, P. W. J., Harris, D., ... Kellis, M. (2009). Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, 459(7247), 657-662. https://doi.org/10.1038/nature08064

Butler, G, Rasmussen, MD, Lin, MF, Santos, MAS, Sakthikumar, S, Munro, CA, Rheinbay, E, Grabherr, M, Forche, A, Reedy, JL, Agrafioti, I, Arnaud, MB, Bates, S, Brown, AJP, Brunke, S, Costanzo, MC, Fitzpatrick, DA, De Groot, PWJ, Harris, D, Hoyer, LL, Hube, B, Klis, FM, Kodira, C, Lennard, N, Logue, ME, Martin, R, Neiman, AM, Nikolaou, E, Quail, MA, Quinn, J, Santos, MC, Schmitzberger, FF, Sherlock, G, Shah, P, Silverstein, KAT, Skrzypek, MS, Soll, D, Staggs, R, Stansfield, I, Stumpf, MPH, Sudbery, PE, Srikantha, T, Zeng, Q, Berman, J, Berriman, M, Heitman, J, Gow, NAR, Lorenz, MC, Birren, BW & Kellis, M 2009, 'Evolution of pathogenicity and sexual reproduction in eight Candida genomes', Nature, vol. 459, no. 7247, pp. 657-662. https://doi.org/10.1038/nature08064

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title = "Evolution of pathogenicity and sexual reproduction in eight Candida genomes",

abstract = "Candida species are the most common cause of opportunistic fungal infection worldwide. Here we report the genome sequences of six Candida species and compare these and related pathogens and non-pathogens. There are significant expansions of cell wall, secreted and transporter gene families in pathogenic species, suggesting adaptations associated with virulence. Large genomic tracts are homozygous in three diploid species, possibly resulting from recent recombination events. Surprisingly, key components of the mating and meiosis pathways are missing from several species. These include major differences at the mating-type loci (MTL); Lodderomyces elongisporus lacks MTL, and components of the a1/α2 cell identity determinant were lost in other species, raising questions about how mating and cell types are controlled. Analysis of the CUG leucine-to-serine genetic-code change reveals that 99% of ancestral CUG codons were erased and new ones arose elsewhere. Lastly, we revise the Candida albicans gene catalogue, identifying many new genes.",

author = "Geraldine Butler and Rasmussen, {Matthew D.} and Lin, {Michael F.} and Santos, {Manuel A.S.} and Sharadha Sakthikumar and Munro, {Carol A.} and Esther Rheinbay and Manfred Grabherr and Anja Forche and Reedy, {Jennifer L.} and Ino Agrafioti and Arnaud, {Martha B.} and Steven Bates and Brown, {Alistair J.P.} and Sascha Brunke and Costanzo, {Maria C.} and Fitzpatrick, {David A.} and {De Groot}, {Piet W.J.} and David Harris and Hoyer, {Lois L.} and Bernhard Hube and Klis, {Frans M.} and Chinnappa Kodira and Nicola Lennard and Logue, {Mary E.} and Ronny Martin and Neiman, {Aaron M.} and Elissavet Nikolaou and Quail, {Michael A.} and Janet Quinn and Santos, {Maria C.} and Schmitzberger, {Florian F.} and Gavin Sherlock and Prachi Shah and Silverstein, {Kevin A.T.} and Skrzypek, {Marek S.} and David Soll and Rodney Staggs and Ian Stansfield and Stumpf, {Michael P.H.} and Sudbery, {Peter E.} and Thyagarajan Srikantha and Qiandong Zeng and Judith Berman and Matthew Berriman and Joseph Heitman and Gow, {Neil A.R.} and Lorenz, {Michael C.} and Birren, {Bruce W.} and Manolis Kellis",

note = "Funding Information: Acknowledgements We thank the US National Human Genome Research Institute (NHGRI) for support under the Fungal Genome Initiative at the Broad Institute. We thank C. Kurtzman for providing the sequenced strains of L. elongisporus, C. guilliermondii and C. lusitaniae, M. Koehrsen for Broad Institute website support, D. Park for informatics support and K. Wolfe and A. Regev for comments on the manuscript. We acknowledge the contributions of the Broad Institute Sequencing Platform and A. Barron, L. Clark, C. Corton, D. Ormond, D. Saunders, K. Seeger and R. Squares from the Wellcome Trust Sanger Institute for the C. parapsilosis sequencing and assembly. N.A.R.G., A.J.P.B., M.B. and co-workers were supported by the Wellcome Trust; M.G., S.S., Q.Z., C.K., B.W.B. and C.A.C. were supported by NHGRI and the National Institute of Allergy and Infectious Disease, US National Institutes of Health (NIH), Department of Health and Human Services; G.B. and co-workers were supported by Science Foundation Ireland; J.B., A.F., J.H., A.M.N. and co-workers were supported by the NIH; and M.K., M.D.R. and M.F.L. by the NIH, the US National Science Foundation and the Sloan Foundation.",

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doi = "10.1038/nature08064",

language = "English (US)",

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TY - JOUR

T1 - Evolution of pathogenicity and sexual reproduction in eight Candida genomes

AU - Butler, Geraldine

AU - Rasmussen, Matthew D.

