Advertisement

Analytical and Bioanalytical Chemistry

, Volume 410, Issue 30, pp 7901–7907 | Cite as

Disposable amperometric immunosensor for Saccharomyces cerevisiae based on carboxylated graphene oxide-modified electrodes

  • Boryana Borisova
  • Alfredo Sánchez
  • Paul E. D. Soto-Rodríguez
  • Abderrahmane Boujakhrout
  • María Arévalo-Villena
  • José M. Pingarrón
  • Ana Briones-Pérez
  • Concepción Parrado
  • Reynaldo Villalonga
Research Paper

Abstract

A sensitive and disposable amperometric immunosensor for Saccharomyces cerevisiae was constructed by using carbon screen-printed electrodes modified with propionic acid-functionalized graphene oxide as transduction element. The affinity-based biosensing interface was assembled by covalent immobilization of a specific polyclonal antibody on the carboxylate-enriched electrode surface via a water-soluble carbodiimide/N-hydroxysuccinimide coupling approach. A concanavalin A-peroxidase conjugate was further used as signaling element. The immunosensor allowed the amperometric detection of the yeast in buffer solution and white wine samples in the range of 10–107 CFU/mL. This electroanalytical device also exhibited low detection limit and high selectivity, reproducibility, and storage stability. The immunosensor was successfully validated in spiked white wine samples.

Keywords

Saccharomyces cerevisiae Immunosensor Graphene Wine Screen-printed electrodes 

Notes

Funding information

Financial support from the Spanish Ministry of Economy and Competitiveness (MINECO Projects CTQ2014-58989-P, CTQ2015-71936-REDT and CTQ2017-87954-P), the Junta de Comunidades de Castilla La Mancha (JCCM Project POII-2014-011-A), and the Comunidad de Madrid, Programme NANOAVANSENS (Project S2013/MIT-3029) is gratefully acknowledged.

