Hanseniaspora uvarum from Winemaking Environments Show Spatial and Temporal Genetic Clustering
Open accessAbstract
Hanseniaspora uvarum is one of the most abundant yeast species found on grapes and in grape must, at least before the onset of alcoholic fermentation (AF) which is usually performed by Saccharomyces species. The aim of this study was to characterize the genetic and phenotypic variability within the H. uvarum species. One hundred and fifteen strains isolated from winemaking environments in different geographical origins were analyzed using 11 microsatellite markers and a subset of 47 strains were analyzed by AFLP. H. uvarum isolates clustered mainly on the basis of their geographical localization as revealed by microsatellites. In addition, a strong clustering based on year of isolation was evidenced, indicating that the genetic diversity of H. uvarum isolates was related to both spatial and temporal variations. Conversely, clustering analysis based on AFLP data provided a different picture with groups showing no particular characteristics, but provided higher strain discrimination. This result indicated that AFLP approaches are inadequate to establish the genetic relationship between individuals, but allowed good strain discrimination. At the phenotypic level, several extracellular enzymatic activities of enological relevance (pectinase, chitinase, protease, β-glucosidase) were measured but showed low diversity. The impact of environmental factors of enological interest (temperature, anaerobia, and copper addition) on growth was also assessed and showed poor variation. Altogether, this work provided both new analytical tool (microsatellites) and new insights into the genetic and phenotypic diversity of H. uvarum, a yeast species that has previously been identified as a potential candidate for co-inoculation in grape must, but whose intraspecific variability had never been fully assessed.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Hanseniaspora species are widespread and frequent in the environment, mostly studied with respect to their occurrence on grapes and winemaking, and their antagonistic activity against green mould of citrus or B. cinerea has been shown.
“Hanseniaspora species are widespread and frequent in the environment, mostly studied with respect to their occurrence on grapes and winemaking, and their antagonistic activity against green mould of citrus or B. cinerea was shown [78–82].”
From Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi (2017) · cites this paper as [80]
The Introduction describes H. uvarum as occurring in diverse environments, frequently on grapes and in fermentation, and reports its antagonistic properties against Botrytis cinerea and Penicillium spp. on citrus. It does not establish these claims for Hanseniaspora species generally, say that they have mostly been studied in relation to grapes and winemaking, or specifically identify the citrus disease as green mould. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
No references could be resolved yet.
Research works printed but not linked: 108
- Agrawal T. Kotasthane A. S. (2012). Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India. Springerplus 1: 73. 10.1186/2193-1801-1-73 23526575 PMC3602610 · DOI
- Albertin W. Chasseriaud L. Comte G. Panfili A. Delcamp A. Salin F.. (2014a). Winemaking and bioprocesses strongly shaped the genetic diversity of the ubiquitous yeast Torulaspora delbrueckii. PLoS ONE 9: e94246. 10.1371/journal.pone.0094246 24718638 PMC3981792 · DOI
