Skip to main content
SpringerLink
Log in

Interaction of Saccharomyces cerevisiae–Lactobacillus fermentum–Dekkera bruxellensis and feedstock on fuel ethanol fermentation

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

Abstract

The alcoholic fermentation for fuel ethanol production in Brazil occurs in the presence of several microorganisms present with the starter strain of Saccharomyces cerevisiae in sugarcane musts. It is expected that a multitude of microbial interactions may exist and impact on the fermentation yield. The yeast Dekkera bruxellensis and the bacterium Lactobacillus fermentum are important and frequent contaminants of industrial processes, although reports on the effects of both microorganisms simultaneously in ethanolic fermentation are scarce. The aim of this work was to determine the effects and interactions of both contaminants on the ethanolic fermentation carried out by the industrial yeast S. cerevisiae PE-2 in two different feedstocks (sugarcane juice and molasses) by running multiple batch fermentations with the starter yeast in pure or co-cultures with D. bruxellensis and/or L. fermentum. The fermentations contaminated with D. bruxellensis or L. fermentum or both together resulted in a lower average yield of ethanol, but it was higher in molasses than that of sugarcane juice. The decrease in the CFU number of S. cerevisiae was verified only in co-cultures with both D. bruxellensis and L. fermentum concomitant with higher residual sucrose concentration, lower glycerol and organic acid production in spite of a high reduction in the medium pH in both feedstocks. The growth of D. bruxellensis was stimulated in the presence of L. fermentum resulting in a more pronounced effect on the fermentation parameters than the effects of contamination by each microorganism individually.

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
Fig. 4

Similar content being viewed by others

References

  • Amorim HV, Lopes ML, Oliveira JVC, Buckeridge MS, Goldman GH (2011) Scientific challenges of bioethanol production in Brazil. Appl Microbiol Biotechnol 91:1267–1275

    Article  PubMed  CAS  Google Scholar 

  • Andrietta MGS, Andrietta SR, Stupiello ENA (2011) Bioethanol—what has Brazil learned about yeasts inhabiting the ethanol production processes from sugar cane? In: Bernardes MAS (ed) Biofuel production—recent developments and prospects. InTech, Rijeka, pp 67–84

    Google Scholar 

  • Barnett JA, Payne RW, Yarrow D (2000) Yeasts: characteristics and identification. Cambridge University Press, Cambridge

    Google Scholar 

  • Bassi APG, Silva JCG, Reis VR, Ceccato-Antonini SR (2013) Effects of single and combined cell treatments based on low pH and high concentrations of ethanol on the growth and fermentation of Dekkera bruxellensis and Saccharomyces cerevisiae. World J Microbiol Biotechnol 29:1661–1676

    Article  PubMed  CAS  Google Scholar 

  • Basso LC, Amorim HV, Oliveira AJ, Lopes ML (2008) Yeast selection for fuel ethanol production in Brazil. FEMS Yeast Res 8:1155–1163

    Article  PubMed  CAS  Google Scholar 

  • Basso TO, Gomes FS, Lopes ML, Amorim HV, Eggleston G, Basso LC (2014) Homo- and heterofermentative lactobacilli differently affect sugarcane-based fuel ethanol fermentation. Antonie Van Leeuwenhoek 105:169–177

    Article  PubMed  CAS  Google Scholar 

  • Blomqvist J (2011) Dekkera bruxellensis—a competitive yeast for ethanol production from conventional and non-conventional substrates. PhD Thesis, Swedish University of Agricultural Sciences

  • Bonatelli ML, Quecine MC, Silva MS, Labate CA (2017) Characterization of the contaminant bacterial communities in sugarcane first-generation industrial ethanol production. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnx159

    Article  PubMed  Google Scholar 

  • Burns TR, Osborne JP (2013) Impact of malolactic fermentation on the color and color stability of pinot noir and merlot wine. Am J Enol Vitic 64:370–377

