Dataset Information

Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization.

ABSTRACT: Polyploidization is an important process in the evolution of eukaryotic genomes, but ensuing molecular mechanisms remain to be clarified. Autopolyploidization or whole-genome duplication events frequently are resolved in resulting lineages by the loss of single genes from most duplicated pairs, causing transient gene dosage imbalance and accelerating speciation through meiotic infertility. Allopolyploidization or formation of interspecies hybrids raises the problem of genetic incompatibility (Bateson-Dobzhansky-Muller effect) and may be resolved by the accumulation of mutational changes in resulting lineages. In this article, we show that an osmotolerant yeast species, Pichia sorbitophila, recently isolated in a concentrated sorbitol solution in industry, illustrates this last situation. Its genome is a mosaic of homologous and homeologous chromosomes, or parts thereof, that corresponds to a recently formed hybrid in the process of evolution. The respective parental contributions to this genome were characterized using existing variations in GC content. The genomic changes that occurred during the short period since hybrid formation were identified (e.g., loss of heterozygosity, unilateral loss of rDNA, reciprocal exchange) and distinguished from those undergone by the two parental genomes after separation from their common ancestor (i.e., NUMT (NUclear sequences of MiTochondrial origin) insertions, gene acquisitions, gene location movements, reciprocal translocation). We found that the physiological characteristics of this new yeast species are determined by specific but unequal contributions of its two parents, one of which could be identified as very closely related to an extant Pichia farinosa strain.

SUBMITTER: Louis VL

PROVIDER: S-EPMC3284337 | biostudies-literature | 2012 Feb

REPOSITORIES: biostudies-literature

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Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization.

Louis Véronique Leh VL Despons Laurence L Friedrich Anne A Martin Tiphaine T Durrens Pascal P Casarégola Serge S Neuvéglise Cécile C Fairhead Cécile C Marck Christian C Cruz José A JA Straub Marie-Laure ML Kugler Valérie V Sacerdot Christine C Uzunov Zlatyo Z Thierry Agnes A Weiss Stéphanie S Bleykasten Claudine C De Montigny Jacky J Jacques Noemie N Jung Paul P Lemaire Marc M Mallet Sandrine S Morel Guillaume G Richard Guy-Franck GF Sarkar Anasua A Savel Guilhem G Schacherer Joseph J Seret Marie-Line ML Talla Emmanuel E Samson Gaelle G Jubin Claire C Poulain Julie J Vacherie Benoît B Barbe Valérie V Pelletier Eric E Sherman David J DJ Westhof Eric E Weissenbach Jean J Baret Philippe V PV Wincker Patrick P Gaillardin Claude C Dujon Bernard B Souciet Jean-Luc JL

G3 (Bethesda, Md.) 20120201 2

Polyploidization is an important process in the evolution of eukaryotic genomes, but ensuing molecular mechanisms remain to be clarified. Autopolyploidization or whole-genome duplication events frequently are resolved in resulting lineages by the loss of single genes from most duplicated pairs, causing transient gene dosage imbalance and accelerating speciation through meiotic infertility. Allopolyploidization or formation of interspecies hybrids raises the problem of genetic incompatibility (Ba ...[more]

PMID: 22384408

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Project description:BACKGROUND:Genomic studies on fungal species with hydrolytic activity have gained increased attention due to their great biotechnological potential for biomass-based biofuel production. The amylolytic yeast Saccharomycopsis fibuligera has served as a good source of enzymes and genes involved in saccharification. Despite its long history of use in food fermentation and bioethanol production, very little is known about the basic physiology and genomic features of S. fibuligera. RESULTS:We performed whole-genome (WG) de novo sequencing and complete assembly of S. fibuligera KJJ81 and KPH12, two isolates from wheat-based Nuruk in Korea. Intriguingly, the KJJ81 genome (~38 Mb) was revealed as a hybrid between the KPH12 genome (~18 Mb) and another unidentified genome sharing 88.1% nucleotide identity with the KPH12 genome. The seven chromosome pairs of KJJ81 subgenomes exhibit highly conserved synteny, indicating a very recent hybridization event. The phylogeny inferred from WG comparisons showed an early divergence of S. fibuligera before the separation of the CTG and Saccharomycetaceae clades in the subphylum Saccharomycotina. Reconstructed carbon and sulfur metabolic pathways, coupled with RNA-Seq analysis, suggested a marginal Crabtree effect under high glucose and activation of sulfur metabolism toward methionine biosynthesis under sulfur limitation in this yeast. Notably, the lack of sulfate assimilation genes in the S. fibuligera genome reflects a unique phenotype for Saccharomycopsis clades as natural sulfur auxotrophs. Extended gene families, including novel genes involved in saccharification and proteolysis, were identified. Moreover, comparative genome analysis of S. fibuligera ATCC 36309, an isolate from chalky rye bread in Germany, revealed that an interchromosomal translocation occurred in the KPH12 genome before the generation of the KJJ81 hybrid genome. CONCLUSIONS:The completely sequenced S. fibuligera genome with high-quality annotation and RNA-Seq analysis establishes an important foundation for functional inference of S. fibuligera in the degradation of fermentation mash. The gene inventory facilitates the discovery of new genes applicable to the production of novel valuable enzymes and chemicals. Moreover, as the first gapless genome assembly in the genus Saccharomycopsis including members with desirable traits for bioconversion, the unique genomic features of S. fibuligera and its hybrid will provide in-depth insights into fungal genome dynamics as evolutionary adaptation.

Dataset Information

Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization.

Publications

Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization.

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