- Albertin W. Miot-Sertier C. Bely M. Marullo P. Coulon J. Moine V.. (2014b). Oenological prefermentation practices strongly impact yeast population dynamics and alcoholic fermentation kinetics in Chardonnay grape must. Int. J. Food Microbiol. 178, 87– 97. 10.1016/j.ijfoodmicro.2014.03.009 24681710 · DOI
- Albertin W. Panfili A. Miot-Sertier C. Goulielmakis A. Delcamp A. Salin F.. (2014c). Development of microsatellite markers for the rapid and reliable genotyping of Brettanomyces bruxellensis at strain level. Food Microbiol. 42, 188– 195. 10.1016/j.fm.2014.03.012 24929736 · DOI
- Almeida P. Gonçalves C. Teixeira S. Libkind D. Bontrager M. Masneuf-Pomarède I.. (2014). A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nat. Commun. 5: 4044. 10.1038/ncomms5044 24887054 PMC5081218 · DOI
- Angioni A. Caboni P. Garau A. Farris A. Orro D. Budroni M.. (2007). In vitro interaction between ochratoxin A and different strains of Saccharomyces cerevisiae and Kloeckera apiculata. J. Agric. Food Chem. 55, 2043– 2048. 10.1021/jf062768u 17279767 · DOI
- Basha H. Ramanujam B. (2014). Growth promotion effect of Pichia guilliermondii in chilli and biocontrol potential of Hanseniaspora uvarum against Colletotrichum capsici causing fruit rot. Biocont. Sci. Technol. 25, 185– 206. 10.1080/09583157.2014.968092 · DOI · Paper page
- Batista N. N. Ramos C. L. Ribeiro D. D. Pinheiro A. C. M. Schwan R. F. (2015). Dynamic behavior of Saccharomyces cerevisiae, Pichia kluyveri and Hanseniaspora uvarum during spontaneous and inoculated cocoa fermentations and their effect on sensory characteristics of chocolate. LWT Food Sci. Technol. 63, 221– 227. 10.1016/j.lwt.2015.03.051 · DOI
- Beltran G. Torija M. J. Novo M. Ferrer N. Poblet M. Guillamón J. M.. (2002). Analysis of yeast populations during alcoholic fermentation: a six year follow-up study. Syst. Appl. Microbiol. 25, 287– 293. 10.1078/0723-2020-00097 12353885 · DOI
- Bilbao A. Irastorza A. Dueñas M. Fernandez K. (1997). The effect of temperature on the growth of strains of Kloeckera apiculata and Saccharomyces cerevisiae in apple juice fermentation. Lett. Appl. Microbiol. 24, 37– 39. 10.1046/j.1472-765X.1997.00340.x 9024002 · DOI
- Bilinski C. A. Russell I. Stewart G. G. (1987). Applicability of yeast extracellular proteinases in brewing: physiological and biochemical aspects. Appl. Environ. Microbiol. 53, 495– 499. 16347298 PMC203694
- Bruvo R. Michiels N. K. D'souza T. G. Schulenburg H. (2004). A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101– 2106. 10.1111/j.1365-294X.2004.02209.x 15189230 · DOI
- Cabranes C. Mangas J. J. Blanco D. (1997). Selection and biochemical characterisation of Saccharomyces cerevisiae and Kloeckera apiculata strains isolated from spanish cider. J. Inst. Brew. 103, 165– 169. 10.1002/j.2050-0416.1997.tb00945.x · DOI
- Cai Z. Yang R. Xiao H. Qin X. Si L. (2015). Effect of preharvest application of Hanseniaspora uvarum on postharvest diseases in strawberries. Postharvest Biol. Technol. 100, 52– 58. 10.1016/j.postharvbio.2014.09.004 · DOI
- Capece A. Fiore C. Maraz A. Romano P. (2005). Molecular and technological approaches to evaluate strain biodiversity in Hanseniaspora uvarum of wine origin. J. Appl. Microbiol. 98, 136– 144. 10.1111/j.1365-2672.2004.02434.x 15610426 · DOI
- Capriotti A. (1955). Yeasts in some Netherlands soils. Antonie Van Leeuwenhoek 21, 145– 156. 10.1007/BF02543809 14388635 · DOI
- Caruso M. Capece A. Salzano G. Romano P. (2002). Typing of Saccharomyces cerevisiae and Kloeckera apiculata strains from Aglianico wine. Lett. Appl. Microbiol. 34, 323– 328. 10.1046/j.1472-765X.2002.01090.x 11967053 · DOI
- Charoenchai C. Fleet G. H. Henschke P. A. Todd B. E. N. T. (1997). Screening of non-Saccharomyces wine yeasts for the presence of extracellular hydrolytic enzymes. Aust. J. Grape Wine Res. 3, 2– 8. 10.1111/j.1755-0238.1997.tb00109.x · DOI
