Abstract
A novel yeast species of Starmerella vitis f.a. sp. nov. is proposed to accommodate five strains isolated from flowers, grapes and an insect in the Azores, Canada, Hungary, Palau and Taiwan. As the strains were genetically distinct, we used parsimony network analysis based on ITS-D1/D2 sequences to delineate the species in a statistically objective manner. According to sequence comparisons and phylogenetic analysis, the novel species is most closely related to Starmerella lactis-condensi. The two species cannot be distinguished by conventional physiological tests. The type strain of Starmerella vitis f.a., sp. nov. is CBS 16418T; Mycobank number MB 835251.
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References
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Barata A, Malfeito-Ferreira M, Loureiro V (2012) The microbial ecology of wine grape berries. Int J Food Microbiol 153:243–259. https://doi.org/10.1016/j.ijfoodmicro.2011.11.025
Bokulich NA, Thorngate JH, Richardson PM, Mills DA (2014) Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci USA 111:E139–E148. https://doi.org/10.1073/pnas.1317377110
Čadež N, Raspor P, Smith MT (2006) Phylogenetic placement of Hanseniaspora-Kloeckera species using multigene sequence analysis with taxonomic implications: descriptions of Hanseniaspora pseudoguilliermondii sp. nov. and Hanseniaspora occidentalis var. citrica var. nov. Int J Syst Evol Microbiol 56:1157–65. https://doi.org/10.1099/ijs.0.64052-0
Čadež N, Zupan J, Raspor P (2010) The effect of fungicides on yeast communities associated with grape berries. FEMS Yeast Res 10:619–630. https://doi.org/10.1111/j.1567-1364.2010.00635.x
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–9. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Daniel H (2003) Evaluation of ribosomal RNA and actin gene sequences for the identification of ascomycetous yeasts. Int J Food Microbiol 86(1–2):61–78
Daniel HM, Rosa CA, Sao Thiago-Calaca PS, Antonini Y, Bastos EM, Evrard P et al (2013) Starmerella neotropicalis f.a., sp. nov., a yeast species found in bees and pollen. Int J Syst Evol Microbiol 63:3896–903. https://doi.org/10.1099/ijs.0.055897-0
de Vega C, Albaladejo RG, Guzmán B, Steenhuisen SL, Johnson SD, Herrera CM et al (2017) Flowers as a reservoir of yeast diversity: description of Wickerhamiella nectarea f.a. sp. nov., and Wickerhamiella natalensis f.a. sp. nov. from South African flowers and pollinators, and transfer of related Candida species to the genus Wickerhamiella as new combinations. FEMS Yeast Res. https://doi.org/10.1093/femsyr/fox054
de Vega C, Albaladejo RG, Lachance MA (2018) Metschnikowia maroccana f.a., sp nov., a new yeast species associated with floral nectar from Morocco. Int J Syst Evol Microbiol 68:2028–35. https://doi.org/10.1099/ijsem.0.002784
Drumonde-Neves J, Franco-Duarte R, Lima T, Schuller D, Pais C (2016) Yeast biodiversity in vineyard environments is increased by human intervention. PLoS ONE 11:e0160579. https://doi.org/10.1371/journal.pone.0160579
Gao W-L, Liu T, Zheng J, Hui FL (2017) Kodamaea neixiangensis f.a., sp. nov. and Kodamaea jinghongensis f.a., sp. nov., two yeast species isolated from rotting wood. Int J Syst Evolut Microbiol 67(9):3358–3362
Gonçalves C, Gonçalves P (2019) Multilayered horizontal operon transfers from bacteria reconstruct a thiamine salvage pathway in yeasts. Proc Natl Acad Sci USA 116(44):22219–22228. https://doi.org/10.1073/pnas.1909844116
Gonçalves C, Coelho MA, Salema-Oom M, Gonçalves P (2016) Stepwise functional evolution in a fungal sugar transporter family. Mol Biol Evol 33:352–366. https://doi.org/10.1093/molbev/msv220
