Population genomics reveals gene flow and positive selection patterns in the wine-related yeast Hanseniaspora uvarum

Ruiqi Ma , Hui Wang , Yue Wei , Yue Sun , Jie Xue , Yi Qin , Shiheng Tao , Yanlin Liu

Stress Biology ›› 2026, Vol. 6 ›› Issue (1) : 54

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Stress Biology ›› 2026, Vol. 6 ›› Issue (1) :54 DOI: 10.1007/s44154-026-00319-z
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Population genomics reveals gene flow and positive selection patterns in the wine-related yeast Hanseniaspora uvarum
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Abstract

Hanseniaspora uvarum is a representative non-Saccharomyces species that plays a significant role in fermentation processes such as winemaking. In recent years, this species has gained attention in food engineering and evolutionary biology. However, the population genomic signatures in this species remain poorly understood. In this study, a population genomics analysis was conducted on 151 H. uvarum strains (45 from Ningxia, China; 21 from other regions of China; 67 from Australia; and 18 from other regions or of unspecified origin), and a pangenome analysis was performed on 159 strains, incorporating eight additional genome assemblies. Phylogenetic analysis, ancestry coefficient analysis, and principal component analysis generally distinguished Chinese strains from those sampled on other continents. However, substantial post-divergence gene flow and introgression were inferred between intercontinentally paired clades. Positively selected candidate genes exhibited region-specific patterns: GO terms related to the positive regulation of filamentous growth in response to external stimuli were significantly enriched in the Ningxia strains; the stress-related GO term “cytoplasmic stress granule” was significantly enriched in both the Ningxia and Australian strains, but with distinct sets of associated genes. Although the samples were primarily isolated from anthropogenic environments, H. uvarum exhibited an open pangenome, indicating substantial adaptive potential to diverse stresses. This study advances our understanding of the evolutionary dynamics of H. uvarum and establishes a genomic foundation for future ecological and industrial research on this yeast.

Keywords

Hanseniaspora uvarum / Non-Saccharomyces yeasts / Population genomics / Gene flow / Positive selection / Pangenome

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Ruiqi Ma, Hui Wang, Yue Wei, Yue Sun, Jie Xue, Yi Qin, Shiheng Tao, Yanlin Liu. Population genomics reveals gene flow and positive selection patterns in the wine-related yeast Hanseniaspora uvarum. Stress Biology, 2026, 6 (1) : 54 DOI:10.1007/s44154-026-00319-z

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References

[1]

Alachiotis N, Pavlidis P. RAiSD detects positive selection based on multiple signatures of a selective sweep and SNP vectors. Commun Biol, 2018, 1: 79

[2]

Albertin W, Setati ME, Miot-Sertier C, Mostert TT, Colonna-Ceccaldi B, Coulon J, Girard P, Moine V, Pillet M, Salin F, Bely M, Divol B, Masneuf-Pomarede I. Hanseniaspora uvarum from winemaking environments show spatial and temporal genetic clustering. Front Microbiol, 2016, 6: 1569

[3]

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res, 2009, 19: 1655-1664

[4]

Alonge M, Lebeigle L, Kirsche M, Jenike K, Ou S, Aganezov S, Wang X, Lippman ZB, Schatz MC, Soyk S. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol, 2022, 23: 258

[5]

Arias CR, Burns JK, Friedrich LM, Goodrich RM, Parish ME. Yeast species associated with orange juice: evaluation of different identification methods. Appl Environ Microbiol, 2002, 68: 1955-1961

[6]

Astashyn A, Tvedte ES, Sweeney D, Sapojnikov V, Bouk N, Joukov V, Mozes E, Strope PK, Sylla PM, Wagner L, Bidwell SL, Brown LC, Clark K, Davis EW, Smith-White B, Hlavina W, Pruitt KD, Schneider VA, Murphy TD. Rapid and sensitive detection of genome contamination at scale with FCS-GX. Genome Biol, 2024, 25 ArticleID: 60

[7]

Bhatia G, Patterson N, Sankararaman S, Price AL. Estimating and interpreting FST: the impact of rare variants. Genome Res, 2013, 23: 1514-1521

[8]

Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature, 2002, 419: 411-415

[9]

Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJN, van Wezel GP, Medema MH, Weber T. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res, 2023, 51: W46-W50

[10]

Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol, 2021, 38: 5825-5829

[11]

Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience, 2015, 4: 375-394

[12]

Chen S. Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp. iMeta, 2023, 2 ArticleID: e107

[13]