- Ciani M. Beco L. Comitini F. (2006). Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations. Int. J. Food Microbiol. 108, 239– 245. 10.1016/j.ijfoodmicro.2005.11.012 16487611 · DOI
- Codon A. C. Gasentramirez J. M. Benitez T. (1995). Factors which affect the frequency of sporulation and tetrad formation in Saccharomyces cerevisiae bakers yeasts. Appl. Environ. Microbiol. 61, 1677– 1677. 16535013 PMC1388431
- Combina M. Elía A. Mercado L. Catania C. Ganga A. Martinez C. (2005). Dynamics of indigenous yeast populations during spontaneous fermentation of wines from Mendoza, Argentina. Int. J. Food Microbiol. 99, 237– 243. 10.1016/j.ijfoodmicro.2004.08.017 15808358 · DOI
- Comi G. Romano P. Cocolin L. Fiore C. (2001). Characterization of Kloeckera apiculata strains from the Friuli region in Northern Italy. World J. Microbiol. Biotechnol. 17, 391– 394. 10.1023/A:1016731420425 · DOI
- Comitini F. Ciani M. (2010). The zymocidial activity of Tetrapisispora phaffii in the control of Hanseniaspora uvarum during the early stages of winemaking. Lett. Appl. Microbiol. 50, 50– 56. 10.1111/j.1472-765X.2009.02754.x 19874485 · DOI
- de Araujo F. V. Soares C. A. G. Hagler A. N. Mendonça-Hagler L. C. (1995). Ascomycetous yeast communities of marine invertebrates in a Southeast Brazilian mangrove ecosystem. Antonie Van Leeuwenhoek 68, 91– 99. 10.1007/BF00873096 8546456 · DOI
- de Arruda Moura Pietrowski G. Grochoski M. Sartori G. F. Gomes T. A. Wosiacki G. Nogueira A. (2015). Viability of Hanseniaspora uvarum yeast preserved by lyophilization and cryopreservation. Yeast 32, 559– 565. 10.1002/yea.3079 26095929 · DOI
- Emmanouil-Nikoloussi E. Kanellaki-Kyparissi M. Papavassiliou P. Koliakos K. Dermentzopoulou M. Foroglou C. (1994). “Hanseniaspora uvarum” the ultrastructural morphology of a rare ascomycete, isolated from oral thrush. Bull. Group. Int. Rech. Sci. Stomatol. Odontol. 37, 13– 17. 7994154
- Esteve-Zarzoso B. Belloch C. Uruburu F. Querol A. (1999). Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. Int. J. Syst. Bacteriol. 49, 329– 337. 10.1099/00207713-49-1-329 10028278 · DOI
- Esteve-Zarzoso B. Hierro N. Mas A. Guillamon J. M. (2010). A new simplified AFLP method for wine yeast strain typing. LWT Food Sci. Technol. 43, 1480– 1484. 10.1016/j.lwt.2010.05.016 · DOI
- Esteve-Zarzoso B. Peris-Torán M. Ramón D. Querol A. (2001). Molecular characterisation of Hanseniaspora species. Antonie Van Leeuwenhoek 80, 85– 92. 10.1023/A:1012268931569 11761370 · DOI
- Farías M. E. Manca de Nadra M. C. (2003). Flocculation and cell surface characterization of Kloeckera apiculata from wine. J. Appl. Microbiol. 95, 457– 462. 10.1046/j.1365-2672.2003.01994.x 12911692 · DOI
- Gao C. Fleet G. H. (1988). The effects of temperature and pH on the ethanol tolerance of the wine yeasts, Saccharomyces cerevisiae, Candida stellata and Kloeckera apiculata. J. Appl. Bacteriol. 65, 405– 409. 10.1111/j.1365-2672.1988.tb01909.x · DOI
- Garcia-Martos P. Hernandez-Molina J. M. Galan F. Ruiz-Henestrosa J. R. Garcia-Agudo R. J. P. M. Mira J. (1999). Isolation of Hanseniaspora uvarum (Kloeckera apiculata) in humans. Mycopathologia 144, 73– 75. 10.1023/A:1006900909455 10481287 · DOI
- Gaudeul M. Till-Bottraud I. Barjon F. Manel S. (2004). Genetic diversity and differentiation in Eryngium alpinum L. (Apiaceae): comparison of AFLP and microsatellite markers. Heredity 92, 508– 518. 10.1038/sj.hdy.6800443 15014426 · DOI
- Ghosh S. (2015). Metagenomic Screening of Cell Wall Hydrolases, Their Anti-Fungal Activities and Potential Role in Wine Fermentation. Ph.D. thesis, Stellenbosch University.