Gonçalves C, Wisecaver JH, Kominek J, Oom MS, Leandro MJ, Shen XX et al (2018) Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage. eLife. https://doi.org/10.7554/eLife.33034
Gonçalves P, Gonçalves C, Brito PH, Sampaio JP (2020) The Wickerhamiella/Starmerella clade - a treasure trove for the study of the evolution of yeast metabolism. Yeast 37:313–320. https://doi.org/10.1002/yea.3463
Gonzalez SS, Alcoba-Florez J, Laich F (2013) Lachancea lanzarotensis sp nov., an ascomycetous yeast isolated from grapes and wine fermentation in Lanzarote, Canary Islands. Int J Syst Evol Microbiol 63:358–363. https://doi.org/10.1099/ijs.0.046029-0
Kachalkin AV, Abdullabekova DA, Magomedova ES, Magomedov GG, Chernov IY (2015) Yeasts of the vineyards in Dagestan and other regions. Microbiology 84:425–432
Kominek J, Doering DT, Opulente DA, Shen XX, Zhou X, DeVirgilio J et al (2019) Eukaryotic acquisition of a bacterial operon. Cell 176:1356-1366.e10. https://doi.org/10.1016/j.cell.2019.01.034
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73:331–371. https://doi.org/10.1023/a:1001761008817
Kurtzman CP, Robnett CJ (2003) Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Res 3:417–432. https://doi.org/10.1016/S1567-1356(03)00012-6
Kurtzman CP, Fell JW, Boekhout T (2011) Methods for isolation, phenotypic characterization and maintenance of yeasts. In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study. Elsevier , Amsterdam, pp 87–110
Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF et al (2001) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8. https://doi.org/10.1111/j.1567-1364.2001.tb00007.x
Lachance MA, Dobson J, Wijayanayaka DN, Smith AM (2010) The use of parsimony network analysis for the formal delineation of phylogenetic species of yeasts: Candida apicola, Candida azyma, and Candida parazyma sp. nov., cosmopolitan yeasts associated with floricolous insects. Antonie van Leeuwenhoek 97:155–70. https://doi.org/10.1007/s10482-009-9399-3
Lachance MA, Boekhout T, Scorzetti G, Fell JW, Kurtzman CP (2011a) Candida Berkhout (1923). In: Kurtzman CP, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study. Elsevier Science, Amsterdam, pp 987–1278
Lachance MA, Wijayanayaka TM, Bundus JD, Wijayanayaka DN (2011b) Ribosomal DNA sequence polymorphism and the delineation of two ascosporic yeast species: Metschnikowia agaves and Starmerella bombicola. FEMS Yeast Res 11:324–333. https://doi.org/10.1111/j.1567-1364.2011.00718.x
Rosa CA, Lachance MA, Silva JO, Teixeira AC, Marini MM et al (2003) Yeast communities associated with stingless bees. FEMS Yeast Res 4:271–275. https://doi.org/10.1016/S1567-1356(03)00173-9
Roscini L, Tristezza M, Corte L, Colabella C, Perrotta C, Rampino P et al (2018) Early ongoing speciation of Ogataea uvarum sp. nov. within the grape ecosystem revealed by the internal variability among the rDNA operon repeats. Front Microbiol 9:1687. https://doi.org/10.3389/fmicb.2018.01687
Santos ARO, Leon MP, Barros KO, Freitas LFD, Hughes AFS, Morais PB, Lachance M-A, Rosa CA (2018) Starmerella camargoi f.a., sp. nov., Starmerella ilheusensis f.a., sp. nov., Starmerella litoralis f.a., sp. nov., Starmerella opuntiae f.a., sp. nov., Starmerella roubikii f.a., sp. nov. and Starmerella vitae f.a., sp. nov., isolated from flowers and bees, and transfer of related Candida species to the genus Starmerella as new combinations. Int J Syst Evolut Microbiol 68(4):1333–1343
