SpringerLink
Log in

Novel yeasts with potential probiotic characteristics isolated from the endogenous ferment of artisanal Minas cheese

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Artisanal Minas cheese (QMA) is traditionally elaborate using raw milk and endogenous ferment (**o — whey or rala — grated ripened cheese). In the present study, 91 yeast strains were isolated and identified from **o and rala. Eight yeast species were identified by the MALDI-TOF mass spectrometry and confirmed by sequencing of the ITS region. The yeasts’ protease and lipase activities were evaluated in addition to probiotic properties such as tolerance to low pH and bile salts, hydrophobicity, autoaggregation, co-aggregation with pathogens, and antimicrobial susceptibility. The rala ferment showed a greater variety of species. Yarrowia lipolytica was the dominant specie (52.7% of isolates), followed by the Kluyveromyces lactis and Kodamaea ohmeri (9.9 and 6.6%, respectively). From the total yeasts evaluated, 74 strains showed positive enzymatic activity: 52 strains showed lipolytic (51 Y. lipolytica and one Trichosporon japonicum) and 44 proteolytic activities (18 Y. lipolytica, 13 K. ohmeri, 11 K. lactis, and 2 Wickerhamiella sp.). All evaluated isolates demonstrated tolerance to pH 2.0, and 69 isolates supported the presence of bile salts. From them, 12 isolates showed the capacity of autoaggregation (> 30%) and hydrophobicity (> 90.0%) and were then selected for co-aggregation and antibiotic resistance assays. All selected isolates showed co-aggregation with Salmonella Enteritidis, Escherichia coli, and Listeria monocytogenes greater than 30%. None of the yeast showed sensibility to the evaluated antibiotics and antagonistic activity against the evaluated pathogens. The results demonstrated that **o and rala have different yeast composition with different enzymatic activity, which may affect the characteristics of the cheese. Furthermore, some yeast strains: Y. lipolytica (9 strains isolated from rala) and K. ohmeri (3 strains isolated from **o) demonstrated attractive probiotic potential.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  1. EMATER-MG (2021) Minas Gerais conquista 40 das 57 medalhas do Brasil em concurso mundial de queijos na França. Retrieved from https://www.emater.mg.gov.br/portal.do/site-noticias/minas-gerais-conquista-40-das-57-medalhas-do-brasil-em-concurso-mundial-de-queijos-na-franca/?flagweb=novosite_pagina_interna_noticia&id=25889. Accessed 16 Jul 2021

  2. FIEMG (2019) Queijos mineiros são premiados em concurso na França. Retrieved from https://www7.fiemg.com.br/noticias/detalhe/queijos-mineiros-sao-premiados-em-concurso-na-franca. Accessed 16 Jul 2021

  3. Filho MJ, Klein B, Wagner R, Godoy HT (2021) Key aroma compounds of Canastra cheese: HS-SPME optimization assisted by olfactometry and chemometrics. Food Res Int 150(10):110788. https://doi.org/10.1016/j.foodres.2021.110788

    Article  CAS  Google Scholar 

  4. Kamimura BA, Magnani M, Luciano WA, Campagnollo FB, Pimentel TC, Alvarenga VO, Plegrino BO, Cruz AG, AS S’A (2019) Brazilian artisanal cheeses: an overview of their characteristics, main types and regulatory aspects. Compr Rev Food Sci Food Saf 18:1636–1657. https://doi.org/10.1111/1541-4337.12486

    Article  PubMed  Google Scholar 

  5. IPHAN (2008) Modo artesanal de fazer queijo de Minas: Serro, Serra da Canastra e Serra do Salitre (Alto Paranaíba) / Instituto do Patrimônio histórico e artístico nacional. Retrieved from http://portal.iphan.gov.br/uploads/publicacao/Dossie_Queijo_de_Minas_web.pdf. Accessed 16 Jul 2021

  6. Minas Gerais (2002) Lei estadual n° 14.185. Dispõe sobre o processo de produção do Queijo Minas Artesanal e dá outras providências. Secretaria de Agricultura, Pecuária e Abastecimento de Minas Gerais. Retrieved from https://leisestaduais.com.br/mg/lei-ordinaria-n-14185-2002-minas-gerais-dispoe-sobre-o-processo-de-producao-do-queijo-minas-artesanal-e-da-outras-providencias. Accessed 16 Jul 2021