Cheng X, Côté V, Côté J. NuA4 and SAGA acetyltransferase complexes cooperate for repair of DNA breaks by homologous recombination. PLoS Genet, 2021, 17 ArticleID: e1009459

[14]

Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, Li H. Twelve years of SAMtools and BCFtools. GigaScience, 2021, 10 ArticleID: giab008

[15]

Dellacassa E, Trenchs O, Fariña L, Debernardis F, Perez G, Boido E, Carrau F. Pineapple (Ananas comosus L. Merr.) wine production in Angola: characterisation of volatile aroma compounds and yeast native flora. Int J Food Microbiol, 2017, 241: 161-167

[16]

Drumonde-Neves J, Fernandes T, Lima T, Pais C, Franco-Duarte R. Learning from 80 years of studies: a comprehensive catalogue of non-Saccharomyces yeasts associated with viticulture and winemaking. FEMS Yeast Res, 2021, 21 ArticleID: foab017

[17]

Duan S-F, Han P-J, Wang Q-M, Liu W-Q, Shi J-Y, Li K, Zhang X-L, Bai F-Y. The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nat Commun, 2018, 9 ArticleID: 2690

[18]

Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol, 2019, 20: 238

[19]

Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 2003, 164: 1567-1587

[20]

Farris JS, Albert VA, Källersjö M, Lipscomb D, Kluge AG. Parsimony jackknifing outperforms neighbor-joining. Cladistics, 1996, 12: 99-124

[21]

Feng L, Wang J, Ye D, Song Y, Qin Y, Liu Y. Yeast population dynamics during spontaneous fermentation of icewine and selection of indigenous Saccharomyces cerevisiae strains for the winemaking in Qilian, China. J Sci Food Agric, 2020, 100: 5385-5394

[22]

Figueroa-Hernández C, Mota-Gutierrez J, Ferrocino I, Hernández-Estrada ZJ, González-Ríos O, Cocolin L, Suárez-Quiroz ML. The challenges and perspectives of the selection of starter cultures for fermented cocoa beans. Int J Food Microbiol, 2019, 301: 41-50

[23]

Fitak RR. OptM: estimating the optimal number of migration edges on population trees using Treemix. Biol Methods Protoc, 2021, 6 ArticleID: bpab017

[24]

Frichot E, Mathieu F, Trouillon T, Bouchard G, François O. Fast and efficient estimation of individual ancestry coefficients. Genetics, 2014, 196: 973-983

[25]

González B, Vázquez J, Cullen PJ, Mas A, Beltran G, Torija M-J. Aromatic amino acid-derived compounds induce morphological changes and modulate the cell growth of wine yeast species. Front Microbiol, 2018, 9: 670

[26]

Grousl T, Vojtova J, Hasek J, Vomastek T (2022) Yeast stress granules at a glance. Yeast 39:247–261. https://doi.org/10.1002/yea.3681

[27]

Guaragnella N, Chiara M, Capece A, Romano P, Pietrafesa R, Siesto G, Manzari C, Pesole G. Genome sequencing and comparative analysis of three Hanseniaspora uvarum indigenous wine strains reveal remarkable biotechnological potential. Front Microbiol, 2020, 10 ArticleID: fmicb.2019.03133

[28]

Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics, 2013, 29: 1072-1075

[29]

Haase MAB, Steenwyk JL, Boeke JD (2024) Gene loss and cis-regulatory novelty shaped core histone gene evolution in the apiculate yeast Hanseniaspora uvarum. Genetics 226:iyae008. https://doi.org/10.1093/genetics/iyae008

[30]

Hu K, Jin G-J, Xu Y-H, Tao Y-S. Wine aroma response to different participation of selected Hanseniaspora uvarum in mixed fermentation with Saccharomyces cerevisiae. Food Res Int, 2018, 108: 119-127

[31]

Hu J, Fan J, Sun Z, Liu S. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics, 2019, 36: 2253-2255

[32]

Hudson RR, Slatkin M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics, 1992, 132: 583-589

[33]

Kahlke T, Ralph PJ. BASTA – taxonomic classification of sequences and sequence bins using last common ancestor estimations. Methods Ecol Evol, 2019, 10: 100-103

[34]

Korunes KL, Samuk K. pixy: unbiased estimation of nucleotide diversity and divergence in the presence of missing data. Mol Ecol Resour, 2021, 21: 1359-1368

[35]