- Granchi L. Bosco M. Messini A. Vincenzini M. (1999). Rapid detection and quantification of yeast species during spontaneous wine fermentation by PCR-RFLP analysis of the rDNA ITS region. J. Appl. Microbiol. 87, 949– 956. 10.1046/j.1365-2672.1999.00600.x 10692077 · DOI
- Grangeteau C. Gerhards D. Rousseaux S. von Wallbrunn C. Alexandre H. Guilloux-Benatier M. (2015). Diversity of yeast strains of the genus Hanseniaspora in the winery environment: what is their involvement in grape must fermentation? Food Microbiol. 50, 70– 77. 10.1016/j.fm.2015.03.009 25998817 · DOI
- Heard G. M. Fleet G. H. (1985). Growth of natural yeast flora during the fermentation of inoculated wines. Appl. Environ. Microbiol. 50, 727– 728. 16346894 PMC238702
- Heard G. M. Fleet G. H. (1988). The effects of temperature and pH on the growth of yeast species during the fermentation of grape juice. J. Appl. Bacteriol. 65, 23– 28. 10.1111/j.1365-2672.1988.tb04312.x · DOI
- Hierro N. González Á. Mas A. Guillamón J. M. (2006). Diversity and evolution of non-Saccharomyces yeast populations during wine fermentation: effect of grape ripeness and cold maceration. FEMS Yeast Res. 6, 102– 111. 10.1111/j.1567-1364.2005.00014.x 16423075 · DOI
- Hoffman C. S. (2001). Preparation of yeast DNA, in Current Protocols in Molecular Biology, eds Ausubel F. M. Brent R. Kingston R. E. Moore D. D. Seidman J. G. Smith J. A. Struhl K. (John Wiley & Sons Inc), 13.11.11– 13.11.14.
- Holloway P. Subden R. E. Lachance M. A. (1990). The yeasts in a riesling must from the Niagara grape-growing region of Ontario. Can. Inst. Food Sci. Technol. J. 23, 212– 216. 10.1016/S0315-5463(90)70245-3 · DOI
- Hong Y.-A. Park H.-D. (2013). Role of non-Saccharomyces yeasts in Korean wines produced from Campbell early grapes: potential use of Hanseniaspora uvarum as a starter culture. Food Microbiol. 34, 207– 214. 10.1016/j.fm.2012.12.011 23498200 · DOI
- Jones C. J. Edwards K. J. Castaglione S. Winfield M. O. Sala F. van de Wiel C. (1997). Reproducibility testing of RAPD, AFLP and SSR markers in plants by a network of European laboratories. Mol. Breed. 3, 381– 390. 10.1023/A:1009612517139 · DOI
- Kachalkin A. V. Abdullabekova D. A. Magomedova E. S. Magomedov G. G. Chernov I. Y. (2015). Yeasts of the vineyards in Dagestan and other regions. Microbiology 84, 425– 432. 10.1134/S002626171503008X 26263696 · DOI
- Kocan R. M. Hasenclever H. F. (1972). Normal yeast flora of the upper digestive tract of some wild columbids. J. Wildl. Dis. 8, 365– 368. 10.7589/0090-3558-8.4.365 4564184 · DOI
- Kosse D. Seiler H. Amann R. Ludwig W. Scherer S. (1997). Identification of Yoghurt-spoiling Yeasts with 18S rRNA-targeted Oligonucleotide Probes. Syst. Appl. Microbiol. 20, 468– 480. 10.1016/S0723-2020(97)80016-1 · DOI
- Kurtzman C. P. Fell J. W. Boekhout T. (2011). The Yeasts: A Taxonomic Study. Amsterdam: Elsevier.
- Kurtzman C. P. Robnett C. J. (1998). Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73, 331– 371. 10.1023/A:1001761008817 9850420 · DOI
- Lachance M.-A. (1995). Yeast communities in a natural tequila fermentation. Antonie Van Leeuwenhoek 68, 151– 160. 10.1007/BF00873100 8546452 · DOI
- Lam S. S. Howell K. S. (2015). Drosophila-associated yeast species in vineyard ecosystems. FEMS Microbiol Lett 362. 10.1093/femsle/fnv170 26391524 · DOI
- Legras J. L. Ruh O. Merdinoglu D. Karst F. (2005). Selection of hypervariable microsatellite loci for the characterization of Saccharomyces cerevisiae strains. Int. J. Food Microbiol. 102, 73– 83. 10.1016/j.ijfoodmicro.2004.12.007 15925004 · DOI
