Skip to main content
SpringerLink
Log in

Exploration of yeast communities in fresh coconut, palmyra, and nipa palm saps and ethanol-fermenting ability of isolated yeasts

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

This study aimed to explore communities and the ethanol-fermenting ability of yeasts in fresh coconut, palmyra, and nipa palm saps. From the 90 samples of coconut, palmyra, and nipa palm saps, 204 yeast isolates were isolated and identified as 15 species in the phylum Ascomycota and a species (one strain) in Basidiomycota. Saccharomyces cerevisiae, Hanseniaspora guilliermondii, and Lachancea thermotolerans were found in the saps of all three palm species. Candida tropicalis and Pichia kudriavzevii were obtained from the coconut and palmyra palm saps, Hanseniaspora vineae, Lachancea fermentati, and Pichia manshurica were present in the coconut and nipa palm saps, whereas Torulaspora delbrueckii was found in the palmyra and nipa palm saps. The species with the highest occurrence in the saps of coconut, palmyra, and nipa palms was S. cerevisiae with 76.67%, 86.70%, and 100% frequency of occurrence, respectively. Using principal coordinates analysis for ordination, no marked difference was observed in the yeast communities from the saps of the three palm species. A total of 199 isolates were found to possess ethanol-fermentation ability when cultivated using shake flask in 160 g/L of glucose medium at 28°C for 48 h. Lachancea fermentati YSP-383, isolated from nipa palm sap, produced the highest amount of ethanol (76.74 g/L). Twenty-six isolates of Candida sanyaensis (1), C. tropicalis (1), H. guilliermondii (7), L. fermentati (8), L. thermotolerans (1), Pichia kudriavzevii (2), and S. cerevisiae (6) produced high amounts of ethanol ranging from 69.57 to 76.74 g/L. The result demonstrated that yeasts in the palm saps could play roles in the natural fermentation of palm saps.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alloue-Boraud WA, N’Guessan KF, Hiligsmann S, Djè KM, Delvigne F (2015) Fermentation profile of Saccharomyces cerevisiae and Candida tropicalis as starter cultures on barley malt medium. J Food Sci Technol 52:5236–5242

    CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boonmak C, Khunnamwong P, Limtong S (2020) Yeast communities of primary and secondary peat swamp forests in southern Thailand. Antonie Van Leeuwenhoek 113:55–69

    PubMed  Google Scholar 

  • Bernal R, Galeano G, García N, Olivares IL, Cocomá C (2010) Uses and commercial prospects for the wine palm, Attalea butyracea, in Colombia. Ethnobot Res Applic 8:255–268

    Google Scholar 

  • Barh D, Mazumdar BC (2008) Comparative nutritive values of palm saps before and after their partial fermentation and effective use of wild date (Phoenix sylvestris Roxb.) sap in treatment of anemia. Res J Medicine & Med Sci 3:173–176

    CAS  Google Scholar 

  • Bellut K, Michel M, Hutzler M, Zarnkow M, Jacob F, De Schutter DP, Daenen L, Lynch KM, Zannini E, Arendt EK (2019) Investigation into the potential of Lachancea fermentati strain KBI 12.1 for low alcohol beer brewing. J Am Soc Brew Chem 77:157–169

    CAS  Google Scholar 

  • Chamnipa N, Thanonkeo S, Klanrit P, Thanonkeo P (2018) The potential of the newly isolated thermotolerant yeast Pichia kudriavzevii RZ8-1 for high-temperature ethanol production. Braz J Microbiol 49:378–391

    PubMed  Google Scholar 

  • Chandrasekhar K, Sreevani S, Seshapani P, Pramodhakumari J (2012) A review on palm wine. Int J Res Biol Sci 2:33–38

    Google Scholar 

  • Chanthachum S, Beuchat LR (1997) Inhibitory effect of kiam (Cotylelobium lanceotatumcraih.) wood extract on gram-positive food-borne pathogens and spoilage micro-organisms. Food Microbiol 14:603–608

