Skip to main content
Log in

Evaluation of the Potential Probiotic Yeast Characteristics with Anti-MRSA Abilities

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a disreputable pathogenic bacterium that has been proven to colonize the intestinal tract. The goal of this study is to find anti-MRSA probiotic yeast from food and evaluate its probiotic characteristics and safety. Finally, 15 strains were isolated from fruit peel with anti-MRSA ability. Using DNA sequence analysis, they were identified as the genus Hanseniaspora (7 strains) and Starmerella (8 strains). Starmerella bacillaris CC-PT4 (CGMCC No. 23573) that was isolated from the grape peel has good auto-aggregation ability and hydrophobicity, and can tolerate 0.3% bile, pH 2, simulated gastric fluid (SGF), and simulated intestinal fluid (SIF). Strikingly, Starmerella bacillaris CC-PT4, like commercial probiotic Saccharomyces boulardii CNCM I-745 (Florastor ®), can adapt to the temperature of the human body (37 ℃). After safety assessment, this strain is sensitive to amphotericin B and cannot produced β-hemolytic activities. Overall, this study provides a new candidate for probiotic yeast with anti-MRSA ability.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability Statement

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

References

  1. Hill C, Guarner 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 11:506–514

    Article  PubMed  Google Scholar 

  2. Yilmaz S, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E, Abdel-Latif HMR (2022) Probiotics, prebiotics, and synbiotics used to control vibriosis in fish: a review. Aquaculture 547:737514

  3. El-Saadony MT, Alagawany M, Patra AK, Kar I, Tiwari R, Dawood MAO, Dhama K, Abdel-Latif HMR (2021) The functionality of probiotics in aquaculture: an overview. Fish Shellfish Immunol 117:36–52

    Article  PubMed  Google Scholar 

  4. Abdel-Latif HMR, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E, Yilmaz S (2022) Shrimp vibriosis and possible control measures using probiotics, postbiotics, prebiotics, and synbiotics: a review. Aquaculture 551:737951

  5. Galdeano CM, Cazorla SI, Dumit JML, Vélez E, Perdigón G (2019) Beneficial effects of probiotic consumption on the immune system. Ann Nutr Metab 74:115–124

    Article  CAS  Google Scholar 

  6. Miller LE, Lehtoranta L, Lehtinen MJ (2019) Short-term probiotic supplementation enhances cellular immune function in healthy elderly: systematic review and meta-analysis of controlled studies. Nutr Res 64:1–8

    Article  CAS  PubMed  Google Scholar 

  7. Azad M, Kalam A, Sarker M, Li T, Yin J (2018) Probiotic species in the modulation of gut microbiota: an overview. Biomed Res Int 2018. https://doi.org/10.1155/2018/9478630

  8. Vemuri R, Shinde T, Gundamaraju R, Gondalia S, Karpe A, Beale D, Martoni C, Eri R (2018) Lactobacillus acidophilus dds-1 modulates the gut microbiota and improves metabolic profiles in aging mice. Nutrients 10:1255

    Article  PubMed Central  CAS  Google Scholar 

  9. Darani KK, Zoghi A, Jazayeri S, da Cruz AG (2020) Decontamination of aflatoxins with a focus on Aflatoxin B-1 by probiotic bacteria and yeasts: a review. J Microbiol Biotechnol Food Sci 10:424–435

    Article  CAS  Google Scholar 

  10. Poloni VL, Bainotti MB, Vergara LD, Escobar F, Montenegro M, Cavaglieri L (2021) Influence of technological procedures on viability, probiotic and anti-mycotoxin properties of Saccharomyces boulardii RC009, and biological safety studies. Curr Res Food Sci 4:132–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mekonnen SA, Merenstein D, Fraser CM, Marco ML (2020) Molecular mechanisms of probiotic prevention of antibiotic-associated diarrhea. Curr Opin Biotechnol 61:226–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lai H-H, Chiu C-H, Kong M-S, Chang C-J, Chen C-C (2019) Probiotic Lactobacillus casei : effective for managing childhood diarrhea by altering gut microbiota and attenuating fecal inflammatory markers. Nutrients 11:1150