AU - Lin, Michael F.

AU - Santos, Manuel A.S.

AU - Sakthikumar, Sharadha

AU - Munro, Carol A.

AU - Rheinbay, Esther

AU - Grabherr, Manfred

AU - Forche, Anja

AU - Reedy, Jennifer L.

AU - Agrafioti, Ino

AU - Arnaud, Martha B.

AU - Bates, Steven

AU - Brown, Alistair J.P.

AU - Brunke, Sascha

AU - Costanzo, Maria C.

AU - Fitzpatrick, David A.

AU - De Groot, Piet W.J.

AU - Harris, David

AU - Hoyer, Lois L.

AU - Hube, Bernhard

AU - Klis, Frans M.

AU - Kodira, Chinnappa

AU - Lennard, Nicola

AU - Logue, Mary E.

AU - Martin, Ronny

AU - Neiman, Aaron M.

AU - Nikolaou, Elissavet

AU - Quail, Michael A.

AU - Quinn, Janet

AU - Santos, Maria C.

AU - Schmitzberger, Florian F.

AU - Sherlock, Gavin

AU - Shah, Prachi

AU - Silverstein, Kevin A.T.

AU - Skrzypek, Marek S.

AU - Soll, David

AU - Staggs, Rodney

AU - Stansfield, Ian

AU - Stumpf, Michael P.H.

AU - Sudbery, Peter E.

AU - Srikantha, Thyagarajan

AU - Zeng, Qiandong

AU - Berman, Judith

AU - Berriman, Matthew

AU - Heitman, Joseph

AU - Gow, Neil A.R.

AU - Lorenz, Michael C.

AU - Birren, Bruce W.

AU - Kellis, Manolis

N1 - Funding Information: Acknowledgements We thank the US National Human Genome Research Institute (NHGRI) for support under the Fungal Genome Initiative at the Broad Institute. We thank C. Kurtzman for providing the sequenced strains of L. elongisporus, C. guilliermondii and C. lusitaniae, M. Koehrsen for Broad Institute website support, D. Park for informatics support and K. Wolfe and A. Regev for comments on the manuscript. We acknowledge the contributions of the Broad Institute Sequencing Platform and A. Barron, L. Clark, C. Corton, D. Ormond, D. Saunders, K. Seeger and R. Squares from the Wellcome Trust Sanger Institute for the C. parapsilosis sequencing and assembly. N.A.R.G., A.J.P.B., M.B. and co-workers were supported by the Wellcome Trust; M.G., S.S., Q.Z., C.K., B.W.B. and C.A.C. were supported by NHGRI and the National Institute of Allergy and Infectious Disease, US National Institutes of Health (NIH), Department of Health and Human Services; G.B. and co-workers were supported by Science Foundation Ireland; J.B., A.F., J.H., A.M.N. and co-workers were supported by the NIH; and M.K., M.D.R. and M.F.L. by the NIH, the US National Science Foundation and the Sloan Foundation.

PY - 2009/6/4

Y1 - 2009/6/4

N2 - Candida species are the most common cause of opportunistic fungal infection worldwide. Here we report the genome sequences of six Candida species and compare these and related pathogens and non-pathogens. There are significant expansions of cell wall, secreted and transporter gene families in pathogenic species, suggesting adaptations associated with virulence. Large genomic tracts are homozygous in three diploid species, possibly resulting from recent recombination events. Surprisingly, key components of the mating and meiosis pathways are missing from several species. These include major differences at the mating-type loci (MTL); Lodderomyces elongisporus lacks MTL, and components of the a1/α2 cell identity determinant were lost in other species, raising questions about how mating and cell types are controlled. Analysis of the CUG leucine-to-serine genetic-code change reveals that 99% of ancestral CUG codons were erased and new ones arose elsewhere. Lastly, we revise the Candida albicans gene catalogue, identifying many new genes.

AB - Candida species are the most common cause of opportunistic fungal infection worldwide. Here we report the genome sequences of six Candida species and compare these and related pathogens and non-pathogens. There are significant expansions of cell wall, secreted and transporter gene families in pathogenic species, suggesting adaptations associated with virulence. Large genomic tracts are homozygous in three diploid species, possibly resulting from recent recombination events. Surprisingly, key components of the mating and meiosis pathways are missing from several species. These include major differences at the mating-type loci (MTL); Lodderomyces elongisporus lacks MTL, and components of the a1/α2 cell identity determinant were lost in other species, raising questions about how mating and cell types are controlled. Analysis of the CUG leucine-to-serine genetic-code change reveals that 99% of ancestral CUG codons were erased and new ones arose elsewhere. Lastly, we revise the Candida albicans gene catalogue, identifying many new genes.

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JO - Nature

JF - Nature

IS - 7247

ER -

Evolution of pathogenicity and sexual reproduction in eight Candida genomes

Abstract

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