    Article  CAS  Google Scholar 

  • Cardenas N, Laiño JE, Delgado S, Jiménez E, Del Valle MJ, de Giori GS, Sesma F, Mayo B, Fernández L, LeBlanc JG, Rodriguez JM (2015) Relationships between the genome and some phenotypical properties of Lactobacillus fermentum CECT 5716, a probiotic strain isolated from human milk. Appl Microbiol Biotechnol 99:4343–4353

    Article  PubMed  CAS  Google Scholar 

  • Carvalho-Netto OV, Carazzolle MF, Mofatto LS, Teixeira PJPL, Noronha MF, Calderón LAL, Mieczkowski PA, Argueso JL, Pereira GAG (2015) Saccharomyces cerevisiae transcription reprogramming due to bacterial contamination during industrial scale bioethanol production. Microb Cell Fact 14:1–13

    Article  CAS  Google Scholar 

  • Cogan TM, Jordan KN (1994) Metabolism of Leuconostoc bacteria. J Dairy Sci 77:2704–2717

    Article  CAS  Google Scholar 

  • Conterno L, Fondazione E, Henick-Kling T (2010) Brettanomyces/Dekkera off-flavours and other wine faults associated with microbial spoilage. In: Reynolds AG (ed) Managing wine quality. Woodhead Publishing, Cambridge, pp 346–387

    Chapter  Google Scholar 

  • Costa MAS, Cerri BC, Ceccato-Antonini SR (2017) Ethanol addition enhances acid treatment to eliminate Lactobacillus fermentum from the fermentation process for fuel ethanol production. Lett Appl Microbiol. https://doi.org/10.1111/lam.12819

    Article  PubMed  Google Scholar 

  • Curtin CD, Langhans G, Henschke PA, Grbin PR (2013) Impact of Australian Dekkera bruxellensis strains grown under oxygen-limited conditions on model wine composition and aroma. Food Microbiol 36:241–247

    Article  PubMed  CAS  Google Scholar 

  • Duarte-Almeida JM, Salatino A, Genovese MI, Lajolo FM (2011) Phenolic composition and antioxidant activity of culms and sugarcane (Saccharum officinarum L.) products. Food Chem 125:660–664

    Article  CAS  Google Scholar 

  • Filannino P, Gobbetti M, de Angelis M, di Cagno R (2014) Hydroxycinnamic acids used as external acceptors of electrons: an energetic advantage for strictly heterofermentative lactic acid bacteria. Appl Environ Microbiol 80(24):7574–7582

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Galafassi S, Capusoni C, Moktaduzzaman M, Compagno C (2013) Utilization of nitrate abolishes the ‘Custers effect’ in Dekkera bruxellensis and determines a different pattern of fermentation products. J Ind Microbiol Biotechnol 40:297–303

    Article  PubMed  CAS  Google Scholar 

  • Heresztyn T (1986) Formation of substituted tetrahydropyridines by species of Brettanomyces and Lactobacillus isolated from mousy wines. Am J Enol Vitic 37:127–131

    CAS  Google Scholar 

  • Hucker B, Christophersen M, Vriesekoop F (2017) The influence of thiamine and riboflavin on various spoilage microorganisms commonly found in beer. J Inst Brew 123:24–30

    Article  CAS  Google Scholar 

  • Jayashree S, Rajendhran J, Jayaraman K, Kalaichelvan G, Gunasekaran P (2011) Improvement of riboflavin production by Lactobacillus fermentum isolated from yogurt. Food Biotechnol 25:240–251

    Article  CAS  Google Scholar 

  • Kheir J, Salameh D, Strehaiano P, Brandam C, Lteif R (2013) Impact of volatile phenols and their precursors on wine quality and control measures of Brettanomyces/Dekkera yeasts. Eur Food Res Technol 237(5):655–671

    Article  CAS  Google Scholar 

  • Kosel J, Cadez N, Raspor P (2014) Factors affecting volatile phenol production during fermentations with pure and mixed cultures of Dekkera bruxellensis and Saccharomyces cerevisiae. Food Technol Biotechnol 52(1):35–45