    Article  CAS  PubMed Central  Google Scholar 

  13. Pinto-Sanchez M I, Hall G B, Ghajar K, Nardelli A, Bolino C, Lau JT, Martin F-P, Cominetti O, Welsh C, Rieder A (2017) Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 153:448–459, e448

  14. Quan L-H, Zhang C, Dong M, Jiang J, Xu H, Yan C, Liu X, Zhou H, Zhang H, Chen L (2019) Myristoleic acid produced by enterococci reduces obesity through brown adipose tissue activation. Gut 69:1239–1247

    Article  PubMed  CAS  Google Scholar 

  15. Briand F, Sulpice T, Giammarinaro P, Roux X (2019) Saccharomyces boulardii CNCM I-745 changes lipidemic profile and gut microbiota in a hamster hypercholesterolemic model. Beneficial Microbes 10:555–567

    Article  CAS  PubMed  Google Scholar 

  16. Lo RS, Austin AS, Freeman JG (2014) Is there a role for probiotics in liver disease? Sci World J. https://doi.org/10.1155/2014/874768

    Article  Google Scholar 

  17. Kang M-S, Yeu J-E, Hong S-P (2019) Safety evaluation of oral care probiotics Weissella cibaria CMU and CMS1 by phenotypic and genotypic analysis. Int J Mol Sci 20:2693

    Article  CAS  PubMed Central  Google Scholar 

  18. McLoughlin R, Berthon BS, Rogers GB, Baines KJ, Leong LEX, Gibson PG, Williams EJ, Wood LG (2019) Soluble fibre supplementation with and without a probiotic in adults with asthma: a 7-day randomised, double blind, three way cross-over trial. EBioMedicine 46:473–485

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gagné JW, Wakshlag JJ, Simpson KW, Dowd SE, Latchman S, Brown DA, Brown K, Swanson KS, Fahey GC, Jr. (2013) Effects of a synbiotic on fecal quality, short-chain fatty acid concentrations, and the microbiome of healthy sled dogs. BMC Vet Res 9:246–246

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Carvalho FM, Teixeira-Santos R, Mergulhão FJM, Gomes LC (2020) The use of probiotics to fight biofilms in medical devices: a systematic review and Meta-Analysis. Microorganisms 9:27

    Article  PubMed Central  Google Scholar 

  21. Shi X, Zhang J, Mo L, Shi J, Qin M, Huang X (2019) Efficacy and safety of probiotics in eradicating Helicobacter pylori: a network meta-analysis. Medicine 98:e15180–e15180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Khalique A, Zeng D, Shoaib M, Wang H, Qing X, Rajput DS, Pan K, Ni X (2020) Probiotics mitigating subclinical necrotic enteritis (SNE) as potential alternatives to antibiotics in poultry. AMB Express 10:50–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jäger R, Purpura M, Farmer S, Cash HA, Keller D (2018) Probiotic Bacillus coagulans GBI-30, 6086 improves protein absorption and utilization. Probiotics Antimicrob Proteins 10:611–615

    Article  PubMed  CAS  Google Scholar 

  24. Tsutsumi S, Mochizuki M, Sakai K, Ieda A, Ohara R, Mitsui S, Ito A, Hirano T, Shimizu M, Kato M (2019) Ability of Saccharomyces cerevisiae MC87-46 to assimilate isomaltose and its effects on sake taste. Sci Rep 9:13908–13908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Menezes AGT, Ramos CL, Cenzi G, Melo DS, Dias DR, Schwan RF (2019) Probiotic Potential, Antioxidant Activity, and Phytase Production of Indigenous Yeasts Isolated from Indigenous Fermented Foods. Probiotics and Antimicrobial Proteins 12:280–288

    Article  CAS  Google Scholar 

  26. Al-zaidi RE, Al-Mozan HD, Alrikabi NJ (2020) Eukaryotic probiotic Saccharomyces boulardii application in clinical trails: a review. Int J Pharm Qual Assur 11:160–165

