Draft genome sequences of strains CBS6241 and CBS6242 of the basidiomycetous yeast Filobasidium floriforme

Guerreiro, Marco Alexandre; Ahrendt, Steven; Pangilinan, Jasmyn; Chen, Cindy; Yan, Mi; Lipzen, Anna; Barry, Kerrie; Grigoriev, Igor V.; Begerow, Dominik; Nowrousian, Minou

doi:10.1093/g3journal/jkab398

Draft genome sequences of strains CBS6241 and CBS6242 of the basidiomycetous yeast Filobasidium floriforme

Journal Article · Sun Nov 14 23:00:00 EST 2021 · G3

DOI:https://doi.org/10.1093/g3journal/jkab398· OSTI ID:1894069

^[1]; Ahrendt, Steven ^[2]; Pangilinan, Jasmyn ^[2]; Chen, Cindy ^[2]; Yan, Mi ^[2]; Lipzen, Anna ^[2]; Barry, Kerrie ^[2]; Grigoriev, Igor V. ^[3]; Begerow, Dominik ^[1]; ^[1]

Ruhr Univ., Bochum (Germany)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

The Tremellomycetes are a species-rich group within the basidiomycete fungi; however, most analyses of this group to date have focused on pathogenic Cryptococcus species within the order Tremellales. Recent genome-assisted studies of other Tremellomycetes have identified interesting features with respect to biotechnological applications as well as the evolution of genes involved in mating and sexual development. Here, we report genome sequences of two strains of Filobasidium floriforme, a species from the order Filobasidiales, which branches basally to the Tremellales, Trichosporonales, and Holtermanniales. The assembled genomes of strains CBS6241 and CBS6242 are 27.4 Mb and 26.4 Mb in size, respectively, with 8314 and 7695 predicted protein-coding genes. Overall sequence identity at nucleic acid level between the strains is 97%. Among the predicted genes are pheromone precursor and pheromone receptor genes as well as two genes encoding homedomain (HD) transcription factors, which are predicted to be part of the mating type (MAT) locus. Sequence analysis indicates that CBS6241 and CBS6242 carry different alleles for both the pheromone/receptor genes as well as the HD transcription factors. Orthology inference identified 1482 orthogroups exclusively found in F. floriforme, some of which were involved in carbohydrate transport and metabolism. Subsequent CAZyme repertoire characterization identified 267 and 247 enzymes for CBS6241 and CBS6242, respectively, the second highest number of CAZymes among the analyzed Tremellomycete species. In addition, F. floriforme contains five CAZymes absent in other species and several plant-cell-wall degrading CAZymes with the highest copy number in Tremellomycota, indicating the biotechnological potential of this species.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); German Research Foundation (DFG)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1894069

Journal Information:: G3, Journal Name: G3 Journal Issue: 2 Vol. 12; ISSN 2160-1836