    Google Scholar 

  • Chinnamma M, Bhasker S, Hari BM, Sreekumar D, Madhav H (2019) Coconut neera-a vital health beverage from coconut palms: harvesting, processing and quality analysis. Beverages 5:22. https://doi.org/10.3390/beverages5010022

    Article  CAS  Google Scholar 

  • Chongkhong S, Puangpee S (2018) Alternative energy under the royal initiative of his majesty the king: ethanol from nipa sap with yeast isolated. Songklanakarin J Sci Technol 40:648–658

    CAS  Google Scholar 

  • Colombo AL, Ju ´nior JNA, Guinea J, (2017) Emerging multidrug-resistant Candida species. Curr Opin Infect Dis 30:528–538

    PubMed  Google Scholar 

  • Domizio P, House JF, Joseph CML, Bisson LF, Bamforth CW (2016) Lachancea thermotolerans as an alternative yeast for the production of beer. J Inst Brew 122:599–604

    CAS  Google Scholar 

  • Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int J Syst Evol Microbiol 50:1351–1371

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Guinea J (2014) Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect 20:5–10

    PubMed  Google Scholar 

  • Gumienna M, Szwengiel A, Szczepańska-Alvarez A, Szambelan K, Lasik-Kurdyś M, Czarnecki Z, Sitarski A (2016) The impact of sugar beet varieties and cultivation conditions on ethanol productivity. Biomass Bioenerg 85:228–234

    CAS  Google Scholar 

  • Gupta RC, Jain VK, Shanker G (1980) Palm sap as a potential starting material for vinegar production. Res Ind 25:5–7

    CAS  Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hossain MF, Islam MA (2015) Utilization of mangrove forest plant: nipa palm (Nypa fruticans Wurmb.). Am J Agr For 3:156–160

    Google Scholar 

  • Into P, Khunnamwong P, Jindamoragot S, Am-in S, Intanoo W, Limtong S (2020) Yeast associated with rice phylloplane and their contribution to control of rice sheath blight disease. Microorganisms 8:362. https://doi.org/10.3390/microorganisms8030362

    Article  CAS  PubMed Central  Google Scholar 

  • Jamai L, Sendide K, Ettayebi K, Errachidi F, Hamdouni-Alami O, Tahri-Jouti MA, McDermott T, Ettayebi M (2001) Physiological difference during ethanol fermentation between calcium alginate-immobilized Candida tropicalis and Saccharomyces cerevisiae. FEMS Microbiol Lett 204:375–379

    CAS  PubMed  Google Scholar 

  • Jespersen L (2003) Occurrence and taxonomic characteristics of strains of Saccharomyces cerevisiae predominant in African indigenous fermented foods and beverages. FEMS Yeast Res 3:191–200

    CAS  PubMed  Google Scholar 

  • Kaewwichian R, Khunnamwong P, Am-In S, Jindamorakot S, Limtong S (2020) Torulaspora nypae sp. nov., a novel yeast species isolated from nipa (Nypa fruticans Wurmb.) inflorescence sap in southern Thailand. Int J Syst Evol Microbiol 70:1112–1116

    CAS  PubMed  Google Scholar 

  • Kalaiyarasi K, Sangeetha K, Rajarajan S (2013) A comparative study on the microbial flora of the fresh sap from cut inflorescence and fermented sap (toddy) of Borrassus flabellifer Linn. (palmyra tree) and of Cocos nucifera Linn. (coconut tree) to identify the microbial fermenters. Int J Res Pure Appl Microbiol 3:43–47

    Google Scholar 

  • Kapilan R, Kailayalingam R, Mahilrajan S, Srivijeindran S (2015) Determination of efficient fermentation inhibitor of sweet sap of Cocos nucifera and optimization of concentration for quality outputs in Northern Sri Lanka. IJSRAS 2:166–174

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lachance MA, Bowles JM, Starmer WT, Baker SF (1999) Kodamaea kadaduensis and Candida tolerans, two new ascomycetous yeast species from Australian Hibiscus flowers. Can J Microbiol 45:172–177