  7. Oliveira SPP, Martins JM, Nogueira CH, Vale RC, Rodrigues MPJ, Galleti AN (2018) Características físico-químicas de queijo Minas artesanal do Serro fabricados com **o e com rala. Rev Inst Lat Cândido Tostes 73:235–244. https://doi.org/10.14295/2238-6416.v73i4.717

    Article  CAS  Google Scholar 

  8. Do Vale RC, Rodrigues MPJ, Martins JM (2018) Influência do tipo de fermento nas características físico-químicas de queijo Minas artesanal do Serro – Minas Gerais, maturado em condições controladas. Revista do Instituto de Laticínios Cândido Tostes, Juiz de Fora 73(2):82–90. https://doi.org/10.14295/2238-6416.v73i2.686

    Article  Google Scholar 

  9. Andretta M, Almeida TT, Ferreira LR, Carvalho AF, Yamatogi RS, Nero LA (2019) Microbial safety status of Serro artisanal cheese produced in Brazil. Journal of Dairy Science 102:10790–10798. https://doi.org/10.3168/jds.2019-16967

    Article  CAS  PubMed  Google Scholar 

  10. BRASIL (2018) Lei n°13.680, de 14 de junho de 2018. Altera a Lei de n°1.283 de dezembro de 1950, para dispor sobre o processo de fiscalização de produtos alimentícios de origem animal produzidos de forma artesanal. Retrieved from https://www2.camara.leg.br/legin/fed/lei/2018/lei-13680-14-junho-2018-786861-publicacaooriginal-155848-pl.html. Accessed 16 Jul 2021

  11. Nero LA, Andretta M, Almeida TT, Ferreira LR, Camargo AC, Yamatogi RS, Carvalho AF, Call DR (2021) Lactic microbiota of the Minas artisanal cheese produced in the Serro region, Minas Gerais, Brazil. LWT – Food Sci Technol 148:111698. https://doi.org/10.1016/j.lwt.2021.111698

    Article  CAS  Google Scholar 

  12. Margalho LP, Feliciano MD, Silva CE, Abreu JS, Piran MVF, Sant’Ana AS (2020) Brazilian artisanal cheeses are rich and diverse sources of nonstarter lactic acid bacteria regarding technological, biopreservative, and safety properties- insights through multivariate analysis. J Dairy Sci 103(9):7908–7926. https://doi.org/10.3168/jds.2020-18194

    Article  CAS  PubMed  Google Scholar 

  13. Perin LM, Sardaro MLS, Nero LA, Neviani E, Gatti M (2017) Bacterial ecology of artisanal Minas cheeses evaluated by culture-dependent and independent methods. Food Microbiol 65:160–169. https://doi.org/10.1016/j.fm.2017.02.005

    Article  CAS  PubMed  Google Scholar 

  14. Campagnollo FB, Margalho LP, Kamimura BA, Feliciano MD, Freire L, Lopes LS, Alvarenga VO, Cadavez VAP, Gonzales-Barron U, Schaffner DW, AS S’A (2018) Selection of indigenous lactic acid bacteria presenting anti-listerial activity, and their role in reducing the maturation period and assuring the safety of traditional Brazilian cheeses. Food Microbiol 73:288–297. https://doi.org/10.1016/j.fm.2018.02.006

    Article  CAS  PubMed  Google Scholar 

  15. Souza TP, Evangelista SR, Passamani FRF, Bertechini R, de Abreu LR, Batista LR (2021) Mycobiota of Minas artisanal cheese: safety and quality. Int Dairy J 120:105085. https://doi.org/10.1016/j.idairyj.2021.105085

    Article  CAS  Google Scholar 

  16. Saad SMI (2006) Probióticos e prebióticos: o estado da arte. Rev Bras Cienc Farm 42(1):1–16. https://doi.org/10.1590/S1516-93322006000100002