    CAS  Google Scholar 

  • LeBlanc JG, Lain JE, del Valle JM, Vannini V, van Sinderen D, Taranto MP, Font de Valdez G, Savoy de Giori G, Sesma F (2011) B-Group vitamin production by lactic acid bacteria—current knowledge and potential applications. J Appl Microbiol 111:1297–1309

    Article  PubMed  CAS  Google Scholar 

  • LeBlanc JG, Chain F, Martin R, Bermudez-Humaran LG, Courau S, Langella P (2017) Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Fact 16:79–89

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee SS, Robinson FM, Wang HY (1981) Rapid determination of yeast viability. Biotechnol Bioeng 11:641–649

    Google Scholar 

  • Leite FCB, Basso TO, de Barros Pita W, Gombert AK, Simões DA, Morais MA Jr (2013) Quantitative aerobic physiology of the yeast Dekkera bruxellensis, a major contaminant in bioethanol production plants. FEMS Yeast Res 13:34–43

    Article  PubMed  CAS  Google Scholar 

  • Lopes ML, Paulillo SCL, Godoy A, Cherubin RA, Lorenzi MS, Giometti FHC, Bernardino CD, Amorim Neto HB, Amorim HV (2016) Ethanol production in Brazil: a bridge between science and industry. Braz J Microbiol 47(1):64–76

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lucena BTL, dos Santos BM, Moreira JLS, Moreira APB, Nunes AC, Azevedo V, Miuoshi A, Thompson FL, Morais MA Jr (2010) Diversity of lactic acid bacteria of the bioethanol process. BMC Microbiol 10:298–305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martín R, Olivares M, Marín ML, Xaus J, Fernández L, Rodríguez JM (2005) Characterization of a reuterin-producing Lactobacillus coryniformis strain isolated from a goat’s milk cheese. Int J Food Microbiol 104:267–277

    Article  PubMed  CAS  Google Scholar 

  • Meneghin MC, Bassi APG, Codato CB, Reis VR, Ceccato-Antonini SR (2013) Fermentative and growth performances of Dekkera bruxellensis in different batch systems and the effect of initial low cell counts in co cultures with Saccharomyces cerevisiae. Yeast 30:295–305

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Naczak M, Shahidi F (2006) Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J Pharm Biomed Anal 41(5):1523–1542

    Article  CAS  Google Scholar 

  • National Center for Biotechnology Information (2017) PubChem Compound Database, CID 31242. https://pubchem.ncbi.nlm.nih.gov/compound/31242. Accessed 19 Dec 2017

  • Passoth V, Blomqvist J, Schnurer J (2007) Dekkera bruxellensis and Lactobacillus vini form a stable ethanol-producing consortium in a commercial alcohol production process. Appl Environ Microbiol 73:4354–4356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pereira LF, Bassi APG, Avansini SH, Neto AG, Brasileiro BT, Ceccato-Antonini SR, Morais MA Jr (2012) The physiological characteristics of the yeast Dekkera bruxellensis in fully fermentative conditions with cell recycling and in mixed cultures with Saccharomyces cerevisiae. Antonie Van Leeuwenhoek 101:529–539

    Article  PubMed  CAS  Google Scholar 

  • Pereira LF, Lucatti E, Basso LC, Morais MA Jr (2014) The fermentation of sugarcane molasses by Dekkera bruxellensis and the mobilization of reserve carbohydrates. Antonie Van Leeuwenhoek 105:481–489

    Article  PubMed  CAS  Google Scholar 

  • Pinto JT, Zempleni J (2016) Riboflavin. Adv Nutr 7(5):973–975

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pita WB, Leite FCB, Souza- Liberal AT, Simões DA, Morais MA Jr (2011) The ability to use nitrate confers advantage to Dekkera bruxellensis over S. cerevisiae and can explain its adaptation to industrial fermentation processes. Antonie Van Leeuwenhoek 100:99–107