    CAS  PubMed  Google Scholar 

  • Lasekan O, Buettner A, Christlbaure M (2007) Investigation of important odorant of palm wine (Elaeis guineensis). Food Chem 105:15–23

    CAS  Google Scholar 

  • Lleixà J, Martín V, Giorello F, Portillo MC, Carrau F, Beltran G, Mas A (2019) Analysis of the NCR mechanisms in Hanseniaspora vineae and Saccharomyces cerevisiae during winemaking. Front Gene 9:747. https://doi.org/10.3389/fgene.2018.00747

    Article  CAS  Google Scholar 

  • Lombardi SJ, Pannella G, Iorizzo M, Moreno-Arribas MV, Tremonte P, Succi M, Sorrentino E, Macciola V, Di Renzo M, Coppola R (2018) Sequential inoculum of Hanseniaspora guilliermondii and Saccharomyces cerevisiae for winemaking Campanino on an industrial scale. World J Microbiol Biotechno 34:161. https://doi.org/10.1007/s11274-018-2540-6

    Article  CAS  Google Scholar 

  • Limtong S, Kaewwichian R, Yongmanitchai W, Kawasaki H (2014) Diversity of culturable yeasts in phylloplane of sugarcane in Thailand and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 30:1785–1796

    CAS  PubMed  Google Scholar 

  • Limtong S, Koowadjanakul N (2012) Yeasts from phylloplanes and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 28:3323–3335

    CAS  PubMed  Google Scholar 

  • Manel Z, Nedia K, Moktar H, Ali F (2011) Microbiological analysis and screening of lactic acid bacteria from Tunisian date palm sap. Int Food Res J 5:2929–2935

    Google Scholar 

  • Martin V, Valera MJ, Medina K, Boido E, Carrau F (2018) Oenological Impact of the Hanseniaspora/Kloeckera Yeast Genus on Wines a review. Fermentation 4:76. https://doi.org/10.3390/fermentation4030076

    Article  CAS  Google Scholar 

  • Mehrotra RC, Tiwari RP, Mazumder BI (2003) Nypa megafossils from the Tertiary sediments of Northeast India. Geobios 36:83–92

    Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    CAS  Google Scholar 

  • Minh NP (2014) Various factors influencing to the nipa (Nypa Fruticans) wine fermentation. IJMRD 1:111–114

    Google Scholar 

  • Misra S (2016) Neera: the coconut sap: a review. Int J Food Sci Nutr 1:35–38

    Google Scholar 

  • N’Guessan FK, Dénis YN, Camara F, Djè MK (2010) Saccharomyces cerevisiae and Candida tropicalis as starter cultures for the alcoholic fermentation of tchapalo, a traditional sorghum beer. World J Microbiol Biotechnol 26:693–699

    Google Scholar 

  • Naknean P, Meenune M, Roudaut G (2010) Characterization of palm sap harvested in Songkhla province. Southern Thailand Int Food Res J 17:977–986

    CAS  Google Scholar 

  • Nardi T, Panero L, Petrozziello M, Guaita M, Tsolakis C, Cassino C, Vagnoli P, Bosso A (2019) Managing wine quality using Torulaspora delbrueckii and Oenococcus oeni starters in mixed fermentations of a red Barbera wine. Eur Food Res Technol 245:293–307

    CAS  Google Scholar 

  • Nguyen VD, Harifara R, Shiro S (2016) Sap from various palms as a renewable energy source for bioethanol production. Chem Ind Chem Eng Q 22:355–373

    CAS  Google Scholar 

  • Perpetuini G, Tittarelli F, Battistelli N, Suzzi G, Tofalo R (2020) Contribution of Pichia manshurica strains to aroma profile of organic wines. Eur Food Res Technol 246:1405–1417

    CAS  Google Scholar 

  • Phaichamnan M, Posri W, Meenune M (2010) Quality profile of palm sugar concentrate produced in Songkhla province, Thailand. Int Food Res J 17:425–432