    Article  CAS  Google Scholar 

  17. ANVISA (2021) Guia para instrução processual de petição de avaliação de probióticos para uso em alimentos. Retrieved from http://antigo.anvisa.gov.br/documents/10181/5280930/guia+21+v2.pdf/dac5bf5f-ae56-4444-b53c-2cf0f7c15301. Acessed 16 Jul 2021

  18. Hill C, Guardião F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  19. FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Joint working group report on drafting guidelines for the evaluation of probiotics in food. Retrieved from https://www.mhlw.go.jp/file/05-Shingikai-11121000-Iyakushokuhinkyoku-Soumuka/0000197343.pdf. Accessed 21 Jul 2021

  20. Liu W, Chen M, Duo L, Wang J, Guo S, Haotian S, Menghe B, Zhang H (2020) Characterization of potentially probiotic lactic acid bacteria and bifidobacteria isolated from human colostrum. J Dairy Sci 103(5):4013–4025. https://doi.org/10.3168/jds.2019-17602

    Article  CAS  PubMed  Google Scholar 

  21. Reuben RC, Roy PC, Sarkar SL, Rubayet ASM, Alam UI, Jahid IK (2020) Characterization and evaluation of lactic acid bacteria from indigenous raw milk for potential probiotic properties. J Dairy Sci 103(2):1223–1237. https://doi.org/10.3168/jds.2019-17092

    Article  CAS  PubMed  Google Scholar 

  22. Zhang D, Zhang S, Guidesi E, Zonenschain D, Sagheddu V, Lim CY, Elli M (2017) Isolation and characterization of new probiotic strains from Chinese babies. J Clin Gastroenterol 52:S27–S34. https://doi.org/10.1097/MCG.0000000000001113

    Article  CAS  Google Scholar 

  23. Awasti N, Tomar SK, Pophaly SD, Poonam LVK, Singh TP, Anand S (2016) Probiotic and functional characterization of bifidobacteria of Indian human origin. J Appl Microbiol 120(4):1021–1032. https://doi.org/10.1111/jam.13086

    Article  CAS  PubMed  Google Scholar 

  24. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolated from Brazilian food products. Food Microbiol 36(1):22–29. https://doi.org/10.1016/j.fm.2013.03.010

    Article  CAS  PubMed  Google Scholar 

  25. Minj J, Chandra P, Paulo C, Sharma RK (2021) Bio-functional properties of probiotic Lactobacillus: current applications and research perspectives. Crit Rev Food Sci Nutr 61(13):2207–2224. https://doi.org/10.1080/10408398.2020.1774496

    Article  CAS  PubMed  Google Scholar 

  26. Bonatsou S, Karamouza M, Zoumpopoulou G, Mavrogonatou E, Kletsas D, Papadimitriou K, Tsakalidou E, Nychas G-JE, Panagou EZ (2018) Evaluating the probiotic potential and technological characteristics of yeasts implicated in cv. Kalamata natural black olive fermentation. Int J Food Microbiol 271:48–59. https://doi.org/10.1016/j.ijfoodmicro.2018.02.018

    Article  CAS  PubMed  Google Scholar 

  27. Chen P, Zhang Q, Dang H, Liu X, Tian F, Zhao J, Chen Y, Zhang H, Chen W (2014) Screening for potential new probiotic based on probiotic properties and αglucosidase inhibitory activity. Food Control 35:65–72. https://doi.org/10.1016/j.foodcont.2013.06.027

    Article  CAS  Google Scholar 

  28. Czerucka D, Piche T, Rampal P (2007) Review article: yeast as probiotics - Saccharomyces boulardii. Aliment Pharmacol Ther 26(6):767–778. https://doi.org/10.1111/j.1365-2036.2007.03442.x

    Article  CAS  PubMed  Google Scholar 

  29. Quarella S, Lovrovich P, Scalabrin S, Campedelli A, Backovic V, Gatto V, Cattonaro F, Turello A, Torriani S, Felis GE (2016) Draft genome sequence of the probiotic yeast Kluyveromyces marxianus fragilis B0399. Genome Amnounc 4:e00923-16. https://doi.org/10.1128/genomeA.00923-16

    Article  Google Scholar 

  30. Cecchini FN, Zanvit A, Miclavez A, Nobili P (2018) Halitosis treatment through the administration of antibiotic-resistant probiotic lactic yeast Kluyveromyces marxianus fragilis B0399 (K-B0399). Biomed J Scient Tech Res 12:8887–8890. https://doi.org/10.26717/BJSTR.2018.12.002180.