Santos ARO, Lee DK, Ferreira AG, do Carmo MC, Rondelli VM, Barros KO, Hsiang T, Rosa CA, Lachance MA (2020) The yeast community of Conotelus sp. (Coleoptera: Nitidulidae) in Brazilian passionfruit flowers (Passiflora edulis) and description of Metschnikowia amazonensis sp. nov., a large-spored clade yeast. Yeast 37:253–260. https://doi.org/10.1002/yea.3453
Setati ME, Jacobson D, Bauer FF (2015) Sequence-based analysis of the Vitis vinifera L. cv Cabernet Sauvignon Grape must mycobiome in three South African vineyards employing distinct agronomic systems. Front Microbiol 30:1358. https://doi.org/10.3389/fmicb.2015.01358
Shen X-X, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV et al (2018) Tempo and mode of genome evolution in the budding yeast subphylum. Cell 175:P1533. https://doi.org/10.1016/j.cell.2018.10.023
Sipiczki M (2003) Candida zemplinina sp. nov., an osmotolerant and psychrotolerant yeast that ferments sweet botrytized wines. Int J Syst Evol Microbiol 53:2079–2083. https://doi.org/10.1099/ijs.0.02649-0
Taylor MW, Tsai P, Anfang N, Ross HA, Goddard MR (2014) Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environ Microbiol 16:2848–2858. https://doi.org/10.1111/1462-2920.12456
Teixeira ACP, Marini MM, Nicoli JR, Antonini Y, Martins RP, Lachance MA et al (2003) Starmerella meliponinorum sp. nov., a novel ascomycetous yeast species associated with stingless bees. Int J Syst Evol Microbiol 53:339–343. https://doi.org/10.1099/ijs.0.02262-0
Torriani S, Lorenzini M, Salvetti E, Fells GE (2011) Zygosaccharomyces gambellarensis sp. nov., an ascosporogenous yeast isolated from an Italian ‘passito’ style wine. Int J Syst Evol Microbiol 61:3084–3088. https://doi.org/10.1099/ijs.0.031146-0
Vu D, Groenewald M, Szöke S, Cardinali G, Eberhardt U et al (2016) DNA barcoding analysis of more than 9000 yeast isolates contributes to quantitative thresholds for yeast species and genera delimitation. Stud Mycol 85:91–105. https://doi.org/10.1016/j.simyco.2016.11.007
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, London, pp 315–322
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This work was partly funded by the Slovenian Research Agency (P4-0116 and MRIC-UL ZIM, IP-0510) (N.Č.), the State Secretariat for Education of the Hungarian Ministry of Human Capacities and by the European Union and co-financed by the European Social Fund (Grant Agreement No. EFOP-3.6.3-VEKOP-16-2017-00005) (D.D. and G.P.).
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NČ wrote the manuscript, analysed the data and prepared the figures, GP and M-AL contributed to text preparation and revised the manuscript, JD-N, RF-D, MS, M-AL, GP and DD isolated, identified and deposited the strains, DS conceptualized the study, TL and CP supervised JD-N. and RF-D. All authors read and approved the final version of the manuscript.
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Dorit Schuller: Department of Biology, Centre of Molecular and Environmental Biology (CBMA), University of Minho, Braga, Portugal until 2013.
The GenBank/EMBL/DDBJ accession numbers of the LSU and ITS sequences of Starmerella vitis sp. nov. CBS 16418T are KC992848 and MN317383, respectively. The MycoBank accession numbers is MB 835251.
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Čadež, N., Drumonde-Neves, J., Sipiczki, M. et al. Starmerella vitis f.a., sp. nov., a yeast species isolated from flowers and grapes. Antonie van Leeuwenhoek 113, 1289–1298 (2020). https://doi.org/10.1007/s10482-020-01438-x
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DOI: https://doi.org/10.1007/s10482-020-01438-x