    CAS  Google Scholar 

  • Pongsanat P, Miyuki KK (2018) Identification and characterization of Candida tropicalis isolated from soil of sugarcane plantation in Thailand for ethanol production. Asia Pac J Sci Technol 23:1–9

    Google Scholar 

  • Porter TJ, Divol B, Setati ME (2019) Lachancea yeast species: Origin, biochemical characteristics and oenological significance. Food Res Int 119:378–389

    CAS  PubMed  Google Scholar 

  • Ramírez M, Velázquez R (2018) The yeast Torulaspora delbrueckii: an interesting but difficult-to-use tool for winemaking. Fermentation 4:94. https://doi.org/10.3390/fermentation4040094

    Article  CAS  Google Scholar 

  • Saez JS, Lopes CA, Kirs VE, Sangorrín M (2011) Production of volatile phenols by Pichia manshurica and Pichia membranifaciens isolated from spoiled wines and cellar environment in Patagonia. Food Microbiol 28:503–509

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Somawiharja Y, Purnomo H, Wonohadidjojo DM, Kartikawati M, Suniati FRT (2018) Indigenous technology of tapping, collecting and processing of coconut (Cocos Nucifera) sap and its quality in Blitar Regency, East Java, Indonesia. Food Res 2:398–403

    Google Scholar 

  • Srisuk N, Nutaratat P, Surussawadee J, Limtong S (2019) Yeast communities in sugarcane phylloplane. Microbiology (Moscow) 88:353–369

    CAS  Google Scholar 

  • Stringini M, Comitini F, Taccari M, Ciani M (2009) Yeast diversity during tapping and fermentation of palm wine from Cameroon. Food Microbiol 26:415–420

    CAS  PubMed  Google Scholar 

  • Sudha R, Niral V, Hebbar KB, Samsudeen K (2019) Coconut inflorescence sap. Curr Sci 116:1809–1817

    CAS  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    CAS  PubMed  Google Scholar 

  • Thorasin T (2018) A comparative study of the physicochemical, nutritional characteristics and microbiological contamination of fresh nipa palm (Nypa fruticans) Sap. Burapha Sci J 23:1301–1316

    Google Scholar 

  • Toyotome T, Yamamoto M, Horie M (2019) Draft genome sequence of the yeast Pichia manshurica YM63, a participant in secondary fermentation of Ishizuchi-Kurocha, a Japanese fermented tea. Microbiol Resour Announc 8:27.e00528–19. https://doi.org/10.1128/MRA.00528-19

    Article  Google Scholar 

  • Tsuji K, Ghazalli MN, Ariffin ZU, Nordin MS, Khaidizar MI, Dulloo ME, Sebastian LS (2011) Biological and ethnobotanical characteristics of nipa palm (Nypa fructicans Wurmb.): A Review. Sains Malaysiana 40:1407–1412

    Google Scholar 

  • Udomsaksakul N, Kodama K, Tanasupawat S, Savarajara A (2018a) Indigenous Saccharomyces cerevisiae strains from coconut inflorescence sap: characterization and use in coconut wine fermentation. CMU J Nat Sci 17:219–230

    Google Scholar 

  • Udomsaksakul N, Kodama K, Tanasupawat S, Savarajara A (2018b) Diversity of ethanol fermenting yeasts in coconut inflorescence sap and their application potential. ScienceAsia 44:371–381

    CAS  Google Scholar 

  • Uzochukwu S, Balogh E, Tucknot OG, Lewis MJ, Ngoddy PO (1999) Role of palm wine yeasts and bacteria in palm wine aroma. J Food Sci Technol 36:301–304

    CAS  Google Scholar 

  • Valder R, Nooralabettu KP (2018) Microbial characteristics of freshly tapped Palmyra Palm (Borassus flabellifer) sap. IJSER 9:347–353