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Using SPAdes De Novo Assembler Prjibelski, Andrey; Antipov, Dmitry; Meleshko, Dmitry Current Protocols in Bioinformatics, Vol. 70, Issue 1 https://doi.org/10.1002/cpbi.102	journal	June 2020
A Trichosporonales genome tree based on 27 haploid and three evolutionarily conserved ‘natural’ hybrid genomes: Trichosporonales genome tree Takashima, Masako; Sriswasdi, Sira; Manabe, Ri-Ichiroh Yeast, Vol. 35, Issue 1 https://doi.org/10.1002/yea.3284	journal	December 2017
Filobasidium capsuligenum nov. comb. Rodrigues de Miranda, L. Antonie van Leeuwenhoek, Vol. 38, Issue 1 https://doi.org/10.1007/BF02328080	journal	December 1972
Research Progress Concerning Fungal and Bacterial β-Xylosidases Bosetto, Adilson; Justo, Priscila Innocenti; Zanardi, Bruna Applied Biochemistry and Biotechnology, Vol. 178, Issue 4 https://doi.org/10.1007/s12010-015-1908-4	journal	November 2015
Multiallelic recognition: Nonself-dependent dimerization of the bE and bW homeodomain proteins in ustilago maydis Kämper, Jörg; Reichmann, Michael; Romeis, Tina Cell, Vol. 81, Issue 1 https://doi.org/10.1016/0092-8674(95)90372-0	journal	April 1995
Plant biomass degradation by fungi Mäkelä, Miia R.; Donofrio, Nicole; de Vries, Ronald P. Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.08.010	journal	November 2014
Genome sequence of a microbial lipid producing fungus Cryptococcus albidus NT2002 Yong, Xiaoyu; Yan, Zhiying; Xu, Lin Journal of Biotechnology, Vol. 223 https://doi.org/10.1016/j.jbiotec.2016.02.026	journal	April 2016
Phylogeny of tremellomycetous yeasts and related dimorphic and filamentous basidiomycetes reconstructed from multiple gene sequence analyses Liu, X. -Z.; Wang, Q. -M.; Theelen, B. Studies in Mycology, Vol. 81 https://doi.org/10.1016/j.simyco.2015.08.001	journal	June 2015
Towards an integrated phylogenetic classification of the Tremellomycetes Liu, X. -Z.; Wang, Q. -M.; Göker, M. Studies in Mycology, Vol. 81 https://doi.org/10.1016/j.simyco.2015.12.001	journal	June 2015
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Multiple convergent supergene evolution events in mating-type chromosomes Branco, Sara; Carpentier, Fantin; Rodríguez de la Vega, Ricardo C. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04380-9	journal	May 2018
Cryptococcus terricola is a promising oleaginous yeast for biodiesel production from starch through consolidated bioprocessing Tanimura, Ayumi; Takashima, Masako; Sugita, Takashi Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep04776	journal	April 2014
Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism Branco, Sara; Badouin, Hélène; Rodríguez de la Vega, Ricardo C. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1701658114	journal	June 2017
Identification of the MATa mating-type locus of Cryptococcus neoformans reveals a serotype A MATa strain thought to have been extinct Lengeler, K. B.; Wang, P.; Cox, G. M. Proceedings of the National Academy of Sciences, Vol. 97, Issue 26 https://doi.org/10.1073/pnas.97.26.14455	journal	December 2000
Fueling the future with fungal genomics Grigoriev, Igor V.; Cullen, Daniel; Goodwin, Stephen B. Mycology, Vol. 2, Issue 3 https://doi.org/10.1080/21501203.2011.584577	journal	July 2011
Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi Sista Kameshwar, Ayyappa Kumar; Qin, Wensheng Mycology, Vol. 9, Issue 2 https://doi.org/10.1080/21501203.2017.1419296	journal	December 2017
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
Using native and syntenically mapped cDNA alignments to improve de novo gene finding Stanke, Mario; Diekhans, Mark; Baertsch, Robert Bioinformatics, Vol. 24, Issue 5 https://doi.org/10.1093/bioinformatics/btn013	journal	January 2008
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
FinisherSC: a repeat-aware tool for upgrading de novo assembly using long reads Lam, Ka-Kit; LaButti, Kurt; Khalak, Asif Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv280	journal	June 2015
Unique genomic traits for cold adaptation in Naganishia vishniacii , a polyextremophile yeast isolated from Antarctica Nizovoy, Paula; Bellora, Nicolás; Haridas, Sajeet FEMS Yeast Research, Vol. 21, Issue 1 https://doi.org/10.1093/femsyr/foaa056	journal	November 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Thompson, J. Nucleic Acids Research, Vol. 25, Issue 24 https://doi.org/10.1093/nar/25.24.4876	journal	December 1997
Pfam: The protein families database in 2021 Mistry, Jaina; Chuguransky, Sara; Williams, Lowri Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa913	journal	October 2020
