High-quality genome of the basidiomycete yeast Dioszegia hungarica PDD-24b-2 isolated from cloud water

Jarrige, Domitille; Haridas, Sajeet; Bleykasten-Grosshans, Claudine; Joly, Muriel; Nadalig, Thierry; Sancelme, Martine; Vuilleumier, Stéphane; Grigoriev, Igor V.; Amato, Pierre; Bringel, Françoise

doi:10.1093/g3journal/jkac282

Title: High-quality genome of the basidiomycete yeast Dioszegia hungarica PDD-24b-2 isolated from cloud water

Journal Article · Wed Oct 19 00:00:00 UTC 2022 · G3

DOI: https://doi.org/10.1093/g3journal/jkac282 · OSTI ID:1992470

^[1];

^[2];

^[1];

^[3];

^[1]; Sancelme, Martine ^[3];

^[1];

^[4];

^[3];

^[1]

Université de Strasbourg (France)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. Clermont Auvergne, Clermont-Ferrand (France)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

The genome of the basidiomycete yeast Dioszegia hungarica strain PDD-24b-2 isolated from cloud water at the summit of puy de $$D\hat{o}me$$ (France) was sequenced using a hybrid PacBio and Illumina sequencing strategy. The obtained assembled genome of 20.98 Mb and a GC content of 57% is structured in 16 large-scale contigs ranging from 90 kb to 5.56Mb, and another 27.2 kb contig representing the complete circular mitochondrial genome. In total, 8,234 proteins were predicted from the genome sequence. The mitochondrial genome shows 16.2% cgu codon usage for arginine but has no canonical cognate tRNA to translate this codon. Detected transposable element (TE)-related sequences account for about 0.63% of the assembled genome. A dataset of 2,068 hand-picked public environmental metagenomes, representing over 20 Tbp of raw reads, was probed for D. hungarica related ITS sequences, and revealed worldwide distribution of this species, particularly in aerial habitats. Growth experiments suggested a psychrophilic phenotype and the ability to disperse by producing ballistospores. The high-quality assembled genome obtained for this D. hungarica strain will help investigate the behavior and ecological functions of this species in the environment.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1992470

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

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (65)