    Article  Google Scholar 

  27. Quarella S, Lovrovich P, Scalabrin S, Campedelli I, Backovic A, Gatto V, Cattonaro F, Turello A, Torriani S, Felis GE (2016) Draft genome sequence of the probiotic yeast Kluyveromyces marxianus B0399. Genome Announc 4:e00923-e1916

    Article  PubMed  PubMed Central  Google Scholar 

  28. Sambrani R, Abdolalizadeh J, Kohan L, Jafari B (2021) Recent advances in the application of probiotic yeasts, particularly Saccharomyces, as an adjuvant therapy in the management of cancer with focus on colorectal cancer. Mol Biol Rep 48:951–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ost KS, O’Meara TR, Stephens WZ, Chiaro T, Zhou H, Penman J, Bell R, Catanzaro JR, Song D, Singh S, Call DH, Hwang-Wong E, Hanson KE, Valentine JF, Christensen KA, O’Connell RM, Cormack B, Ibrahim AS, Palm NW, Noble SM, Round JL (2021) Adaptive immunity induces mutualism between commensal eukaryotes. Nature

  30. Hallen-Adams HE, Suhr MJ (2017) Fungi in the healthy human gastrointestinal tract. Virulence 8:352–358

    Article  CAS  PubMed  Google Scholar 

  31. Nataraj BH, Mallappa RH (2021) Antibiotic resistance crisis: an update on antagonistic interactions between probiotics and methicillin-resistant Staphylococcus aureus (MRSA). Curr Microbiol 78:2194–2211

    Article  CAS  PubMed  Google Scholar 

  32. Ren DY, Gong SJ, Shu JY, Zhu JW, Liu HY, Chen P (2018) Effects of mixed lactic acid bacteria on intestinal microbiota of mice infected with Staphylococcus aureus. BMC Microbiol 18

  33. Spinelli E, Requena T, Caruso M, Parisi A, Capozzi L, Difato L, Normanno G (2020) Fate of Methicillin-resistant Staphylococcus aureus (MRSA) under simulated acidic conditions of the human stomach. Food Sci Nutr 8:4739–4745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Piewngam P, Zheng Y, Nguyen TH, Dickey SW, Joo H-S, Villaruz AE, Glose KA, Fisher EL, Hunt RL, Li B (2018) Pathogen elimination by probiotic Bacillus via signalling interference. Nature 562:532–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Teo AY-L, Tan H-M (2005) Inhibition of Clostridium perfringens by a novel strain of Bacillus subtilis isolated from the gastrointestinal tracts of healthy chickens. Appl Environ Microbiol 71:4185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kim YJ, Yu HH, Song YJ, Park YJ, Lee N-K, Paik H-D (2021) Anti-biofilm effect of the cell-free supernatant of probiotic Saccharomyces cerevisiae against Listeria monocytogenes. Food Control 121:107667

  37. Lohith K, Anu-Appaiah KA (2018) Antagonistic effect of Saccharomyces cerevisiae (italic) KTP and Issatchenkia occidentalis ApC on hyphal development and adhesion of Candida albicans. Med Mycol 56:1023–1032

    CAS  PubMed  Google Scholar 

  38. Wang S, Zhang Z, Malakar PK, Pan Y, Zhao Y (2019) The fate of bacteria in human digestive fluids: A new perspective into the pathogenesis of Vibrio parahaemolyticus. Front Microbiol 10

  39. Xie JL, Singh-Babak SD, Cowen LE (2012) Minimum inhibitory concentration (MIC) assay for antifungal drugs. Bio-Protoc 2:e252

  40. Singh-Babak SD, Babak T, Diezmann S, Hill JA, Xie JL, Chen Y-L, Poutanen SM, Rennie RP, Heitman J, Cowen LE (2012) Global analysis of the evolution and mechanism of echinocandin resistance in Candida glabrata. PLoS Pathog 8:e1002718