Lee TJ, Liu Y-C, Liu W-A, Lin Y-F, Lee H-H, Ke H-M, Huang J-P, Lu M-YJ, Hsieh C-L, Chung K-F, Liti G, Tsai IJ. Extensive sampling of Saccharomyces cerevisiae in Taiwan reveals ecology and evolution of predomesticated lineages. Genome Res, 2022, 32: 864-877

[36]

Li R, Feng D, Wang H, Zhang Z, Li N, Sun Y. Genetic diversity of non-Saccharomyces yeasts associated with spontaneous fermentation of Cabernet Sauvignon wines from Ningxia, China. Front Microbiol, 2023, 14 ArticleID: fmicb.2023.1253969

[37]

Ludlow CL, Cromie GA, Garmendia-Torres C, Sirr A, Hays M, Field C, Jeffery EW, Fay JC, Dudley AM. Independent origins of yeast associated with coffee and cacao fermentation. Curr Biol, 2016, 26: 965-971

[38]

Malinsky M, Svardal H, Tyers AM, Miska EA, Genner MJ, Turner GF, Durbin R. Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nat Ecol Evol, 2018, 2: 1940-1955

[39]

Malinsky M, Matschiner M, Svardal H. Dsuite - fast D-statistics and related admixture evidence from VCF files. Mol Ecol Resour, 2021, 21: 584-595

[40]

Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen W-M. Robust relationship inference in genome-wide association studies. Bioinformatics, 2010, 26: 2867-2873

[41]

Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. BUSCO Update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol, 2021, 38: 4647-4654

[42]

Marr RA, Moore J, Formby S, Martiniuk JT, Hamilton J, Ralli S, Konwar K, Rajasundaram N, Hahn A, Measday V. Whole genome sequencing of Canadian Saccharomyces cerevisiae strains isolated from spontaneous wine fermentations reveals a new Pacific West Coast Wine clade. G3 Bethesda, 2023, 13 ArticleID: jkad130

[43]

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A. Pfam: the protein families database in 2021. Nucleic Acids Res, 2020, 49: D412-D419

[44]

Onetto CA, Ward CM, Varela C, Hale L, Schmidt SA, Borneman AR (2025) Genetic and phenotypic diversity of wine-associated Hanseniaspora species. FEMS Yeast Res 25:foaf031. https://doi.org/10.1093/femsyr/foaf031

[45]

Ou S, Su W, Liao Y, Chougule K, Agda JRA, Hellinga AJ, Lugo CSB, Elliott TA, Ware D, Peterson T, Jiang N, Hirsch CN, Hufford MB. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol, 2019, 20: 275

[46]

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 2019, 35: 526-528

[47]

Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet, 2006, 2 ArticleID: e190

[48]

Paysan-Lafosse T, Blum M, Chuguransky S, Grego T, Pinto BL, Salazar GA, Bileschi ML, Bork P, Bridge A, Colwell L, Gough J, Haft DH, Letunić I, Marchler-Bauer A, Mi H, Natale DA, Orengo CA, Pandurangan AP, Rivoire C, Sigrist CJA, Sillitoe I, Thanki N, Thomas PD, Tosatto SCE, Wu CH, Bateman A. InterPro in 2022. Nucleic Acids Res, 2022, 51: D418-D427

[49]

Pereira GVdM, Soccol VT, Soccol CR. Current state of research on cocoa and coffee fermentations. Curr Opin Food Sci, 2016, 7: 50-57

[50]

Peter J, De Chiara M, Friedrich A, Yue J-X, Pflieger D, Bergström A, Sigwalt A, Barre B, Freel K, Llored A, Cruaud C, Labadie K, Aury J-M, Istace B, Lebrigand K, Barbry P, Engelen S, Lemainque A, Wincker P, Liti G, Schacherer J. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature, 2018, 556: 339-344

[51]

Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet, 2012, 8 ArticleID: e1002967

[52]

Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet, 2006, 38: 904-909

[53]

Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics, 2020, 70 ArticleID: e102

[54]

Pryszcz LP, Gabaldón T. Redundans: an assembly pipeline for highly heterozygous genomes. Nucleic Acids Res, 2016, 44: e113-e113

[55]

Ramachandran S, Haddad D, Li C, Le MX, Ling AK, So CC, Nepal RM, Gommerman JL, Yu K, Ketela T, Moffat J, Martin A. The SAGA deubiquitination module promotes DNA repair and class switch recombination through ATM and DNAPK-mediated γH2AX formation. Cell Rep, 2016, 15: 1554-1565

[56]