    Article  CAS  Google Scholar 

  • Reis VRR, Bassi APG, Cerri BC, Almeida AR, Carvalho IGB, Bastos RG, Ceccato-Antonini SR (2018) Effects of feedstock and co-culture of Lactobacillus fermentum and wild Saccharomyces cerevisiae strain during fuel ethanol fermentation by the industrial yeast strain PE-2. AMB Express 8:23. https://doi.org/10.1186/s13568-018-0556-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rodriguez H, Curiel JÁ, Landete JM, de las Rivas B, Felipe FL, Gómez-Cordovés C, Mancheño JM, Muñoz R (2009) Food phenolics and lactic acid bacteria. Int J Food Microbiol 132:79–90

    Article  PubMed  CAS  Google Scholar 

  • Santos F, Wegkamp A, de Vos WM, Smid EJ, Hugenholtz J (2008) High-level folate production in fermented foods by the B12 producer Lactobacillus reuteri JCM1112. Appl Environ Microbiol 74:3291–3294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silva I, Campos FM, Hogg T, Couto JA (2011) Factors influencing the production of volatile phenols by wine lactic acid bacteria. Int J Food Microbiol 145:471–475

    Article  PubMed  CAS  Google Scholar 

  • Souza RB, dos Santos BM, Rodrigues de Souza RF, Silva PKN, Lucena BTL, Morais MA Jr (2012) The consequences of Lactobacillus vini and Dekkera bruxellensis as contaminants of the sugarcane-based ethanol fermentation. J Ind Microbiol Biotechnol 39:1645–1650

    Article  PubMed  CAS  Google Scholar 

  • Souza-Liberal AT, Basilio ACM, Brasileiro BTRV, Silva Filho EA, Simões DA, Morais MA Jr (2007) Identification of Dekkera bruxellensis as a major contaminant yeast in continuous fuel ethanol fermentation. J Appl Microbiol 102:538–547

    Article  PubMed  CAS  Google Scholar 

  • Spaepen M, van Oevelen D, Verachtert H (1978) Fatty acids and esters produced during the spontaneous fermentation of lambic and gueuze. J Inst Brew 84:278–282

    Article  CAS  Google Scholar 

  • Tiukova I (2014) Dekkera bruxellensis, a non-conventional ethanol production yeast. PhD Thesis, Swedish University of Agricultural Sciences

  • Tiukova I, Eberhard T, Passoth V (2014) Interaction of Lactobacillus vini with the ethanol-producing yeasts Dekkera bruxellensis and Saccharomyces cerevisiae. Biotechnol Appl Biochem 61:40–44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • von Weymarn N, Hujanen M, Leisola M (2002) Production of d-mannitol by hetero-fermentative lactic acid bacteria. Process Biochem 37:1207–1213

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Research Grant No. 2011/17928-0; Scholarship Grant No. 2012/16258-4 to A. P. G. Bassi) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Scholarship Grant No. 301701/2012-1 to S. R. Ceccato-Antonini). The authors wish to acknowledge the Centro de Tecnologias Estratégicas do Nordeste (CETENE) for the chromatographic analysis.

Author information

Authors and Affiliations

  1. Laboratory of Molecular and Agricultural Microbiology, Dept Tecnologia Agroindustrial e Sócio-Economia Rural, Centro de Ciências Agrárias, Universidade Federal de São Carlos, P.O. Box 153, Araras, São Paulo State, 13600-970, Brazil

    Ana Paula Guarnieri Bassi, Leticia Meneguello, Anna Livia Paraluppi, Beatriz Cristina Pecoraro Sanches & Sandra Regina Ceccato-Antonini

Authors
  1. Ana Paula Guarnieri Bassi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leticia Meneguello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Livia Paraluppi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Beatriz Cristina Pecoraro Sanches
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sandra Regina Ceccato-Antonini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandra Regina Ceccato-Antonini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

No ethical approval was required, as this study did not involve human participants or animals.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bassi, A.P.G., Meneguello, L., Paraluppi, A.L. et al. Interaction of Saccharomyces cerevisiae–Lactobacillus fermentum–Dekkera bruxellensis and feedstock on fuel ethanol fermentation. Antonie van Leeuwenhoek 111, 1661–1672 (2018). https://doi.org/10.1007/s10482-018-1056-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-018-1056-2

Keywords

Search

Navigation