Fungal Genome Annotation Haridas, Sajeet; Salamov, Asaf; Grigoriev, Igor V. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7804-5_15	book	January 2018
Clouds: A Transient and Stressing Habitat for Microorganisms Delort, Anne Marie; Vaïtilingom, Mickael; Joly, Muriel Microbial Ecology of Extreme Environments https://doi.org/10.1007/978-3-319-51686-8_10	book	January 2017
Biology, dynamics, and applications of transposable elements in basidiomycete fungi Castanera, Raúl; Borgognone, Alessandra; Pisabarro, Antonio G. Applied Microbiology and Biotechnology, Vol. 101, Issue 4 https://doi.org/10.1007/s00253-017-8097-8	journal	January 2017
Tolerance to Ultraviolet Radiation of Psychrotolerant Yeasts and Analysis of Their Carotenoid, Mycosporine, and Ergosterol Content Villarreal, Pablo; Carrasco, Mario; Barahona, Salvador Current Microbiology, Vol. 72, Issue 1 https://doi.org/10.1007/s00284-015-0928-1	journal	October 2015
Characterization of Afp1, an antifreeze protein from the psychrophilic yeast Glaciozyma antarctica PI12 Hashim, Noor Haza Fazlin; Bharudin, Izwan; Nguong, Douglas Law Sie Extremophiles, Vol. 17, Issue 1 https://doi.org/10.1007/s00792-012-0494-4	journal	November 2012
Taxonomy and richness of yeasts associated with angiosperms, bryophytes, and meltwater biofilms collected in the Antarctic Peninsula Ferreira, Eskálath Morganna Silva; de Sousa, Francisca Maria Pinheiro; Rosa, Luiz Henrique Extremophiles, Vol. 23, Issue 1 https://doi.org/10.1007/s00792-018-1069-9	journal	November 2018
Toward a rapid method for the study of biodiversity in cold environments: the characterization of psychrophilic yeasts by MALDI-TOF mass spectrometry Dalluge, Joseph J.; Brown, Elizabeth C.; Connell, Laurie B. Extremophiles, Vol. 23, Issue 4 https://doi.org/10.1007/s00792-019-01097-5	journal	May 2019
Among-site rate variation and its impact on phylogenetic analyses Yang, Ziheng Trends in Ecology & Evolution, Vol. 11, Issue 9 https://doi.org/10.1016/0169-5347(96)10041-0	journal	September 1996
Long-term features of cloud microbiology at the puy de Dôme (France) Vaïtilingom, Mickaël; Attard, Eléonore; Gaiani, Nicolas Atmospheric Environment, Vol. 56 https://doi.org/10.1016/j.atmosenv.2012.03.072	journal	September 2012
Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome Salazar, Guillem; Paoli, Lucas; Alberti, Adriana Cell, Vol. 179, Issue 5 https://doi.org/10.1016/j.cell.2019.10.014	journal	November 2019
Phylloplane yeasts from Portugal: Seven novel anamorphic species in the Tremellales lineage of the Hymenomycetes (Basidiomycota) producing orange-coloured colonies Inacio, J.; Portugal, L.; Spencermartins, I. FEMS Yeast Research, Vol. 5, Issue 12 https://doi.org/10.1016/j.femsyr.2005.05.007	journal	December 2005
tRNA’s Wobble Decoding of the Genome: 40 Years of Modification Agris, Paul F.; Vendeix, Franck A. P.; Graham, William D. Journal of Molecular Biology, Vol. 366, Issue 1 https://doi.org/10.1016/j.jmb.2006.11.046	journal	February 2007
Photoprotective role of carotenoids in yeasts: Response to UV-B of pigmented and naturally-occurring albino strains Moliné, Martín; Libkind, Diego; del Carmen Diéguez, María Journal of Photochemistry and Photobiology B: Biology, Vol. 95, Issue 3 https://doi.org/10.1016/j.jphotobiol.2009.02.006	journal	June 2009
Biosynthesis of the xanthophyll plectaniaxanthin as a stress response in the red yeast Dioszegia (Tremellales, Heterobasidiomycetes, Fungi) Madhour, Abderrahim; Anke, Heidrun; Mucci, Adele Phytochemistry, Vol. 66, Issue 22 https://doi.org/10.1016/j.phytochem.2005.09.010	journal	November 2005
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
Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species Li, A. -H.; Yuan, F. -X.; Groenewald, M. Studies in Mycology, Vol. 96 https://doi.org/10.1016/j.simyco.2020.01.002	journal	June 2020
Mechanisms of rDNA Copy Number Maintenance Nelson, Jonathan O.; Watase, George J.; Warsinger-Pepe, Natalie Trends in Genetics, Vol. 35, Issue 10 https://doi.org/10.1016/j.tig.2019.07.006	journal	October 2019
Functional repertoire convergence of distantly related eukaryotic plankton lineages abundant in the sunlit ocean Delmont, Tom O.; Gaia, Morgan; Hinsinger, Damien D. Cell Genomics, Vol. 2, Issue 5 https://doi.org/10.1016/j.xgen.2022.100123	journal	May 2022
Integrative genomics viewer Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy Nature Biotechnology, Vol. 29, Issue 1 https://doi.org/10.1038/nbt.1754	journal	January 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
A unified classification system for eukaryotic transposable elements Wicker, Thomas; Sabot, François; Hua-Van, Aurélie Nature Reviews Genetics, Vol. 8, Issue 12 https://doi.org/10.1038/nrg2165	journal	December 2007
A global ocean atlas of eukaryotic genes Carradec, Quentin; Pelletier, Eric; Da Silva, Corinne Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02342-1	journal	January 2018