Compliance with ethical standards

Declaration of conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    German JB, Walzem RL. The health benefits of wine. Annu Rev Nutr. 2000;20:561–93.CrossRefGoogle Scholar
  2. 2.
    International Organization of Vine and Wine. (2018) State of the vitiviniculture world market. Available from: http://www.oiv.int Accessed 6 October 2017.
  3. 3.
    Fleet GH, Heard GM. Yeast-growth during fermentation. In: Fleet GH, editor. Wine microbiology and biotechnology. Boca Ratón: CRC Press; 1993. p. 27–54.Google Scholar
  4. 4.
    Swiegers JH, Batowsky EJ, Henschke PA, Pretorius IS. Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res. 2005;11:139–73.CrossRefGoogle Scholar
  5. 5.
    Fay JC, Benavides JA. Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 2005;1:e5.CrossRefGoogle Scholar
  6. 6.
    Saerens SMG, Delvaux F, Verstrepen KJ, Van Dijck P, Thevelein JM, Delvaux FR. Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol. 2008;74:454–61.CrossRefGoogle Scholar
  7. 7.
    Martorell P, Querol A, Fernández-Espinar MT. Rapid identification and enumeration of Saccharomyces cerevisiae cells in wine by real-time PCR. Appl Environ Microbiol. 2005;71:6823–30.CrossRefGoogle Scholar
  8. 8.
    Loureiro V, Querol A. The prevalence and control of spoilage yeast in foods and beverages. Trends Food Sci Technol. 1999;10:356–65.CrossRefGoogle Scholar
  9. 9.
    Andorrà I, Esteve-Zarzoso B, Guillamón JM, Mas A. Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int J Food Microbiol. 2010;144:257–62.CrossRefGoogle Scholar
  10. 10.
    Salinas F, Garrido D, Ganga A, Veliz G, Martínez C. Taqman real-time PCR for the detection and enumeration of Saccharomyces cerevisiae in wine. Food Microbiol. 2009;26:328–32.CrossRefGoogle Scholar
  11. 11.
    Hierro N, Esteve-Zarzoso B, González A, Mas A, Guillamón JM. Real-time quantitative PCR (QPCR) and reverse transcription-QPCR for detection and enumeration of total yeasts in wine. Appl Environ Microbiol. 2006;72:7148–55.CrossRefGoogle Scholar
  12. 12.
    Ertl P, Mikkelsens SR. Electrochemical biosensor array for the identification of microorganisms based on lectin-lipopolysaccharide recognition. Anal Chem. 2001;73:4241–8.CrossRefGoogle Scholar
  13. 13.
    Heo J, Hua SZ. An overview of recent strategies in pathogen sensing. Sensors. 2009;9:4483–502.CrossRefGoogle Scholar
  14. 14.
    Ivnitski D, Abdel-Hamid I, Atanasov P, Wilkins E, Stricker S. Application of electrochemical biosensors for detection of food pathogenic bacteria. Electroanalysis. 2000;12:317–25.CrossRefGoogle Scholar
  15. 15.
    Hayat A, Marty JL. Disposable screen printed electrochemical sensors: tools for environmental monitoring. Sensors. 2014;14:10432–53.CrossRefGoogle Scholar
  16. 16.
    Villalonga R, Villalonga ML, Díez P, Pingarrón JM. Decorating carbon nanotubes with polyethylene glycol-coated magnetic nanoparticles for implementing highly sensitive enzyme biosensors. J Mater Chem. 2011;21:12858–64.CrossRefGoogle Scholar
  17. 17.
    Malhotra BD, Srivastava S, Ali MA, Singh C. Nanomaterial-based biosensors for food toxin detection. Appl Biochem Biotechnol. 2014;174:880–96.CrossRefGoogle Scholar
  18. 18.
    Zhou M, Zhai Y, Dong S. Electrochemical sensing and biosensing platform based on chemically reduced graphene oxide. Anal Chem. 2009;81:5603–13.CrossRefGoogle Scholar
  19. 19.
    Shao Y, Wang J, Wu H, Liu J, Aksay IA, Lin Y. Graphene based electrochemical sensors and biosensors: a review. Electroanalysis. 2010;22:1027–36.CrossRefGoogle Scholar
  20. 20.
    Pumera M, Ambrosi A, Bonanni A, Chng ELK, Poh HL. Graphene for electrochemical sensing and biosensing. TrAC Trends Anal Chem. 2010;29:954–65.CrossRefGoogle Scholar
  21. 21.
    Pumera M. Graphene-based nanomaterials and their electrochemistry. Chem Soc Rev. 2010;39:4146–57.CrossRefGoogle Scholar
  22. 22.
    Chen D, Feng H, Li J. Graphene oxide: preparation, functionalization, and electrochemical applications. Chem Rev. 2012;112:6027–53.CrossRefGoogle Scholar
  23. 23.
