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Genome Announc. 2017 April; 5(14): e00064-17.
Published online 2017 April 6. doi:  10.1128/genomeA.00064-17
PMCID: PMC5383881

Genome Sequences of Cyberlindnera fabianii 65, Pichia kudriavzevii 129, and Saccharomyces cerevisiae 131 Isolated from Fermented Masau Fruits in Zimbabwe


Cyberlindnera fabianii 65, Pichia kudriavzevii 129, and Saccharomyces cerevisiae 131 have been isolated from the microbiota of fermented masau fruits. C. fabianii and P. kudriavzevii especially harbor promising features for biotechnology and food applications. Here, we present the draft annotated genome sequences of these isolates.


Cyberlindnera fabianii 65 [previously known as Lindnera fabianii, Hansenula fabianii, and Pichia fabianii (1, 2)], Pichia kudriavzevii 129 [previously known as Issatchenkia orientalis (2)], and Saccharomyces cerevisiae 131 have been isolated from the microbiota of fermented masau fruits (Ziziphus mauritiana) in Zimbabwe (3, 4).

All three species are found regularly in (fermented) food products (3, 5,14) but also occasionally in clinical sources (15,17). Nevertheless, P. kudriavzevii and S. cerevisiae were given the status of generally recognized as safe by the Food and Drug Administration (FDA) (18). C. fabianii 65 and P. kudriavzevii 129 especially harbor promising features for food fermentation applications, such as the production of extended aroma profiles (19). To further explore these features, the draft genomes of these wild isolates were investigated and annotated.

DNA was sequenced using Illumina MiSeq paired-end (2 × 251 bp) sequencing technology, with total depths of coverage of 83.3× (C. fabianii 65), 83.3× (P. kudriavzevii 129), and 100× (S. cerevisiae 131) based on a 12-Mb genome size. Moreover, PacBio sequencing was performed with total depths of coverage of 36.6× (C. fabianii 65), 32.1× (P. kudriavzevii 129), and 22.2× (S. cerevisiae 131). We performed hybrid assemblies using DBG2OLC with Illumina and PacBio data (20). PBJelly (21) was used for further scaffolding. The final assemblies were polished with Sparc (PacBio) (22) and Pilon (Illumina) (23). MAKER2 (24) was used to annotate the genomes using protein homology evidence from all available fungi in the Swiss-Prot database (25). De novo gene predictors Augustus (26) and SNAP (27) were trained using Pichia stipitis genome sequence data for C. fabianii 65 and P. kudriavzevii 129 and Saccharomyces cerevisiae for S. cerevisiae 131. Functional annotation was performed using BLASTp (28) against Swiss-Prot (25). Protein domains and gene ontology terms were assigned using InterProScan (29). BUSCO (30) analysis showed that more than 90% of the core fungal genes are present in all three assemblies (Table 1). The G+C percentage of C. fabianii 65 is 44.4% but is lower for P. kudriavzevii 129 (38.5%) and S. cerevisiae 131 (38.1%). Other assembly and annotation statistics are listed in Table 1.

Assembly characteristics of three fungal genome sequences

The genome sequences and gene annotations can now be used to develop novel molecular tools to unravel the full metabolic repertoire of the two nonconventional yeasts compared to S. cerevisiae 131. Additionally, links between phenotypes and genotypes, as well as comparative genomic studies among the three species, will reveal opportunities for industrial applications of C. fabianii 65 and P. kudriavzevii 129.

Accession number(s).

The annotated genome sequences are deposited at DDBJ/EMBL/Genbank under the accession numbers listed in Table 1.


This research was financially supported by the Graduate School VLAG (Wageningen University & Research, Wageningen, The Netherlands) and Heineken Supply Chain BV (Zoeterwoude, The Netherlands).


Citation van Rijswijck IMH, Derks MFL, Abee T, de Ridder D, Smid EJ. 2017. Genome sequences of Cyberlindnera fabianii 65, Pichia kudriavzevii 129, and Saccharomyces cerevisiae 131 isolated from fermented masau fruits in Zimbabwe. Genome Announc 5:e00064-17.