Assembly of long, error-prone reads using repeat graphs Kolmogorov, Mikhail; Yuan, Jeffrey; Lin, Yu Nature Biotechnology, Vol. 37, Issue 5 https://doi.org/10.1038/s41587-019-0072-8	journal	April 2019
GlobalFungi, a global database of fungal occurrences from high-throughput-sequencing metabarcoding studies Větrovský, Tomáš; Morais, Daniel; Kohout, Petr Scientific Data, Vol. 7, Issue 1 https://doi.org/10.1038/s41597-020-0567-7	journal	July 2020
Potential impact of microbial activity on the oxidant capacity and organic carbon budget in clouds Vaitilingom, M.; Deguillaume, L.; Vinatier, V. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/pnas.1205743110	journal	December 2012
RepeatModeler2 for automated genomic discovery of transposable element families Flynn, Jullien M.; Hubley, Robert; Goubert, Clément Proceedings of the National Academy of Sciences, Vol. 117, Issue 17 https://doi.org/10.1073/pnas.1921046117	journal	April 2020
Characterization of the complete mitochondrial genome of Dioszegia changbaiensis (Tremellales: Bulleribasidiaceae) with phylogenetic implications Tan, Maoling; Wang, Qiangfeng Mitochondrial DNA Part B, Vol. 6, Issue 12 https://doi.org/10.1080/23802359.2021.1915197	journal	November 2021
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Scaling read aligners to hundreds of threads on general-purpose processors Langmead, Ben; Wilks, Christopher; Antonescu, Valentin Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty648	journal	July 2018
Microbial ecology of the atmosphere Šantl-Temkiv, Tina; Amato, Pierre; Casamayor, Emilio O. FEMS Microbiology Reviews, Vol. 46, Issue 4 https://doi.org/10.1093/femsre/fuac009	journal	February 2022
Sequenceserver: A Modern Graphical User Interface for Custom BLAST Databases Priyam, Anurag; Woodcroft, Ben J.; Rai, Vivek Molecular Biology and Evolution, Vol. 36, Issue 12 https://doi.org/10.1093/molbev/msz185	journal	August 2019
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
CD-Search: protein domain annotations on the fly Marchler-Bauer, A.; Bryant, S. H. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh454	journal	July 2004
The natural history of the WRKY–GCM1 zinc fingers and the relationship between transcription factors and transposons Babu, M. Madan; Iyer, Lakshminarayan M.; Balaji, S. Nucleic Acids Research, Vol. 34, Issue 22 https://doi.org/10.1093/nar/gkl888	journal	November 2006
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
CDD/SPARCLE: functional classification of proteins via subfamily domain architectures Marchler-Bauer, Aron; Bo, Yu; Han, Lianyi Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1129	journal	November 2016
The MAR databases: development and implementation of databases specific for marine metagenomics Klemetsen, Terje; Raknes, Inge A.; Fu, Juan Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1036	journal	November 2017
The Ocean Gene Atlas: exploring the biogeography of plankton genes online Villar, Emilie; Vannier, Thomas; Vernette, Caroline Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky376	journal	May 2018
Dioszegia antarctica sp. nov. and Dioszegia cryoxerica sp. nov., psychrophilic basidiomycetous yeasts from polar desert soils in Antarctica Connell, Laurie B.; Redman, Regina; Rodriguez, Russel International Journal of Systematic and Evolutionary Microbiology, Vol. 60, Issue 6 https://doi.org/10.1099/ijs.0.015412-0	journal	June 2010
Description of Dioszegia patagonica sp. nov., a novel carotenogenic yeast isolated from cold environments Trochine, Andrea; Turchetti, Benedetta; Vaz, Aline B. M. International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 11 https://doi.org/10.1099/ijsem.0.002211	journal	November 2017
tRNA biology charges to the front Phizicky, E. M.; Hopper, A. K. Genes & Development, Vol. 24, Issue 17 https://doi.org/10.1101/gad.1956510	journal	September 2010
Highly efficient concerted evolution in the ribosomal DNA repeats: Total rDNA repeat variation revealed by whole-genome shotgun sequence data Ganley, A. R. D.; Kobayashi, T. Genome Research, Vol. 17, Issue 2 https://doi.org/10.1101/gr.5457707	journal	January 2007
Transposable element annotation in non‐model species: The benefits of species‐specific repeat libraries using semi‐automated EDTA and DeepTE de novo pipelines Bell, Ellen A.; Butler, Christopher L.; Oliveira, Claudio Molecular Ecology Resources, Vol. 22, Issue 2 https://doi.org/10.1111/1755-0998.13489	journal	September 2021
Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina De GarcÃa, Virginia; Brizzio, Silvia; Libkind, Diego FEMS Microbiology Ecology, Vol. 59, Issue 2 https://doi.org/10.1111/j.1574-6941.2006.00239.x	journal	February 2007
Organization of mitochondrial DNA in the basidiomycetousDioszegia hungarica(Cryptococcus hungaricus)species GÃ¡cser, Attila; Hamari, Zsuzsanna; Pfeiffer, Ilona FEMS Microbiology Letters, Vol. 212, Issue 1 https://doi.org/10.1111/j.1574-6968.2002.tb11236.x	journal	June 2002
Organic farming increases richness of fungal taxa in the wheat phyllosphere Karlsson, Ida; Friberg, Hanna; Kolseth, Anna-Karin Molecular Ecology, Vol. 26, Issue 13 https://doi.org/10.1111/mec.14132	journal	April 2017