  41. Borman AM, Muller J, Walsh-Quantick J, Szekely A, Patterson Z, Palmer MD, Fraser M, Johnson EM (2020) MIC distributions for amphotericin B, fluconazole, itraconazole, voriconazole, flucytosine and anidulafungin and 35 uncommon pathogenic yeast species from the UK determined using the CLSI broth microdilution method. J Antimicrob Chemother 75:1194–1205

    Article  CAS  PubMed  Google Scholar 

  42. 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-Food Sci Technol 75:100–106

    Article  CAS  Google Scholar 

  43. Core Team R (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project. Accessed 18 Sept 2020

  44. de Albuquerque TMR, Garcia EF, de Oliveira AA, Magnani M, Saarela M, de Souza EL (2018) In vitro characterization of Lactobacillus strains isolated from fruit processing by-products as potential probiotics. Probiotics Antimicrob Proteins 10:704–716

    Article  PubMed  CAS  Google Scholar 

  45. Rodrigues NPA, Garcia EF, de Souza EL (2021) Selection of lactic acid bacteria with promising probiotic aptitudes from fruit and ability to survive in different food matrices. Braz J Microbiol 52:2257–2269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ansari F, Alian Samakkhah S, Bahadori A, Jafari SM, Ziaee M, Khodayari MT, Pourjafar H (2021) Health-promoting properties of Saccharomyces cerevisiae (italic) var. boulardii as a probiotic; characteristics, isolation, and applications in dairy products. Crit Rev Food Sci Nutr 1–29

  47. Sakandar HA, Usman K, Imran M (2018) Isolation and characterization of gluten-degrading Enterococcus mundtii and Wickerhamomyces anomalus, potential probiotic strains from indigenously fermented sourdough (Khamir). Lwt-Food Sci Technol 91:271–277

    Article  CAS  Google Scholar 

  48. Fernández-Pacheco P, Rosa IZ, Arévalo-Villena M, Gomes E, Pérez AB (2021) Study of potential probiotic and biotechnological properties of non-Saccharomyces yeasts from fruit Brazilian ecosystems. Braz J Microbiol 52:2129–2144

    Article  PubMed  CAS  Google Scholar 

  49. Khatri I, Tomar R, Ganesan K, Prasad GS, Subramanian S (2017) Complete genome sequence and comparative genomics of the probiotic yeast Saccharomyces boulardii. Sci Rep 7:371. https://doi.org/10.1038/s41598-017-00414-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Pais P, Almeida V, Yilmaz M, Teixeira MC (2020) Saccharomyces boulardii: What Makes It Tick as Successful Probiotic? J Fungi 6:78. https://doi.org/10.3390/jof6020078

    Article  CAS  Google Scholar 

  51. Lemos Junior WJF, Binati RL, Felis GE, Slaghenaufi D, Ugliano M, Torriani S (2020) Volatile organic compounds from Starmerella bacillaris to control gray mold on apples and modulate cider aroma profile. Food Microbiol 89:103446. https://doi.org/10.1016/j.fm.2020.103446

    Article  CAS  PubMed  Google Scholar 

  52. Fernandez-Pacheco P, Garcia-Bejar B, Jimenez-del Castillo M, Carreno-Dominguez J, Briones Perez A, Arevalo-Villena M (2021) Potential probiotic and food protection role of wild yeasts isolated from pistachio fruits (Pistacia vera). J Sci Food Agric 101:2201–2209

    Article  CAS  PubMed  Google Scholar 

  53. de Melo PGV, de Oliveira CB, Magalhães Júnior AI, Thomaz-Soccol V, Soccol CR (2018) How to select a probiotic? A review and update of methods and criteria. Biotechnol Adv 36:2060–2076