1. Minter DW. 2009. Cyberlindnera, a replacement name for Lindnera Kurtzman et al., nom. illegit. Mycotaxon 110:473–476.
2. Kurtzman CP, Robnett CJ, Basehoar-Powers E 2008. Phylogenetic relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene sequence analysis, and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8:939–954. doi:.10.1111/j.1567-1364.2008.00419.x [PubMed] [Cross Ref]
3. Nyanga LK, Nout MJ, Gadaga TH, Theelen B, Boekhout T, Zwietering MH 2007. Yeasts and lactic acid bacteria microbiota from masau (Ziziphus mauritiana) fruits and their fermented fruit pulp in Zimbabwe. Int J Food Microbiol 120:159–166. doi:.10.1016/j.ijfoodmicro.2007.06.021 [PubMed] [Cross Ref]
4. Nyanga LK, Nout MJ, Smid EJ, Boekhout T, Zwietering MH 2013. Fermentation characteristics of yeasts isolated from traditionally fermented masau (Ziziphus mauritiana) fruits. Int J Food Microbiol 166:426–432. doi:.10.1016/j.ijfoodmicro.2013.08.003 [PubMed] [Cross Ref]
5. Jeyaram K, Singh WM, Capece A, Romano P 2008. Molecular identification of yeast species associated with “Hamei”—a traditional starter used for rice wine production in Manipur, India. Int J Food Microbiol 124:115–125. doi:.10.1016/j.ijfoodmicro.2008.02.029 [PubMed] [Cross Ref]
6. Meersman E, Steensels J, Struyf N, Paulus T, Saels V, Mathawan M, Allegaert L, Vrancken G, Verstrepen KJ 2015. Tuning chocolate flavor through development of thermotolerant Saccharomyces cerevisiae starter cultures with increased acetate ester production. Appl Environ Microbiol 82:732–746. doi:.10.1128/AEM.02556-15 [PMC free article] [PubMed] [Cross Ref]
7. Mukisa IM, Porcellato D, Byaruhanga YB, Muyanja CM, Rudi K, Langsrud T, Narvhus JA 2012. The dominant microbial community associated with fermentation of Obushera (sorghum and millet beverages) determined by culture-dependent and culture-independent methods. Int J Food Microbiol 160:1–10. doi:.10.1016/j.ijfoodmicro.2012.09.023 [PubMed] [Cross Ref]
8. Pedersen LL, Owusu-Kwarteng J, Thorsen L, Jespersen L 2012. Biodiversity and probiotic potential of yeasts isolated from fura, a West African spontaneously fermented cereal. Int J Food Microbiol 159:144–151. doi:.10.1016/j.ijfoodmicro.2012.08.016 [PubMed] [Cross Ref]
9. Thanh VN, Thuy NT, Chi NT, Hien DD, Ha BT, Luong DT, Ngoc PD, Ty PV 2016. New insight into microbial diversity and functions in traditional Vietnamese alcoholic fermentation. Int J Food Microbiol 232:15–21. doi:.10.1016/j.ijfoodmicro.2016.05.024 [PubMed] [Cross Ref]
10. Del Mónaco SM, Barda NB, Rubio NC, Caballero AC 2014. Selection and characterization of a Patagonian Pichia kudriavzevii for wine deacidification. J Appl Microbiol 117:451–464. doi:.10.1111/jam.12547 [PubMed] [Cross Ref]
11. Golomb BL, Morales V, Jung A, Yau B, Boundy-Mills KL, Marco ML 2013. Effects of pectinolytic yeast on the microbial composition and spoilage of olive fermentations. Food Microbiol 33:97–106. doi:.10.1016/ [PubMed] [Cross Ref]
12. Greppi A, Saubade F, Botta C, Humblot C, Guyot JP, Cocolin L 2017. Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiol 62:169–177. doi:.10.1016/ [PubMed] [Cross Ref]
13. Hellström AM, Almgren A, Carlsson NG, Svanberg U, Andlid TA 2012. Degradation of phytate by Pichia kudriavzevii TY13 and Hanseniaspora guilliermondii TY14 in Tanzanian togwa. Int J Food Microbiol 153:73–77. doi:.10.1016/j.ijfoodmicro.2011.10.018 [PubMed] [Cross Ref]
14. Yuangsaard N, Yongmanitchai W, Yamada M, Limtong S 2013. Selection and characterization of a newly isolated thermotolerant Pichia kudriavzevii strain for ethanol production at high temperature from cassava starch hydrolysate. Antonie Van Leeuwenhoek 103:577–588. doi:.10.1007/s10482-012-9842-8 [PubMed] [Cross Ref]