    Article  Google Scholar 

  31. Navarro-López V, Hernández-Belmonte A, Pérez Soto MI, Ayo-González M, Losa-Rodríguez G, Ros-Sánchez E, Martínez-Gabarrón M, Sánchez-Pellicer P, Aguera-Santos J, Núñez-Delegido E, Ruzafa-Costas B, Picó-Monllor JA, Navarro-Moratalla L (2022) Oral intake of Kluyveromyces marxianus B0399 plus Lactobacillus rhamnosus CECT 30579 to mitigate symptoms in COVID-19 patients: a randomized open label clinical trial. Med Microecol 14:100061. https://doi.org/10.1016/j.medmic.2022.100061

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sen S, Mansell TJ (2020) Yeasts as probiotics: mechanisms, outcomes, and future potential. Fungal Genet Biol 137:103333. https://doi.org/10.1016/j.fgb.2020.103333

    Article  CAS  PubMed  Google Scholar 

  33. Sengun IY, Nielsen DS, Karapinar M, Jakobsen M (2009) Identification of lactic acid bacteria isolated from Tarhana, a traditional Turkish fermented food. Int J Food Microbiol 135(2):105. https://doi.org/10.1016/j.ijfoodmicro.2009.07.033

    Article  CAS  PubMed  Google Scholar 

  34. Naumov GI, Ivannikova IV, Naumov GI (2004) Genetic differentiation of the sherry yeasts Saccharomyces cerevisiae. Appl Biochem Microbiol 41(6):578–582. https://doi.org/10.1007/s10438-005-0105-6

    Article  CAS  Google Scholar 

  35. Sperb JGC, Costa TM, Vaz DA, Valle JAB, Valle RCSC, Tavares LBB (2015) Análise qualitativa da produção de lipases e biossurfactantes por fungos isolados de resíduos oleosos. Engevista 17(3):385–397. https://doi.org/10.22409/engevista.v17i3.690

    Article  Google Scholar 

  36. Colen G, Junqueira RG, Moraes-Santos T (2006) Isolation and screening of alkaline lipase-production fungi from Brazil savanna soil. World J Microbiol Biotechnol 22:881–885. https://doi.org/10.1007/s11274-005-9118-9

    Article  CAS  Google Scholar 

  37. Oliveira RSB, Figueiredo IST, Freitas LBN, Pinheiro RSP, Brito GAC, Alencar NMN, Ramos MV, Ralph MT, Lima-Filho JV (2012) Inflammation induced by phytomodulatory proteins from the látex of Calotropis procera (Asclepiadaceae) protects against Salmonella infection in a murine model of typhoid fever. Inflamm Res 61:689–698. https://doi.org/10.1007/s00011-012-0460-8

    Article  CAS  PubMed  Google Scholar 

  38. Saini K, Tomar SK (2017) In vitro evaluation of probiotic potential of Lactobacillus cultures of human origin capable of selenium bioaccumulation. LWT – Food. Sci Technol 84:497–504. https://doi.org/10.1016/j.lwt.2017.05.034

    Article  CAS  Google Scholar 

  39. Koss B, Suskovic J, Vukovic S, Simpraga M, Frece J, Matosic S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94(6):981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  Google Scholar 

  40. Binetti A, Carrasco M, Reinheimer J, Suárez V (2013) Yeasts from autochthonal cheese starters: technological and functional properties. J Appl Microbiol 115(2):434–444. https://doi.org/10.1111/jam.12228

    Article  CAS  PubMed  Google Scholar 

  41. Cebeci A, Cürakan C (2003) Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol 20(5):511–518. https://doi.org/10.1016/S0740-0020(02)00174-0