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Huerta-Cepas, Jaime; Szklarczyk, Damian; Heller, Davide Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1085	journal	November 2018
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation Zhang, Han; Yohe, Tanner; Huang, Le Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky418	journal	May 2018
Microbe Profile: Cryptococcus neoformans species complex Bahn, Yong-Sun; Sun, Sheng; Heitman, Joseph Microbiology, Vol. 166, Issue 9 https://doi.org/10.1099/mic.0.000973	journal	September 2020
Global deceleration of gene evolution following recent genome hybridizations in fungi Sriswasdi, Sira; Takashima, Masako; Manabe, Ri-ichiroh Genome Research, Vol. 26, Issue 8 https://doi.org/10.1101/gr.205948.116	journal	July 2016
MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes Cantarel, B. L.; Korf, I.; Robb, S. M. C. Genome Research, Vol. 18, Issue 1 https://doi.org/10.1101/gr.6743907	journal	November 2007
Creating novel specificities in a fungal nonself recognition system by single step homologous recombination events Kämper, Jörg; Friedrich, Michael W.; Kahmann, Regine New Phytologist, Vol. 228, Issue 3 https://doi.org/10.1111/nph.16755	journal	July 2020
The Genome of the Basidiomycetous Yeast and Human Pathogen Cryptococcus neoformans Loftus, B. J. Science, Vol. 307, Issue 5713 https://doi.org/10.1126/science.1103773	journal	February 2005
Mating-Type Locus of Cryptococcus neoformans: a Step in the Evolution of Sex Chromosomes Lengeler, Klaus B.; Fox, Deborah S.; Fraser, James A. Eukaryotic Cell, Vol. 1, Issue 5 https://doi.org/10.1128/EC.1.5.704-718.2002	journal	October 2002
Plant-Polysaccharide-Degrading Enzymes from Basidiomycetes Rytioja, Johanna; Hildén, Kristiina; Yuzon, Jennifer Microbiology and Molecular Biology Reviews, Vol. 78, Issue 4 https://doi.org/10.1128/MMBR.00035-14	journal	November 2014
Draft Genome Sequences of Tremellomycetes Strains Isolated from the International Space Station Bijlani, Swati; Singh, Nitin K.; Mason, Christopher E. Microbiology Resource Announcements, Vol. 9, Issue 26 https://doi.org/10.1128/MRA.00504-20	journal	June 2020
Draft Genome Sequence of Naganishia liquefaciens Strain N6, Isolated from the Japan Trench Han, Yong-Woon; Kajitani, Rei; Morimoto, Hiroya Microbiology Resource Announcements, Vol. 9, Issue 47 https://doi.org/10.1128/MRA.00827-20	journal	November 2020
Draft Genome Sequence of the Oleaginous Yeast Cryptococcus albidus var. albidus Vajpeyi, Shashwat; Chandran, Kartik Genome Announcements, Vol. 4, Issue 3 https://doi.org/10.1128/genomeA.00390-16	journal	June 2016
Draft Genome Sequence of the Causative Antigen of Summer-Type Hypersensitivity Pneumonitis, Trichosporon domesticum JCM 9580 Cho, Otomi; Ichikawa, Tomoe; Kurakado, Sanae Genome Announcements, Vol. 4, Issue 4 https://doi.org/10.1128/genomeA.00651-16	journal	August 2016
Draft Genome Sequence of Cryptococcus terricola JCM 24523, an Oleaginous Yeast Capable of Expressing Exogenous DNA Close, Dan; Ojumu, John; Zhang, Gui Genome Announcements, Vol. 4, Issue 6 https://doi.org/10.1128/genomeA.01238-16	journal	December 2016
Genomics and Transcriptomics Analyses of the Oil-Accumulating Basidiomycete Yeast Trichosporon oleaginosus: Insights into Substrate Utilization and Alternative Evolutionary Trajectories of Fungal Mating Systems Kourist, Robert; Bracharz, Felix; Lorenzen, Jan mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00918-15	journal	July 2015
The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies Spatafora, Joseph W.; Aime, M. Catherine; Grigoriev, Igor V. Microbiology Spectrum, Vol. 5, Issue 5 https://doi.org/10.1128/microbiolspec.FUNK-0053-2016	journal	October 2017
The Evolution of Sexual Reproduction and the Mating-Type Locus: Links to Pathogenesis of Cryptococcus Human Pathogenic Fungi Sun, Sheng; Coelho, Marco A.; David-Palma, Márcia Annual Review of Genetics, Vol. 53, Issue 1 https://doi.org/10.1146/annurev-genet-120116-024755	journal	December 2019
Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi Zhao, Zhongtao; Liu, Huiquan; Wang, Chenfang BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-274	journal	January 2013
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
The genome of the basal agaricomycete Xanthophyllomyces dendrorhous provides insights into the organization of its acetyl-CoA derived pathways and the evolution of Agaricomycotina Sharma, Rahul; Gassel, Sören; Steiger, Sabine BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1380-0	journal	March 2015