- Li S.-S. Cheng C. Li Z. Chen J.-Y. Yan B. Han B.-Z.. (2010). Yeast species associated with wine grapes in China. Int. J. Food Microbiol. 138, 85– 90. 10.1016/j.ijfoodmicro.2010.01.009 20116124 · DOI
- Liu H. Guo J. Cheng Y. Luo L. Liu P. Wang B. (2010a). Control of gray mold of grape by Hanseniaspora uvarum and its effects on postharvest quality parameters. Ann. Microbiol. 60, 31– 35. 10.1007/s13213-010-0018-3 · DOI
- Liu H. M. Guo J. H. Luo L. Liu P. Wang B. Q. Cheng Y. J. (2010b). Improvement of Hanseniaspora uvarum biocontrol activity against gray mold by the addition of ammonium molybdate and the possible mechanisms involved. Crop Prot. 29, 277– 282. 10.1016/j.cropro.2009.10.020 · DOI
- Liu P. Cheng Y. Yang M. Liu Y. Chen K. Long C. A.. (2014). Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol. 14: 242. 10.1186/s12866-014-0242-2 25230758 PMC4177429 · DOI
- Long C.-A. Wu Z. Deng B.-X. (2005). Biological control of Penicillium italicum of Citrus and Botrytis cinerea of grape by strain 34–9 of Kloeckera apiculata. Eur. Food Res. Technol. 221, 197– 201. 10.1007/s00217-005-1199-z · DOI
- Manzanares P. Ramón D. Querol A. (1999). Screening of non-Saccharomyces wine yeasts for the production of β-D-xylosidase activity. Int. J. Food Microbiol. 46, 105– 112. 10.1016/S0168-1605(98)00186-X 10728611 · DOI
- Mariette S. Chagné D. Lézier C. Pastuszka P. Raffin A. Plomion C.. (2001). Genetic diversity within and among Pinus pinaster populations: comparison between AFLP and microsatellite markers. Heredity 86, 469– 479. 10.1046/j.1365-2540.2001.00852.x 11520347 · DOI
- Masneuf-Pomarede I. Juquin E. Miot-Sertier C. Renault P. Laizet Y. H. Salin F.. (2015). The yeast Starmerella bacillaris (synonym Candida zemplinina) shows high genetic diversity in winemaking environments. FEMS Yeast Res. 15: fov045. 10.1093/femsyr/fov045 26071435 · DOI
- Masoud W. Bjørg Cesar L. Jespersen L. Jakobsen M. (2004). Yeast involved in fermentation of Coffea arabica in East Africa determined by genotyping and by direct denaturating gradient gel electrophoresis. Yeast 21, 549– 556. 10.1002/yea.1124 15164358 · DOI
- Mateo J. J. Jimenez M. Huerta T. Pastor A. (1991). Contribution of different yeasts isolated from musts of monastrell grapes to the aroma of wine. Int. J. Food Microbiol. 14, 153– 160. 10.1016/0168-1605(91)90102-U 1777384 · DOI
- Mehlomakulu N. N. Setati M. E. Divol B. (2014). Characterization of novel killer toxins secreted by wine-related non-Saccharomyces yeasts and their action on Brettanomyces spp. Int. J. Food Microbiol. 188, 83– 91. 10.1016/j.ijfoodmicro.2014.07.015 25087208 · DOI
- Mendoza L. M. Manca de Nadra M. C. Farías M. E. (2007). Kinetics and metabolic behavior of a composite culture of Kloeckera apiculata and Saccharomyces cerevisiae wine related strains. Biotechnol. Lett. 29, 1057– 1063. 10.1007/s10529-007-9355-0 17440687 · DOI
- Mendoza L. Nadra M. M. Bru E. Farías M. (2009). Influence of wine-related physicochemical factors on the growth and metabolism of non-Saccharomyces and Saccharomyces yeasts in mixed culture. J. Ind. Microbiol. Biotechnol. 36, 229– 237. 10.1007/s10295-008-0489-4 18953586 · DOI
- Merritt A. E. Hurley R. (1972). Evaluation of sporulation media for yeasts obtained from pathological material. J. Med. Microbiol. 5, 21– 30. 10.1099/00222615-5-1-21 4553908 · DOI
- Mocke B. A. (2005). The Breeding of Yeast Strains for Novel Oenological Outcomes. Ph.D. thesis, Stellenbosch University.