Genome‐based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles Lofgren, Lotus A.; Uehling, Jessie K.; Branco, Sara Molecular Ecology, Vol. 28, Issue 4 https://doi.org/10.1111/mec.14995	journal	February 2019
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
Contribution of Microbial Activity to Carbon Chemistry in Clouds Vaitilingom, M.; Amato, P.; Sancelme, M. Applied and Environmental Microbiology, Vol. 76, Issue 1 https://doi.org/10.1128/AEM.01127-09	journal	October 2009
A new medium for the enumeration and subculture of bacteria from potable water. Reasoner, D. J.; Geldreich, E. E. Applied and Environmental Microbiology, Vol. 49, Issue 1 https://doi.org/10.1128/aem.49.1.1-7.1985	journal	January 1985
Microbial Population Dynamics on Leaves Kinkel, Linda L. Annual Review of Phytopathology, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.phyto.35.1.327	journal	September 1997
NOAA’s HYSPLIT Atmospheric Transport and Dispersion Modeling System Stein, A. F.; Draxler, R. R.; Rolph, G. D. Bulletin of the American Meteorological Society, Vol. 96, Issue 12 https://doi.org/10.1175/BAMS-D-14-00110.1	journal	December 2015
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
“One code to find them all”: a perl tool to conveniently parse RepeatMasker output files Bailly-Bechet, Marc; Haudry, Annabelle; Lerat, Emmanuelle Mobile DNA, Vol. 5, Issue 1 https://doi.org/10.1186/1759-8753-5-13	journal	January 2014
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation Agler, Matthew T.; Ruhe, Jonas; Kroll, Samuel PLOS Biology, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pbio.1002352	journal	January 2016
Phs1 and the Synthesis of Very Long Chain Fatty Acids Are Required for Ballistospore Formation Ianiri, Giuseppe; Abhyankar, Ritika; Kihara, Akio PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105147	journal	August 2014
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
Mushrooms as Rainmakers: How Spores Act as Nuclei for Raindrops Hassett, Maribeth O.; Fischer, Mark W. F.; Money, Nicholas P. PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0140407	journal	October 2015
Active microorganisms thrive among extremely diverse communities in cloud water Amato, Pierre; Joly, Muriel; Besaury, Ludovic PLOS ONE, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pone.0182869	journal	August 2017
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
The diversity, extracellular enzymatic activities and photoprotective compounds of yeasts isolated in Antarctica Vaz, Aline B. M.; Rosa, Luiz H.; Vieira, Mariana L. A. Brazilian Journal of Microbiology, Vol. 42, Issue 3 https://doi.org/10.1590/S1517-83822011000300012	journal	September 2011
Carotenoid Pigmentation in Antarctic Heterotrophic Bacteria as a Strategy to Withstand Environmental Stresses Dieser, Markus; Greenwood, Mark; Foreman, Christine M. Arctic, Antarctic, and Alpine Research, Vol. 42, Issue 4 https://doi.org/10.1657/1938-4246-42.4.396	journal	November 2010
Emendation of Dioszegia with redescription of Dioszegia hungarica and two new combinations, Dioszegia aurantiaca and Dioszegia crocea. Takashima, Masako; Deak, Tibor; Nakase, Takashi The Journal of General and Applied Microbiology, Vol. 47, Issue 2 https://doi.org/10.2323/jgam.47.75	journal	January 2001
Spatiotemporal Variation and Networks in the Mycobiome of the Wheat Canopy Sapkota, Rumakanta; Jørgensen, Lise N.; Nicolaisen, Mogens Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01357	journal	August 2017
Fig. 19 in Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: Proposal of two new orders, three new families, eight new genera and one hundred and seven new species Li, A. -H.; Yuan, F. -X.; Groenewald, M. Zenodo https://doi.org/10.5281/zenodo.10497288	image	January 2020

Similar Records

Physical mapping of complex genomes by sampled sequencing: A theoretical analysis

Journal Article · Mon May 01 04:00:00 UTC 1995 · Genomics · OSTI ID:114893

Kupfer, K; Smith, M; Quackenbush, J

Optimizing de novo genome assembly from PCR-amplified metagenomes

Journal Article · Thu May 09 00:00:00 UTC 2019 · PeerJ · OSTI ID:1526560

Roux, Simon; Trubl, Gareth; Goudeau, Danielle; +12 more

Integration of Complete Plasmids Containing Bont Genes into Chromosomes of Clostridium parabotulinum, Clostridium sporogenes, and Clostridium argentinense

Journal Article · Thu Jul 08 00:00:00 UTC 2021 · Toxins · OSTI ID:1815750

Smith, Theresa J.; Tian, Renmao; Imanian, Behzad; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Dioszegia hungarica strain PDD-24b-2
Tremellaceae
aeromicrobiology
airborne microorganisms
cold environment
de novo sequencing
fungal spore
fungi
mitochondrial genome
transposable elements

Title: High-quality genome of the basidiomycete yeast Dioszegia hungarica PDD-24b-2 isolated from cloud water

Citation Formats

References (65)

Similar Records

Related Subjects