15. Muller LA, Lucas JE, Georgianna DR, McCusker JH 2011. Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Mol Ecol 20:4085–4097. doi:.10.1111/j.1365-294X.2011.05225.x [PMC free article] [PubMed] [Cross Ref]
16. Jindal N, Dhuria N, Arora S, Arora D 2015. Cyberlindnera (Pichia) fabianii infection in a neutropenic child: importance of molecular identification. JMM Case Reports 2. doi:.10.1099/jmmcr.0.000033 [Cross Ref]
17. Katagiri S, Gotoh M, Tone K, Akahane D, Ito Y, Ohyashiki K, Makimura K 2016. Fatal Cyberlindnera fabianii fungemia in a patient with mixed phenotype acute leukemia after umbilical cord blood transplantation. Int J Hematol 103:592–595. doi:.10.1007/s12185-016-1953-y [PubMed] [Cross Ref]
18. Bourdichon F, Casaregola S, Farrokh C, Frisvad JC, Gerds ML, Hammes WP, Harnett J, Huys G, Laulund S, Ouwehand A, Powell IB, Prajapati JB, Seto Y, Ter Schure E, Van Boven A, Vankerckhoven V, Zgoda A, Tuijtelaars S, Hansen EB 2012. Food fermentations: microorganisms with technological beneficial use. Int J Food Microbiol 154:87–97. doi:.10.1016/j.ijfoodmicro.2011.12.030 [PubMed] [Cross Ref]
19. van Rijswijck IM, Dijksterhuis J, Wolkers-Rooijackers JC, Abee T, Smid EJ 2015. Nutrient limitation leads to penetrative growth into agar and affects aroma formation in Pichia fabianii, P. kudriavzevii and Saccharomyces cerevisiae. Yeast 32:89–101. doi:.10.1002/yea.3050 [PubMed] [Cross Ref]
20. Ye C, Hill CM, Wu S, Ruan J, Ma ZS 2016. DBG2OLC: efficient assembly of large genomes using long erroneous reads of the third generation sequencing technologies. Sci Rep 6:31900. doi:.10.1038/srep31900 [PMC free article] [PubMed] [Cross Ref]
21. English AC, Richards S, Han Y, Wang M, Vee V, Qu JX, Qin X, Muzny DM, Reid JG, Worley KC, Gibbs RA 2012. Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS One 7:e47768. doi:.10.1371/journal.pone.0047768 [PMC free article] [PubMed] [Cross Ref]
22. Ye CX, Ma ZS 2016. Sparc: a sparsity-based consensus algorithm for long erroneous sequencing reads. PeerJ 4:e2016. doi:.10.7717/peerj.2016 [PMC free article] [PubMed] [Cross Ref]
23. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng QD, Wortman J, Young SK, Earl AM 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9:e112963. doi:.10.1371/journal.pone.0112963 [PMC free article] [PubMed] [Cross Ref]
24. Holt C, Yandell M 2011. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12:491. doi:.10.1186/1471-2105-12-491 [PMC free article] [PubMed] [Cross Ref]
25. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang HZ, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LSL 2004. UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:D115–D119. doi:.10.1093/nar/gkh131 [PMC free article] [PubMed] [Cross Ref]
26. Stanke M, Steinkamp R, Waack S, Morgenstern B 2004. AUGUSTUS: a Web server for gene finding in eukaryotes. Nucleic Acids Res 32:W309–W312. doi:.10.1093/nar/gkh379 [PMC free article] [PubMed] [Cross Ref]
27. Korf I. 2004. Gene finding in novel genomes. BMC Bioinformatics 5:59. doi:.10.1186/1471-2105-5-59 [PMC free article] [PubMed] [Cross Ref]
28. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. [PMC free article] [PubMed]
29. Jones P, Binns D, Chang HY, Fraser M, Li WZ, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S 2014. InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. doi:.10.1093/bioinformatics/btu031 [PMC free article] [PubMed] [Cross Ref]
30. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. doi:.10.1093/bioinformatics/btv351 [PubMed] [Cross Ref]

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