- Morais P. B. Martins M. B. Klaczko L. B. Mendonça-Hagler L. C. Hagler A. N. (1995). Yeast succession in the Amazon fruit Parahancornia amapa as resource partitioning among Drosophila spp. Appl. Environ. Microbiol. 61, 4251– 4257. 8534092 PMC167736
- Morais P. B. Rosa C. A. Linardi V. R. Pataro C. Maia A. B. R. A. (1997). Short communication: characterization and succession of yeast populations associated with spontaneous fermentations during the production of Brazilian sugar-cane aguardente. World J. Microbiol. Biotechnol. 13, 241– 243. 10.1023/A:1018558302062 · DOI
- Moreira N. Mendes F. Guedes de Pinho P. Hogg T. Vasconcelos I. (2008). Heavy sulphur compounds, higher alcohols and esters production profile of Hanseniaspora uvarum and Hanseniaspora guilliermondii grown as pure and mixed cultures in grape must. Int. J. Food Microbiol. 124, 231– 238. 10.1016/j.ijfoodmicro.2008.03.025 18457893 · DOI
- Moreira N. Pina C. Mendes F. Couto J. A. Hogg T. Vasconcelos I. (2011). Volatile compounds contribution of Hanseniaspora guilliermondii and Hanseniaspora uvarum during red wine vinifications. Food Cont. 22, 662– 667. 10.1016/j.foodcont.2010.07.025 · DOI · Paper page
- Nguyen N. H. Suh S. O. Blackwell M. (2007). Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99, 842– 858. 10.3852/mycologia.99.6.842 18333508 · DOI
- Owuama C. I. Saunders J. R. (1990). Physiological variants of Saccharomyces cerevisiae and Kloeckera apiculata from palm wine and cashew juice. J. Appl. Bacteriol. 68, 491– 494. 10.1111/j.1365-2672.1990.tb02901.x 2196256 · DOI
- Pagnocca F. G. Mendonca-Hagler L. C. Hagler A. N. (1989). Yeasts associated with the white shrimp Penaeus schmitti, sediment, and water of Sepetiba Bay, Rio de Janeiro, Brasil. Yeast 5 Spec No, S479– S483. 2750315
- Pando Bedrinana R. Lastra Queipo A. Suarez Valles B. (2012). Screening of enymatic activities in non-Saccharomyces cider yeasts. J. Food Biochem. 36, 683– 689. 10.1111/j.1745-4514.2011.00583.x · DOI
- Paradis E. (2010). Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26, 419– 420. 10.1093/bioinformatics/btp696 20080509 · DOI
- Parker P. G. Snow A. A. Schug M. D. Booton G. C. Fuerst P. A. (1998). What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79, 361– 382. 10.2307/176939 · DOI
- Pu L. Jingfan F. Kai C. Chao-an L. Yunjiang C. (2014). Phenylethanol promotes adhesion and biofilm formation of the antagonistic yeast Kloeckera apiculata for the control of blue mold on citrus. FEMS Yeast Res. 14, 536– 546. 10.1111/1567-1364.12139 24479773 · DOI
- Radler F. Pfeiffer P. Dennert M. (1985). Killer toxins in new isolates of the yeasts Hanseniaspora uvarum and Pichia kluyveri. FEMS Microbiol. Lett. 29, 269– 272. 10.1111/j.1574-6968.1985.tb00874.x · DOI
- Radler F. Schmitt M. J. Meyer B. (1990). Killer toxin of Hanseniaspora uvarum. Arch. Microbiol. 154, 175– 178. 10.1007/BF00423329 2206104 · DOI
- Redzepovic S. Orlic S. Majdak A. Kozina B. Volschenk H. Viljoen-Bloom M. (2003). Differential malic acid degradation by selected strains of Saccharomyces during alcoholic fermentation. Int. J. Food Microbiol. 83, 49– 61. 10.1016/S0168-1605(02)00320-3 12672592 · DOI
- Reid V. J. Theron L. W. du Toit M. Divol B. (2012). Identification and partial characterization of extracellular aspartic protease genes from Metschnikowia pulcherrima IWBT Y1123 and Candida apicola IWBT Y1384. Appl. Environ. Microbiol. 78, 6838– 6849. 10.1128/AEM.00505-12 22820332 PMC3457490 · DOI
- Renard A. Gómez di Marco P. Egea-Cortines M. Weiss J. (2008). Application of whole genome amplification and quantitative PCR for detection and quantification of spoilage yeasts in orange juice. Int. J. Food Microbiol. 126, 195– 201. 10.1016/j.ijfoodmicro.2008.05.021 18597878 · DOI
- Romano P. Palla G. Caligiani A. Brandolini V. Maietti A. Salzano G. (2000). Evaluation of stereoisomers of 2,3-butanediol and acetoin to differentiate Saccharomyces cerevisiae and Kloeckera apiculata wine strains. Biotechnol. Lett. 22, 1947– 1951. 10.1023/A:1026741625019 · DOI
- Romano P. Suzzi G. Zironi R. Comi G. (1993). Biometric study of acetoin production in Hanseniaspora guilliermondii and Kloeckera apiculata. Appl. Environ. Microbiol. 59, 1838– 1841. 16348961 PMC182169
