Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete

Phaffia rhodozyma

Nicolás Bellora, Martín Moliné, Márcia David-Palma, Marco A Coelho, Chris Todd Hittinger, José P Sampaio, Paula Gonçalves, Diego Libkind

Research output: Contribution to journalArticle

8 Citations (Scopus)
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Abstract

BACKGROUND: The class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918(T), the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed.

RESULTS: Both genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 % of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 %. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated.

CONCLUSIONS: A draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.

Original languageEnglish
Pages (from-to)901
JournalBMC Genomics
Volume17
Issue number1
DOIs
Publication statusPublished - 9 Nov 2016

Fingerprint

Sexuality
Genomics
Genome
Introns
Genes
Antioxidants
Reproduction
Fungi
Fungal Genome
Aquaculture
Free Radical Scavengers
Drug Industry
Carotenoids
Multigene Family
Catalase
Superoxide Dismutase
Oxidative Stress
Yeasts
Oxygen
Enzymes

Keywords

  • Aquaculture
  • Basidiomycete
  • Mating type
  • Mycosporines
  • Photoprotection
  • Phylogenomics
  • Type strain
  • Xanthophyllomyces dendrorhous
  • Yeast

Cite this

@article{374bf3a549724f8da555207f7e47e4ac,
title = "Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma",
abstract = "BACKGROUND: The class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918(T), the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed.RESULTS: Both genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 {\%} of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 {\%}. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated.CONCLUSIONS: A draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.",
keywords = "Aquaculture, Basidiomycete , Mating type , Mycosporines , Photoprotection , Phylogenomics , Type strain , Xanthophyllomyces dendrorhous , Yeast",
author = "Nicol{\'a}s Bellora and Mart{\'i}n Molin{\'e} and M{\'a}rcia David-Palma and Coelho, {Marco A} and Hittinger, {Chris Todd} and Sampaio, {Jos{\'e} P} and Paula Gon{\cc}alves and Diego Libkind",
note = "This work was partially funded in Argentina by grants PICT 1814 and PICT 2542 (ANPCYT), PIP 424 (CONICET) and B171 (UNComahue), in Portugal by grant PTDC/BIA-GEN/112799/2009 and by the Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO, which is financed by national funds from FCT/MEC (UID/Multi/04378/2013) and co-financed by the ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728), and in USA by the National Science Foundation under grants DEB-1253634 and DEB-1442148 and funded in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494). CTH is a Pew Scholar in the Biomedical Sciences and an Alfred Toepfer Faculty Fellow, supported by the Pew Charitable Trusts and the Alexander von Humboldt Foundation, respectively. MAC and MD-P hold, respectively, grants SFRH/BPD/79198/2011 and SFRH/BD/81895/2011 from Fundacao para a Ciencia e a Tecnologia, Portugal. We thank Jim Dover for technical support and Mark Johnston for providing access to an Illumina GAIIx instrument at the University of Colorado School of Medicine. To Dr. Cifuentes (U.N. Chile) for providing a set of mRNAs for annotation and quality checks. We thank Laurie Connell, Christina Cuomo, Ratan Gachhui, and Joseph Heitman for the authorization of use of their genome sequences.",
year = "2016",
month = "11",
day = "9",
doi = "10.1186/s12864-016-3244-7",
language = "English",
volume = "17",
pages = "901",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "Springer Verlag",
number = "1",

}

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete : Phaffia rhodozyma. / Bellora, Nicolás; Moliné, Martín; David-Palma, Márcia; Coelho, Marco A; Hittinger, Chris Todd; Sampaio, José P; Gonçalves, Paula; Libkind, Diego.

In: BMC Genomics, Vol. 17, No. 1, 09.11.2016, p. 901.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete

T2 - Phaffia rhodozyma

AU - Bellora, Nicolás

AU - Moliné, Martín

AU - David-Palma, Márcia

AU - Coelho, Marco A

AU - Hittinger, Chris Todd

AU - Sampaio, José P

AU - Gonçalves, Paula

AU - Libkind, Diego

N1 - This work was partially funded in Argentina by grants PICT 1814 and PICT 2542 (ANPCYT), PIP 424 (CONICET) and B171 (UNComahue), in Portugal by grant PTDC/BIA-GEN/112799/2009 and by the Unidade de Ciencias Biomoleculares Aplicadas-UCIBIO, which is financed by national funds from FCT/MEC (UID/Multi/04378/2013) and co-financed by the ERDF under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728), and in USA by the National Science Foundation under grants DEB-1253634 and DEB-1442148 and funded in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494). CTH is a Pew Scholar in the Biomedical Sciences and an Alfred Toepfer Faculty Fellow, supported by the Pew Charitable Trusts and the Alexander von Humboldt Foundation, respectively. MAC and MD-P hold, respectively, grants SFRH/BPD/79198/2011 and SFRH/BD/81895/2011 from Fundacao para a Ciencia e a Tecnologia, Portugal. We thank Jim Dover for technical support and Mark Johnston for providing access to an Illumina GAIIx instrument at the University of Colorado School of Medicine. To Dr. Cifuentes (U.N. Chile) for providing a set of mRNAs for annotation and quality checks. We thank Laurie Connell, Christina Cuomo, Ratan Gachhui, and Joseph Heitman for the authorization of use of their genome sequences.

PY - 2016/11/9

Y1 - 2016/11/9

N2 - BACKGROUND: The class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918(T), the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed.RESULTS: Both genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 % of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 %. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated.CONCLUSIONS: A draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.

AB - BACKGROUND: The class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918(T), the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed.RESULTS: Both genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 % of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 %. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated.CONCLUSIONS: A draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.

KW - Aquaculture

KW - Basidiomycete

KW - Mating type

KW - Mycosporines

KW - Photoprotection

KW - Phylogenomics

KW - Type strain

KW - Xanthophyllomyces dendrorhous

KW - Yeast

U2 - 10.1186/s12864-016-3244-7

DO - 10.1186/s12864-016-3244-7

M3 - Article

VL - 17

SP - 901

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

ER -