Probiotic Yeasts: A Developing Reality?
Abstract
:1. Introduction
2. Beyond Bacteria: Unveiling the Potential of Yeasts
3. Saccharomyces boulardii: A Pioneering Probiotic Yeast
4. Probiotic Yeast Effects
4.1. Interactions with Gut Microbiota
4.2. Immune Modulation Capabilities
4.3. Overall Impact on Gut Health
5. Yeast “New” Strains as Probiotics: Myth or Reality?
Properties and Limitations of Probiotic Yeast Strains
6. Fermentation Process: Boosting Nutrition and Flavor
7. Commercial Formulas with Yeast Probiotics
- (a)
- (b)
- Focus on established strains. Commercially available probiotic formulas often include well-studied strains like Lactobacillus and Bifidobacterium with a longer track record of safety and efficacy in humans;
- (c)
- Formulation challenges. Yeast probiotics like bacteria probiotics might require specific processing or formulation techniques to ensure viability and delivery of its potential benefits. Some factors should be considered during processing and storage, such as temperature, pH, and various environmental aspects. These factors can damage the cells and reduce their viability during processing and storage [4,113].
8. Synergy with Bacteria: A Powerful Duo
- Enhanced Microbial Growth. Certain probiotic yeasts, like S. boulardii, may produce specific compounds such as prebiotics. These prebiotics act as food for beneficial bacteria strains like Bifidobacteria and lactobacilli, stimulating their growth and colonization in the gut [4];
- Improved Barrier Function. Numerous investigations demonstrated a correlation between S. boulardii and a decreased level of Firmicutes and Proteobacteria in the gut microbiota and a greater proportion of Bacteroidetes. Additionally, by increasing the synthesis of short-chain fatty acids and inducing proinflammatory immune responses, this yeast can reduce inflammation [30]. Furthermore, S. boulardii has been shown by Kunyeit et al. to dramatically decrease the adherence of the multidrug-resistant species C. auris to the abiotic surface, suggesting that this would be a useful strategy for managing this yeast [116];
- Immune Modulation. The combined effects of probiotic yeasts and bacteria could have a positive impact on the immune system. Studies suggest that this synergy might help regulate the inflammatory response and potentially reduce the risk of allergies or inflammatory bowel disease [12,30,43];D. hansenii is compatible with lactic acid bacteria (e.g., Lactobacillus spp. and Lactococcus spp.), hence it could be a component of starter cultures for lactic acid products such as cheese and yogurt. D. hansenii can enhance flavor development and improve the texture of the final product. It is capable of thriving in low pH environments, making it suitable for acidic fermentation processes. Certain strains of D. hansenii exhibit thermostability, which enhances its applicability in various thermal processing conditions. D. hansenii demonstrates high resistance to various stress factors, including osmotic stress, oxidative stress, and high salinity. In addition, it exhibits a high tolerance to various chemical agents, including preservatives and antifungal compounds, which underscores its robustness in industrial applications [112,117,118,119]. Furthermore, when cocultured with Bacillus clausii, D. hansenii has the ability to suppress the growth of this bacteria [120]. But the inhibition is related to different strains because it occurs at the strain level [120];
- S. cerevisiae is compatible with acetic acid bacteria (e.g., Acetobacter spp.). It is used in the production of kombucha, where S. cerevisiae ferments the sugars to produce ethanol, which is then converted to acetic acid by acetic acid bacteria, contributing to the final flavor profile [121,122,123];
- C. milleri is compatible with lactic acid bacteria (e.g., Lactobacillus sanfranciscensis). C. milleri and L. sanfranciscensis work together to create the characteristic flavor and texture of sourdough bread through fermentation and acid production [126].