- Ross K. G. Shoemaker D. D. Krieger M. J. DeHeer C. J. Keller L. (1999). Assessing genetic structure with multiple classes of molecular markers: a case study involving the introduced fire ant Solenopsis invicta. Mol. Biol. Evol. 16, 525– 543. 10.1093/oxfordjournals.molbev.a026134 10331278 · DOI
- Schmitt M. J. Neuhausen F. (1994). Killer toxin-secreting double-stranded RNA mycoviruses in the yeasts Hanseniaspora uvarum and Zygosaccharomyces bailii. J. Virol. 68, 1765– 1772. 8107238 PMC236637
- Schuelke M. (2000). An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 18, 233– 234. 10.1038/72708 10657137 · DOI
- Schütz M. Gafner J. (1993). Analysis of yeast diversity during spontaneous and induced alcoholic fermentations. J. Appl. Bacteriol. 75, 551– 558. 10.1111/j.1365-2672.1993.tb01594.x · DOI
- Shimodaira H. (2002). An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492– 508. 10.1080/10635150290069913 12079646 · DOI · Paper page
- Sláviková E. Vadkertiová R. Vránová D. (2009). Yeasts colonizing the leaves of fruit trees. Ann. Microbiol. 59, 419– 424. 10.1007/BF03175125 · DOI
- Sosa O. de Nadra M. M. Farías M. (2008). Modification by glucose of the flocculent phenotype of a Kloeckera apiculata wine strain. J. Ind. Microbiol. Biotechnol. 35, 851– 857. 10.1007/s10295-008-0357-2 18425542 · DOI
- Spencer D. M. Spencer J. F. T. De Figueroa L. Heluane H. (1992). Yeasts associated with rotting citrus fruits in Tucumán, Argentina. Mycol. Res. 96, 891– 892. 10.1016/S0953-7562(09)81038-1 · DOI
- Strauss M. L. Jolly N. P. Lambrechts M. G. van Rensburg P. (2001). Screening for the production of extracellular hydrolytic enzymes by non-Saccharomyces wine yeasts. J. Appl. Microbiol. 91, 182– 190. 10.1046/j.1365-2672.2001.01379.x 11442729 · DOI
- Suzuki R. Shimodaira H. (2006). Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540– 1542. 10.1093/bioinformatics/btl117 16595560 · DOI
- Suzzi G. Schirone M. Sergi M. Marianella R. M. Fasoli G. Aguzzi I.. (2012). Multistarter from organic viticulture for red wine Montepulciano d'Abruzzo production. Front. Microbiol. 3: 135. 10.3389/fmicb.2012.00135 22529841 PMC3328976 · DOI
- Valles B. S. Bedriñana R. P. Tascón N. F. Simón A. Q. Madrera R. R. (2007). Yeast species associated with the spontaneous fermentation of cider. Food Microbiol. 24, 25– 31. 10.1016/j.fm.2006.04.001 16943091 · DOI
- van Wyk H. Divol B. (2010). Recovery of endo-polygalacturonase activity in wine yeast and its effect on wine aroma. FEMS Yeast Res. 10, 58– 71. 10.1111/j.1567-1364.2009.00588.x 19840119 · DOI
- Velázquez J. B. Longo E. Sieiro C. Cansado J. Calo P. Villa T. G. (1991). Improvement of the alcoholic fermentation of grape juice with mixed cultures of Saccharomyces cerevisiae wild strains. Negative effect of Kloeckera apiculata. World J. Microbiol. Biotechnol. 7, 485– 489. 10.1007/BF00303374 24425134 · DOI
- Versavaud A. Hallet J.-N. (1995). Pulsed-field gel electrophoresis combined with rare-cutting endonucleases for strain differentiation of Candida famata, Kloeckera apiculata and Schizosaccharomyces pombe with dhromosome number and size estimation of the two former. Syst. Appl. Microbiol. 18, 303– 309. 10.1016/S0723-2020(11)80401-7 · DOI
- Wang C. Esteve-Zarzoso B. Mas A. (2014). Monitoring of Saccharomyces cerevisiae, Hanseniaspora uvarum, and Starmerella bacillaris (synonym Candida zemplinina) populations during alcoholic fermentation by fluorescence in situ hybridization. Int. J. Food Microbiol. 191, 1– 9. 10.1016/j.ijfoodmicro.2014.08.014 25218463 · DOI
- Wang C. Mas A. Esteve-Zarzoso B. (2015). Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int. J. Food Microbiol. 206, 67– 74. 10.1016/j.ijfoodmicro.2015.04.022 25956738 · DOI
- Weiss S. Samson F. Navarro D. Casaregola S. (2013). YeastIP: a database for identification and phylogeny of Saccharomycotina yeasts. FEMS Yeast Res 13, 117– 125. 10.1111/1567-1364.12017 23110448 · DOI
- White T. J. Bruns T. D. Lee S. B. Taylor J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR Protocols: A Guide to Methods and Applications, eds Innis M. A. Gelfand D. H. Sninsky J. J. White T. J. (London: Academic Press), 315– 322.