Rawlings ND, Barrett AJ, Thomas PD, Huang X, Bateman A, Finn RD. The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res, 2017, 46: D624-D632

[57]

Saubin M, Devillers H, Proust L, Brier C, Grondin C, Pradal M, Legras J-L, Neuvéglise C. Investigation of genetic relationships between Hanseniaspora species found in grape musts revealed interspecific hybrids with dynamic genome structures. Front Microbiol, 2020, 10 ArticleID: 2960

[58]

Stanke M, Diekhans M, Baertsch R, Haussler D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics, 2008, 24: 637-644

[59]

Steenwyk JL, Opulente DA, Kominek J, Shen X-X, Zhou X, Labella AL, Bradley NP, Eichman BF, Čadež N, Libkind D, DeVirgilio J, Hulfachor AB, Kurtzman CP, Hittinger CT, Rokas A. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. PLoS Biol, 2019, 17 ArticleID: e3000255

[60]

Sternes PR, Lee D, Kutyna DR, Borneman AR. A combined meta-barcoding and shotgun metagenomic analysis of spontaneous wine fermentation. GigaScience, 2017, 6 ArticleID: gix040

[61]

Strope PK, Skelly DA, Kozmin SG, Mahadevan G, Stone EA, Magwene PM, Dietrich FS, McCusker JH. The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res, 2015, 25: 762-774

[62]

Sun Q, An P, Li P, Wang H, Tao S, Liu Y. Unraveling time-resolved transcriptional and metabolic shifts in the mixed fermentation of Saccharomyces cerevisiae and Hanseniaspora uvarum. J Agric Food Chem, 2025, 73: 12418-12432

[63]

Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res, 2008, 18: 1979-1990

[64]

Tettelin H, Riley D, Cattuto C, Medini D. Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol, 2008, 11: 472-477

[65]

The UniProt Consortium. UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Res, 2022, 51: D523-D531

[66]

Tian Z, Du Y, Yang F, Zhao J, Liu S, Zhang D, Long CA. Chromosome genome sequencing and comparative transcriptome-based analyses of Kloeckera apiculata 34-9 unveil the potential biocontrol mechanisms against Citrus Green Mold. Front Microbiol, 2021, 12 ArticleID: fmicb.2021.752529

[67]

Tristezza M, Tufariello M, Capozzi V, Spano G, Mita G, Grieco F. The oenological potential of Hanseniaspora uvarum in simultaneous and sequential co-fermentation with Saccharomyces cerevisiae for industrial wine production. Front Microbiol, 2016, 7 ArticleID: fmicb.2016.00670

[68]

Valles BS, Bedriñana RP, Tascón NF, Simón AQ, Madrera RR. Yeast species associated with the spontaneous fermentation of cider. Food Microbiol, 2007, 24: 25-31

[69]

Van der Auwera GA, O'Connor BD. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra, 2020, Sebastopol (CA), USA, O'Reilly Media Inc

[70]

Vasimuddin M, Misra S, Li H, Aluru S. Efficient Architecture-Aware Acceleration of BWA-MEM for Multicore Systems. 2019 IEEE Int Parallel Distributed Process Symposium (IPDPS), 2019, 2019: 314-324

[71]

Wang J, Wang Z, Gao H, Bai X, Li L, Wei R, Dong Z. Metabolomics and flavor diversity in Cabernet Sauvignon wines fermented by various origins of Hanseniaspora uvarum in the presence and absence of Saccharomyces cerevisiae. LWT, 2024, 203 ArticleID: 116396

[72]

Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, Fu X, Liu S, Bo X, Yu G (2021) clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innovation 2:100141. https://doi.org/10.1016/j.xinn.2021.100141

[73]

Yang H, Wei Y, Feng W, Zhang H, Jiang J, Qin Y. Screening of indigenous Hanseniaspora strains from China for ethanol reduction in wine. Foods, 2025, 14 ArticleID: 1113

[74]

Yu G, Lam TT-Y, Zhu H, Guan Y. Two methods for mapping and visualizing associated data on phylogeny using Ggtree. Mol Biol Evol, 2018, 35: 3041-3043

[75]

Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res, 2018, 46: W95-W101

[76]

Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 2012, 28: 3326-3328

Funding

National Natural Science Key Foundation of China(U21A20269)

National Natural Science Foundation of China(32171458)

Earmarked Fund for China Agriculture Research System(CARS-29-jg-3)

Special project of scientific and technological innovation of Xinjiang Research Institute of Arid Area Agriculture (XJHQNY-2025-7)

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