    Google Scholar 

  • Vilela A (2018) Lachancea thermotolerans, the non-Saccharomyces yeast that reduces the volatile acidity of wines. Fermentation 4:56. https://doi.org/10.3390/fermentation4030056

    Article  CAS  Google Scholar 

  • Walker GM, Stewart GG (2016) Saccharomyces cerevisiae in the production of fermented beverages. Beverages 2(4):30. https://doi.org/10.3390/beverages2040030

    Article  CAS  Google Scholar 

  • Wang H, Xu YC, Hsueh PR (2016) Epidemiologyof candidemia and antifungal susceptibility in invasive Candida species in the Asia-Pacific region. Future Microbiol 11:1461–1477

    CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee SJ, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide for methods and applications. Academic Press, California, pp 315–322

    Google Scholar 

  • Xu Y, Zhao GA, Wang LP (2006) Controlled formation of volatile components in cider making using a combination of Saccharomyces cerevisiae and Hanseniaspora valbyensis yeast species. J Ind Microbiol Biotechnol 33:192–196

    PubMed  Google Scholar 

  • Yamagata K, Fujita T, Sanchez PC, Takahashi R, Kozaki M (1980) Yeasts isolated from coconut and nipa tuba in the Philippines. Nippon Kingakukai Kaiho 21:469–476

    Google Scholar 

  • Yuangsaard N, Yongmanitchai W, Yamada M, Limtong S (2013) Selection and characterization of a newly isolated thermotolerant Pichia kudriavzevii for ethanol production at high temperature from cassava starch hydrolysate. Antonie Van Leeuwenhoek 103:77–588

    Google Scholar 

  • Zhang BQ, Luan Y, Duan CQ, Yan GL (2018) Use of Torulaspora delbrueckii co-fermentation with two Saccharomyces cerevisiae strains with different aromatic characteristic to improve the diversity of red wine aroma profile. Front Microbiol 9:606. https://doi.org/10.3389/fmicb.2018.00606

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Huo N, Wang Y, Zhang Y, Wang R, Hou H (2017) Aroma-enhancing role of Pichia manshurica isolated from daqu in the brewing of shanxi aged vinegar. Int J Food Prop 20:2169–2179

    CAS  Google Scholar 

  • Zuza-Alves DL, Silva-Rocha WP, Chaves GM (2017) An update on Candida tropicalis based on basic and clinical approaches. Front Microbiol 8:1927

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Thailand Research Fund through a TRF Research Team Promotion grant (RTA6080004) that is providing to Savitree Limtong.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Science, Kasetsart University, Bangkok, 10900, Thailand

    Savitree Limtong

  2. Academy of Science, Royal Society of Thailand, Bangkok, 10300, Thailand

    Savitree Limtong

  3. National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Pathum Thani, 12120, Thailand

    Somjit Am-In & Sasitorn Jindamorakot

  4. Microbiology Program, Department of Science, Faculty of Science and Technology, Bansomdejchaopraya Rajabhat University, Bangkok, 10600, Thailand

    Rungluk Kaewwichian

  5. Division of Microbiology, Faculty of Science and Technology, Phranakhon Si Ayutthaya Rajabhat University, Phranakhon Si Ayutthaya, 13000, Thailand

    Chutima Kaewkrajay

Authors
  1. Savitree Limtong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Somjit Am-In
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rungluk Kaewwichian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chutima Kaewkrajay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sasitorn Jindamorakot
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SL: Designed study, data discussion and writing the manuscript; SA: Performed experiments and data analysis; PK: Data analysis.; CK: Data analysis; SJ: Performed experiments and data analysis.

Corresponding author

Correspondence to Savitree Limtong.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 60 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Limtong, S., Am-In, S., Kaewwichian, R. et al. Exploration of yeast communities in fresh coconut, palmyra, and nipa palm saps and ethanol-fermenting ability of isolated yeasts. Antonie van Leeuwenhoek 113, 2077–2095 (2020). https://doi.org/10.1007/s10482-020-01479-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-020-01479-2

Keywords

Search

Navigation