    Article  Google Scholar 

  54. Tavares Menezes AG, 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 12:280–288

    Article  CAS  Google Scholar 

  55. Lara-Hidalgo CE, Dorantes-Alvarez L, Hernandez-Sanchez H, Santoyo-Tepole F, Martinez-Torres A, Villa-Tanaca L, Hernandez-Rodriguez C (2019) Isolation of yeasts from guajillo pepper (Capsicum annuum L.) fermentation and study of some probiotic characteristics. Probiotics Antimicrob Proteins 11:748–764

    Article  CAS  PubMed  Google Scholar 

  56. Rodriguez PF-P, Arévalo-Villena M, Rosa IZ, Perez AB (2018) Selection of potential non-Sacharomyces probiotic yeasts from food origin by a step-by-step approach. Food Res Int 112:143–151

    Article  CAS  Google Scholar 

  57. Zupančič Š, Škrlec K, Kocbek P, Kristl J, Berlec A (2019) Effects of electrospinning on the viability of ten species of lactic acid bacteria in poly(ethylene oxide) nanofibers. Pharmaceutics 11:483

    Article  PubMed Central  CAS  Google Scholar 

  58. 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

    Article  CAS  Google Scholar 

  59. Fietto JL, Araujo RS, Valadao FN, Fietto LG, Brandao RL, Neves MJ, Gomes FC, Nicoli JR, Castro IM (2004) Molecular and physiological comparisons between Saccharomyces cerevisiae (italic) and Saccharomyces boulardii. Can J Microbiol 50:615–621

    Article  CAS  PubMed  Google Scholar 

  60. Blanquet-Diot S, Denis S, Chalancon S, Chaira F, Cardot J-M, Alric M (2012) Use of artificial digestive systems to investigate the biopharmaceutical factors influencing the survival of probiotic yeast during gastrointestinal transit in humans. Pharm Res 29:1444–1453

    Article  CAS  PubMed  Google Scholar 

  61. Edwards-Ingram L, Gitsham P, Burton N, Warhurst G, Clarke I, Hoyle D, Oliver Stephen G, Stateva L (2007) Genotypic and physiological characterization of Saccharomyces boulardii, the probiotic strain of Saccharomyces cerevisiae. Appl Environ Microbiol 73:2458–2467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Imran M, Desmasures N, Coton M, Coton E, Le Fleche-Mateos A, Irlinger F, Delbes-Paus C, Stahl V, Montel MC, Vernoux JP (2019) Safety assessment of Gram-negative bacteria associated with traditional French cheeses. Food Microbiol 79:1–10

    Article  CAS  PubMed  Google Scholar 

  63. Filho-Lima JVM, Vieira EC, Nicoli JR (2000) Antagonistic effect of Lactobacillus acidophilus, Saccharomyces boulardii and Escherichia coli combinations against experimental infections with Shigella flexneri and Salmonella enteritidis subsp. Typhimurium in gnotobiotic mice. J Appl Microbiol 88:365–370

    Article  CAS  PubMed  Google Scholar 

  64. Pfaller MA, Diekema DJ (2012) Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol 50:2846–2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Casarotti SN, Carneiro BM, Todorov SD, Nero LA, Rahal P, Penna ALB (2017) In vitro assessment of safety and probiotic potential characteristics of Lactobacillus strains isolated from water buffalo mozzarella cheese. Ann Microbiol 67:289–301

    Article  CAS  Google Scholar 

  66. Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16:189–199

    Article  CAS  Google Scholar 

  67. Shirron N, Korem M, Shuster A, Leikin-Frenkel A, Rosenberg M (2008) Effect of alcohol on bacterial hemolysis. Curr Microbiol 57:318. https://doi.org/10.1007/s00284-008-9196-7

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by the National Natural Science Foundation of China (No. 31772082), and the 13th Five-Year Plan Science and Technology Project of the Education Department of Jilin Province (JJKH20201017KJ).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Na Guo.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, Y., Bai, X., Zhang, Y. et al. Evaluation of the Potential Probiotic Yeast Characteristics with Anti-MRSA Abilities. Probiotics & Antimicro. Prot. 14, 727–740 (2022). https://doi.org/10.1007/s12602-022-09942-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-022-09942-4

Keywords

Navigation