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 BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3244-7	journal	November 2016
Genomic characterization of plant cell wall degrading enzymes and in silico analysis of xylanses and polygalacturonases of Fusarium virguliforme Chang, Hao-Xun; Yendrek, Craig R.; Caetano-Anolles, Gustavo BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0761-0	journal	July 2016
Opportunities and challenges in the development of Cutaneotrichosporon oleaginosus ATCC 20509 as a new cell factory for custom tailored microbial oils Bracharz, Felix; Beukhout, Teun; Mehlmer, Norbert Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0791-9	journal	October 2017
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
The genome of the basal agaricomycete Xanthophyllomyces dendrorhous provides insights into the organization of its acetyl-CoA derived pathways and the evolution of Agaricomycotina Thines, M. BiK-F Data and Metadata Repository https://doi.org/10.12761/sgn.2015.1	dataset	January 2015
Convergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms Fraser, James A.; Diezmann, Stephanie; Subaran, Ryan L. PLoS Biology, Vol. 2, Issue 12 https://doi.org/10.1371/journal.pbio.0020384	journal	November 2004
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
The Mating Type Locus (MAT) and Sexual Reproduction of Cryptococcus heveanensis: Insights into the Evolution of Sex and Sex-Determining Chromosomal Regions in Fungi Metin, Banu; Findley, Keisha; Heitman, Joseph PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000961	journal	May 2010
Discovery of a Modified Tetrapolar Sexual Cycle in Cryptococcus amylolentus and the Evolution of MAT in the Cryptococcus Species Complex Findley, Keisha; Sun, Sheng; Fraser, James A. PLoS Genetics, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pgen.1002528	journal	February 2012
Convergent evolution of linked mating-type loci in basidiomycete fungi Sun, Sheng; Coelho, Marco A.; Heitman, Joseph PLOS Genetics, Vol. 15, Issue 9 https://doi.org/10.1371/journal.pgen.1008365	journal	September 2019
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement Walker, Bruce J.; Abeel, Thomas; Shea, Terrance PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112963	journal	November 2014
Selection of Orthologous Genes for Construction of a Highly Resolved Phylogenetic Tree and Clarification of the Phylogeny of Trichosporonales Species Takashima, Masako; Manabe, Ri-ichiroh; Iwasaki, Wataru PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0131217	journal	August 2015
In silico Proteomic Analysis Provides Insights Into Phylogenomics and Plant Biomass Deconstruction Potentials of the Tremelalles Aliyu, Habibu; Gorte, Olga; Zhou, Xinhai Frontiers in Bioengineering and Biotechnology, Vol. 8 https://doi.org/10.3389/fbioe.2020.00226	journal	April 2020
Biosynthesis of Astaxanthin as a Main Carotenoid in the Heterobasidiomycetous Yeast Xanthophyllomyces dendrorhous Barredo, Jose; García-Estrada, Carlos; Kosalkova, Katarina Journal of Fungi, Vol. 3, Issue 3 https://doi.org/10.3390/jof3030044	journal	July 2017
The Untapped Australasian Diversity of Astaxanthin-Producing Yeasts with Biotechnological Potential—Phaffia australis sp. nov. and Phaffia tasmanica sp. nov. David-Palma, Márcia; Libkind, Diego; Brito, Patrícia H. Microorganisms, Vol. 8, Issue 11 https://doi.org/10.3390/microorganisms8111651	journal	October 2020
Additional file 6: of 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 Figshare-Supplementary information for journal article at DOI: 10.1186/s12864-016-3244-7, 1 zip file (1.39 MB) https://doi.org/10.6084/m9.figshare.c.3618773_d8.v1	dataset	November 2016

Similar Records

The role of pheromone receptors for communication and mating in Hypocrea jecorina (Trichoderma reesei)

Journal Article · Fri Aug 03 00:00:00 EDT 2012 · Fungal Genetics and Biology · OSTI ID:1623668

Genomics and Transcriptomics Analyses of the Oil-Accumulating Basidiomycete Yeast Trichosporon oleaginosus: Insights into Substrate Utilization and Alternative Evolutionary Trajectories of Fungal Mating Systems

Journal Article · Tue Jul 21 00:00:00 EDT 2015 · mBio (Online) · OSTI ID:1626122

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
CAZymes
Filobasidiales
Filobasidium floriforme
basidiomycete
mating-type locus

Draft genome sequences of strains CBS6241 and CBS6242 of the basidiomycetous yeast Filobasidium floriforme

Citation Formats

References (66)

Similar Records

Related Subjects