    Article  Google Scholar 

  42. Fraberger V, Ammer C, Doming KJ (2020) Functional properties and sustainability improvement of sourdough bread by lactic acid bacteria. Microorganisms 8(12):1895. https://doi.org/10.3390/microorganisms8121895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Jorgensen JH, Ferraro MJ (2009) Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Infect Dis 49(11):1749–1755. https://doi.org/10.1086/647952

    Article  CAS  PubMed  Google Scholar 

  44. Pinto MS, Lempk MW, Cabrini CC, Saraiva LKV, Cangussu RRC, Cunha ALFS (2016) Physicochemical and microbiological characteristics of traditional Minas cheese produced in the micro-region of Montes Claros – MG. Rev Inst Lat Cândido Tostes 71(1):43–52. https://doi.org/10.14295/2238-6416.v70i1.514

    Article  CAS  Google Scholar 

  45. Lima CDLC, Lima LA, Cerqueira MMOP, Ferreira EG, Rosa CA (2009) Bactérias do acido láctico e leveduras associadas com o queijo-de- minas artesanal produzido na região da Serra do Salitre, Minas Gerais. Arq Bras Med Vet Zootec 61(1):266–272. https://doi.org/10.1590/S0102-09352009000100037

    Article  Google Scholar 

  46. Bier M, Tutija JF, Pasquatti TN, Oliveira TL, Araújo FR, Verbisck NV (2017) Identificação por espectrometria de massa MALDI-TOF de Salmonella ssp. e Escherichia coli isolados de carcaças bovinas. Pesq Vet Bras 37(12):1373–1379. https://doi.org/10.1590/S0100-736X2017001200003

    Article  Google Scholar 

  47. Pavlovic M, Mewes A, Maggipinto M, Schimidt W, Messelhauber U, Balsliemke J, Hormansdorfer S, Busch U, Huber I (2014) MALDI-TOF MS based identification of food-borne yeast isolates. J Microbiol Methods 106:123–128. https://doi.org/10.1016/j.mimet.2014.08.021

    Article  CAS  PubMed  Google Scholar 

  48. Usbeck JC, Wilde C, Bertrand D, Behr J, Vogel RF (2014) Wine yeast ty** by MALDI-TOF MS. Appl Microbiol Biotechnol 98(8):3737–3752. https://doi.org/10.1007/s00253-014-5586-x

    Article  CAS  PubMed  Google Scholar 

  49. Amorim JC, Schwan RF, Duarte WF (2016) Sugar cane spirit (cachaça): effects of mixed inoculum of yeasts on the sensory and chemical characteristics. Food Res Int 85:76–83. https://doi.org/10.1016/j.foodres.2016.04.014

    Article  CAS  PubMed  Google Scholar 

  50. Cardoso VM, Borelli BM, Lara CA, Soares MA, Pataro C, Bodevan EC, Rosa CA (2015) The influence of seasons and ripening time on yeast communities of a traditional Brazilian cheese. Food Res Int 69:331–340. https://doi.org/10.1016/j.foodres.2014.12.040

    Article  CAS  Google Scholar 

  51. Younis G, Awad A, Dawod RE, Yousef NE (2017) Antimicrobial activity of yeasts against some pathogenic bacteria. Vet Word 10(8):979–983. https://doi.org/10.14202/vetworld.2017.979-983

    Article  CAS  Google Scholar 

  52. Gardini F, Tofalo R, Belleti N, Iucci L, Suzzi G, Torriani S, Guerzoni ME, Lanciotti R (2006) Characterization of yeasts involved in the ripening of Pecorino Crotonese cheese. Food Microbiol 23(7):641–648. https://doi.org/10.1016/j.fm.2005.12.005

    Article  CAS  PubMed  Google Scholar 

  53. Borelli BM, Ferreira EG, Lacerda ICA, Franco GR, Rosa CA (2006) Yeast populations associated with the artisanal cheese produced in the region of Serra da Canastra, Brazil. World J Microbiol Biotechnol 22:1115–1119. https://doi.org/10.1007/s11274-006-9151-3

    Article  CAS  Google Scholar 

  54. Freitas AC, Pintado AE, Pintado ME, Malcata FX (1999) Role of dominant microflora of Picante cheese on proteolysis and lipolysis. Int Dairy J 9(9):593–603. https://doi.org/10.1016/S0958-6946(99)00129-6