- Wiles A. E. (1950). Studies of some yeasts causing spoilage of draught beers. J. Inst. Brew. 56, 183– 193. 10.1002/j.2050-0416.1950.tb01531.x · DOI
- Zagorc T. Maráz A. Cadez N. Jemec K. P. Péter G. Resnik M. (2001). Indigenous wine killer yeasts and their application as a starter culture in wine fermentation. Food Microbiol. 18, 441– 451. 10.1006/fmic.2001.0422 · DOI
- Zironi R. Romano P. Suzzi G. Battistutta F. Comi G. (1993). Volatile metabolites produced in wine by mixed and sequential cultures of Hanseniaspora guilliermondii or Kloeckera apiculata and Saccharomyces cerevisiae. Biotechnol. Lett. 15, 235– 238. 10.1007/BF0012831117440687 · DOI
- Zohre D. E. Erten H. (2002). The influence of Kloeckera apiculata and Candida pulcherrima yeasts on wine fermentation. Proc. Biochem. 38, 319– 324. 10.1016/S0032-9592(02)00086-9 · DOI
- Zott K. Claisse O. Lucas P. Coulon J. Lonvaud-Funel A. Masneuf-Pomarede I. (2010). Characterization of the yeast ecosystem in grape must and wine using real-time PCR. Food Microbiol. 27, 559– 567. 10.1016/j.fm.2010.01.006 20510771 · DOI
Cited by
Sorted by citations
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
Steenwyk, J. L., Opulente, D. A., Kominek, J., Shen, X.-X., Zhou, X., Labella, A. L., Bradley, N. P., Eichman, B. F., Čadež, N., Libkind, D., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000255 · Cited by 162 · see citing works
Hilber-Bodmer, M., Schmid, M., Ahrens, C. H., & Freimoser, F. M. (2017) · BMC Microbiology · doi:10.1186/s12866-016-0908-z · Cited by 106 · see citing works
Gonçalves, C., Steenwyk, J. L., Rinker, D. C., Opulente, D. A., LaBella, A. L., Harrison, M.-C., Wolters, J. F., Zhou, X., Shen, X.-X., Covo, S., et al. (2025) · Molecular Biology and Evolution · doi:10.1093/molbev/msaf285 · Cited by 4 · see citing works
- Authors
- Albertin, W., Setati, M. E., Miot-Sertier, C., Mostert, T. T., Colonna-Ceccaldi, B., Coulon, J., Girard, P., Moine, V., Pillet, M., Salin, F., Bely, M., Divol, B., & Masneuf-Pomarede, I.
- Affiliations
- Université de Bordeaux (FR)
- Stellenbosch University (ZA)
- Pernod Ricard (France) (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Corresponding author
- Albertin, Warren
- ORCID
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2016-01-20
- Volume
- 6
- Issue
- 10
- Pages
- 1569-1569
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC4718985
- OpenAlex
- W2224638443
- Cited by
- 124
- References
- 0
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 12 · 2023: 12 · 2022: 13 · 2021: 12 · 2020: 15 · 2019: 10 · 2018: 9 · 2017: 11 · 2016: 5
- FWCI
- 14.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion)
- SUNScholar (Stellenbosch University) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Horticultural and Viticultural Research
- Keywords
- Hanseniaspora uvarum, genetic diversity, microsatellite markers, AFLP, extracellular enzymes, pectinase, chitinase, proteolytic enzymes, β-glucosidase, grape must, Saccharomyces, strain differentiation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review