    Povedano E, Cincotto FH, Parrado C, Díez P, Sánchez A, Canevari TC, et al. Decoration of reduced graphene oxide with rhodium nanoparticles for the design of a sensitive electrochemical enzyme biosensor for 17β-estradiol. Biosens Bioelectron. 2017;89:343–51.CrossRefGoogle Scholar
  24. 24.
    Tkacz JS, Cybulska EB, Lampen JO. Specific staining of wall mannan in yeast cells with fluorescein-conjugated concanavalin A. J Bacteriol. 1971;105:1–5.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Spontón PG, Spinelli R, Drago SR, Tonarelli GG, Simonetta AC. Acetylcholinesterase-inhibitor hydrolysates obtained from ‘in vitro’ enzymatic hydrolysis of mannoproteins extracted from different strains of yeasts. Int J Food Sci Technol. 2016;51:300–8.CrossRefGoogle Scholar
  26. 26.
    Borisova B, Villalonga ML, Arévalo-Villena M, Boujakhrout A, Sánchez A, Parrado C, et al. Disposable electrochemical immunosensor for Brettanomyces bruxellensis based on nanogold-reduced graphene oxide hybrid nanomaterial. Anal Bioanal Chem. 2017;409:5667–74.CrossRefGoogle Scholar
  27. 27.
    Arenas CB, Sánchez-Tirado E, Ojeda I, Gómez-Suárez CA, González-Cortés A, Villalonga R, et al. An electrochemical immunosensor for adiponectin using reduced graphene oxide–carboxymethylcellulose hybrid as electrode scaffold. Sensors Actuators B Chem. 2016;223:89–94.CrossRefGoogle Scholar
  28. 28.
    Eletxigerra U, Martínez-Perdiguero J, Merino S, Barderas R, Ruiz-Valdepeñas Montiel V, Villalonga R, et al. Electrochemical magnetoimmunosensor for progesterone receptor determination. Application to the simultaneous detection of estrogen and progesterone breast-cancer related receptors in raw cell lysates. Electroanalysis. 2016;28:1787–94.CrossRefGoogle Scholar
  29. 29.
    Smeekens JM, Xiao H, Wu R. Global analysis of secreted proteins and glycoproteins in Saccharomyces cerevisiae. J Proteome Res. 2017;16:1039–49.CrossRefGoogle Scholar
  30. 30.
    Esteban-Fernández de Ávila B, Araque E, Campuzano S, Pedrero M, Dalkiran B, Barderas R, et al. Dual functional graphene derivative-based electrochemical platforms for direct detection of TP53 gene with single nucleotide poly-morphism selectivity in different raw biological samples. Anal Chem. 2015;87:2290–8.CrossRefGoogle Scholar
  31. 31.
    Han S, Li X, Guo G, Sun Y, Yuan Z. Voltammetric measurement of microorganism populations. Anal Chim Acta. 2000;405:115–21.CrossRefGoogle Scholar
  32. 32.
    Chen H, Heng CK, Puiu PD, Zhou XD, Lee AC, Lim TM, et al. Detection of Saccharomyces cerevisiae immobilized on self-assembled monolayer (SAM) of alkanethiolate using electrochemical impedance spectroscopy. Anal Chim Acta. 2005;554:52–9.CrossRefGoogle Scholar
  33. 33.
    Heiskanen AR, Spégel CF, Kostesha N, Ruzgas T, Emnéus J. Monitoring of Saccharomyces cerevisiae cell proliferation on thiol-modified planar gold microelectrodes using impedance spectroscopy. Langmuir. 2008;24:9066–73.CrossRefGoogle Scholar
  34. 34.
    Andorrà I, Monteiro M, Esteve-Zarzoso B, Albergaria H, Mas A. Analysis and direct quantification of Saccharomyces cerevisiae and Hanseniaspora guilliermondii populations during alcoholic fermentation by fluorescence in situ hybridization, flow cytometry and quantitative PCR. Food Microbiol. 2011;28:1483–91.CrossRefGoogle Scholar
  35. 35.
    Escot S, Feuillat M, Dulau L, Charpentier C. Release of polysaccharides by yeasts and the influence of released polysaccharides on colour stability and wine astringency. Aust J Grape Wine Res. 2001;7:153–9.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Boryana Borisova
    • 1
  • Alfredo Sánchez
    • 1
  • Paul E. D. Soto-Rodríguez
    • 1
  • Abderrahmane Boujakhrout
    • 2
  • María Arévalo-Villena
    • 3
  • José M. Pingarrón
    • 4
  • Ana Briones-Pérez
    • 3
  • Concepción Parrado
    • 1
  • Reynaldo Villalonga
    • 1
  1. 1.Nanosensors and Nanomachines Group, Department of Analytical Chemistry, Faculty of ChemistryComplutense University of MadridMadridSpain
  2. 2.Orion High Technologies S.L.ParlaSpain
  3. 3.Regional Institute of Applied Scientific Research (RIASR)Universidad de Castilla-La ManchaCiudad RealSpain
  4. 4.Department of Analytical Chemistry, Faculty of ChemistryComplutense University of MadridMadridSpain

Personalised recommendations