    Article  CAS  Google Scholar 

  55. Nóbrega JE, Ferreira CLLF, Dores MT, Ferreira EM, Domingo EC, Santos JPV (2008) Variações na microbiota leveduriforme do fermento endógeno utilizado na produção do Queijo Canastra. Rev Inst Lat “Cândido Tostes” 63(364):14–18

    Google Scholar 

  56. Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM (2001) Recent advances in cheese microbiology. Int Dairy J 11:259–274. https://doi.org/10.1016/S0958-6946(01)00056-5

    Article  CAS  Google Scholar 

  57. Bove P, Russo P, Capozzi V, Gallone A, Spano G, Fiocco D (2013) Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: carrier matrix effect and transcriptional analysis of genes associated to stress and probiotic. Microbiol Res 168(6):351–359. https://doi.org/10.1016/j.micres.2013.01.004

    Article  CAS  PubMed  Google Scholar 

  58. Oelschlaeger TA (2010) Mechanisms of probiotic actions – a review. Int J Med Microbiol 300(1):57–62. https://doi.org/10.1016/j.ijmm.2009.08.005

    Article  CAS  PubMed  Google Scholar 

  59. Cai J, **ng L, Zhang W, Fu L, Zhang J (2022) Selection of potential probiotic yeasts from dry-cured Xuanwei ham and identification of yeast-derived antioxidant peptides. Antioxidants (Basel) 11(10):1970. https://doi.org/10.3390/antiox11101970

    Article  CAS  PubMed  Google Scholar 

  60. McFarland LV (2015) From yaks to yogurt: the history, development, and current use of probiotics. Clin Infect Dis 60(2):85–90. https://doi.org/10.1093/cid/civ054

    Article  CAS  Google Scholar 

  61. Suvarna S, Dsouza J, Ragavan ML, Das N (2018) Potential probiotic characterization and effect of encapsulation of probiotic yeast strains on survival in simulated gastrointestinal tract condition. Food Sci Biotechnol 27(3):745–753. https://doi.org/10.1007/s10068-018-0310-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ilango S, Antony U (2021) Probiotic microorganisms from non-dairy traditional fermented foods. Trends Food Sci Technol 118:617–638. https://doi.org/10.1016/j.tifs.2021.05.034

    Article  CAS  Google Scholar 

  63. Zullo BA, Ciafardini G (2019) Evaluation of physiological properties of yeast strains isolated from olive oil and their in vitro probiotic trait. Food Microbiol 78:179–187. https://doi.org/10.1016/j.fm.2018.10.016

    Article  CAS  PubMed  Google Scholar 

  64. Gut AM, Vasiljevic T, Yeager T, Donkor ON (2019) Characterization of yeasts isolated from traditional kefir grains for potential probiotic properties. J Funct Foods 58:56–66. https://doi.org/10.1016/j.jff.2019.04.046

    Article  CAS  Google Scholar 

  65. Menezes AGT, Ramos CL, Cenzi G, Melo DS, Dias DR, Schwan RF (2020) Probiotic potential, antioxidant activity, and phytase production of indigenous yeasts isolated from indigenous fermented foods. Probiotics Antimicrob Proteins 12(1):280–288. https://doi.org/10.1007/s12602-019-9518-z

    Article  CAS  PubMed  Google Scholar 

  66. Alvarez SCV, Alaniz MJL, Furlani MVM, Vasquez F, Agresti PM, Nally MC, Maturano YP (2023) Bioprospecting of the probiotic potential of yeasts isolated from a wine environment. Fungal Genet Biol 164:103767. https://doi.org/10.1016/j.fgb.2022.103767

    Article  CAS  Google Scholar 

  67. Fadda ME, Mossa V, Deplano M, Pisano MB, Cosentino S (2017) In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT 75:100–106. https://doi.org/10.1016/j.lwt.2016.08.020

    Article  CAS  Google Scholar 

  68. Ragavan ML, Das N (2017) Isolation and characterization of potential probiotic yeasts from different sources. Asian J Pharm Clin Res 10:451–455. https://doi.org/10.22159/ajpcr.2017.v10i4.17067

    Article  CAS  Google Scholar 

  69. Ilavenil S, Vijayakumar M, Kim DH, Valan Arasu M, Park HS, Ravikumar S, Choi KC (2016) Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian ryegrass. J Sci Food Agric 96:593–601. https://doi.org/10.1002/jsfa.7128

    Article  CAS  PubMed  Google Scholar 

  70. Sidira M, Kourkoutas Y, Kanellaki M, Charalampopoulos D (2015) In vitro study on the cell adhesion ability of immobilized Lactobacilli on natural supports. Food Res Int 76:532–539. https://doi.org/10.1016/j.foodres.2015.07.036

    Article  CAS  PubMed  Google Scholar 

  71. ANVISA (2007) Antimicrobianos – Bases teóricas e uso clínico. Retrieved from https://www.anvisa.gov.br/servicosaude/controle/rede_rm/cursos/rm_controle/opas_web/modulo1/antimicrobianos.htm. Acessed 16 Jul 2021

  72. Fernández-Pacheco P, Ramos MIM, Fernández-González M, Poveda CJM, Arévalo-Villena M (2021) Safety evaluation of yeasts with probiotic potential. Front Nutr 21(8):659328. https://doi.org/10.3389/fnut.2021.659328

    Article  CAS  Google Scholar 

  73. Perricone M, Bevilacqua A, Corbo MR, Sinigaglia M (2014) Technological characterization and probiotic traits of yeasts isolated from Altamura sourdough to select promising microorganisms as functional starter cultures for cereal-based products. Food Microbiol 38:26–35. https://doi.org/10.1016/j.fm.2013.08.006

    Article  CAS  PubMed  Google Scholar 

  74. Boris S, Suárez JE, Vázquez F, Barbés C (1998) Adherence of human vaginal Lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect Immun 66(5):1985–1989. https://doi.org/10.1128/IAI.66.5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Hojjati M, Behabahani BA, Falah F (2020) Aggregation, adherence, anti-adhesion and antagonistic activity properties relating to surface charge of probiotic Lactobacillus brevis gp104 against Staphylococcus aureus. Microb Pathogenes 147:104420. https://doi.org/10.1016/j.micpath.2020.104420

    Article  CAS  Google Scholar 

  76. Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ, Valko M (2017) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38:592–607. https://doi.org/10.1016/j.tips.2017.04.005

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the following Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brasil (CNPQ), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

  1. Institute of Science and Technology, Federal University of Jequitinhonha and Mucuri Valeys, Rodovia MGT 367 - km 583, no. 5000 – Alto da Jacuba - Diamantina, Minas Gerais, 39100-000, Brazil

    Nayara Martins Zille de Miranda & Cíntia Lacerda Ramos

  2. Department of Biology, Federal University of Lavras, Lavras, Minas Gerais, 37200-900, Brazil

    Angélica Cristina de Souza & Rosane Freitas Schwan

  3. Department of Nutrition, Federal University of Jequitinhonha and Mucuri Valeys, Diamantina, Minas Gerais, 39100-000, Brazil

    Paulo de Souza Costa Sobrinho

  4. Department of Food Science, Federal University of Lavras, Lavras, Minas Gerais, 37200-900, Brazil

    Disney Ribeiro Dias

Authors
  1. Nayara Martins Zille de Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angélica Cristina de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paulo de Souza Costa Sobrinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Disney Ribeiro Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rosane Freitas Schwan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cíntia Lacerda Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by NMZM, ACS, and PSCS. The first draft of the manuscript was written by NMZM, and all the authors commented on previous versions of the manuscript. The manuscript was revised by NMZM and CLR. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Cíntia Lacerda Ramos.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Elaine Cristina Pereira de Martinis

Publisher’s note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Miranda, N.M.Z., de Souza, A.C., de Souza Costa Sobrinho, P. et al. Novel yeasts with potential probiotic characteristics isolated from the endogenous ferment of artisanal Minas cheese. Braz J Microbiol 54, 1021–1033 (2023). https://doi.org/10.1007/s42770-023-01002-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-01002-5

Keywords

Search

Navigation