9. The Future
10. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Luo, G.; Li, B.; Yang, C.; Wang, Y.; Bian, X.; Li, W.; Liu, F.; Huo, G. Major Traditional Probiotics: Comparative Genomic Analyses and Roles in Gut Microbiome of Eight Cohorts. Front. Microbiol. 2019, 10, 712. [Google Scholar] [CrossRef] [PubMed]
- Gomaa, E.Z. Human gut microbiota/microbiome in health and diseases: A review. Antonie Van. Leeuwenhoek 2020, 113, 2019–2040. [Google Scholar] [CrossRef] [PubMed]
- Singh, D.; Singh, A.; Kumar, S. Probiotics: Friend or foe to the human immune system. Bull. Natl. Res. Cent. 2023, 47, 126. [Google Scholar] [CrossRef]
- Staniszewski, A.; Kordowska-Wiater, M. Probiotic and Potentially Probiotic Yeasts-Characteristics and Food Application. Foods 2021, 10, 1306. [Google Scholar] [CrossRef] [PubMed]
- Afzaal, M.; Saeed, F.; Shah, Y.A.; Hussain, M.; Rabail, R.; Socol, C.T.; Hassoun, A.; Pateiro, M.; Lorenzo, J.M.; Rusu, A.V.; et al. Human gut microbiota in health and disease: Unveiling the relationship. Front. Microbiol. 2022, 13, 999001. [Google Scholar] [CrossRef] [PubMed]
- Pais, P.; Almeida, V.; Yılmaz, M.; Teixeira, M.C. Saccharomyces boulardii: What Makes It Tick as Successful Probiotic? J. Fungi 2020, 6, 78. [Google Scholar] [CrossRef]
- Gopalan, S.; Ganapathy, S.; Mitra, M.N.; Kumar, J.D.; Veligandla, K.C.; Rathod, R.; Kotak, B.P. Unique Properties of Yeast Probiotic Saccharomyces boulardii CNCM I-745: A Narrative Review. Cureus 2023, 15, e46314. [Google Scholar] [CrossRef] [PubMed]
- Abid, R.; Waseem, H.; Ali, J.; Ghazanfar, S.; Muhammad Ali, G.; Elasbali, A.M.; Alharethi, S.H. Probiotic Yeast Saccharomyces: Back to Nature to Improve Human Health. J. Fungi 2022, 8, 444. [Google Scholar] [CrossRef] [PubMed]
- Shingel, K.M.; Maguen, E.; Lin, H.H.; Blaut, D.; Chang, F. Microbiome Engineering Using Probiotic Yeast: Saccharomyces boulardii and the Secreted Human Lysozyme Lead to Changes in the Gut Microbiome and Metabolome of Mice. Microbiol. Spectr. 2018, 6, e00031-18. [Google Scholar]
- Sun, S.; Xu, X.; Liang, L.; Wang, X.; Bai, X.; Zhu, L.; He, Q.; Liang, H.; Xin, X.; Wang, L.; et al. Lactic Acid-Producing Probiotic Saccharomyces cerevisiae Attenuates Ulcerative Colitis via Suppressing Macrophage Pyroptosis and Modulating Gut Microbiota. Front. Immunol. 2021, 12, 777665. [Google Scholar] [CrossRef]
- Sen, S.; Mansell, T.J. Yeasts as probiotics: Mechanisms, outcomes, and future potential. Fungal Genet. Biol. 2020, 137, 103333. [Google Scholar] [CrossRef] [PubMed]
- Huang, Q.; Zhu, Y.; Yu, J.; Fang, L.; Li, Y.; Wang, M.; Liu, J.; Yan, P.; Xia, J.; Liu, G.; et al. Effects of sulfated β-glucan from Saccharomyces cerevisiae on growth performance, antioxidant ability, nonspecific immunity, and intestinal flora of the red swamp crayfish (Procambarus clarkii). Fish Shellfish Immunol. 2022, 127, 891–900. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Wang, J.; Wu, C. Modulation of Gut Microbiota and Immune System by Probiotics, Pre-biotics, and Post-biotics. Front. Nutr. 2022, 8, 634897. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Li, Y.; Yang, Z.; Li, C.; Liang, H.; Wu, Z.; Pu, W. Yeast Probiotics Shape the Gut Microbiome and Improve the Health of Early-Weaned Piglets. Front. Microbiol. 2018, 9, 2011. [Google Scholar] [CrossRef]
- Pérez-Giraldo, C.; Fresno, S.; Moreno-Haguenauer, J. Killer yeasts: An expanding horizon in yeast antifungal defense. Trends Microbiol. 2018, 26, 709–721. [Google Scholar]
- Nascimento, B.L.; Delabeneta, M.F.; Rosseto, L.R.B.; Junges, D.S.B.; Paris, A.P.; Persel, C.; Gandra, R.F. Yeast Mycocins: A great potential for application in health. FEMS Yeast Res. 2020, 20, foaa016. [Google Scholar] [CrossRef]
- Junges, D.S.B.; Delabeneta, M.F.; Rosseto, L.R.B.; Nascimento, B.L.; Paris, A.P.; Persel, C.; Loth, E.A.; Simão, R.C.G.; Menolli, R.A.; Paula, C.R.; et al. Antibiotic Activity of Wickerhamomyces anomalus Mycocins on Multidrug-Resistant Acinetobacter baumannii. Microb. Ecol. 2020, 80, 278–285. [Google Scholar] [CrossRef]
- Nascimento, B.L.; Martelli, E.C.; da Silva, J.C.; Delabeneta, M.F.; Rosseto, L.R.B.; Junges, D.S.B.; Paris, A.P.; Persel, C.; Paula, C.R.; Simão, R.C.G.; et al. Inhibition of Klebsiella pneumonia carbapenemases by mycocins produced by Wickerhamomyces anomalus. Arch. Microbiol. 2022, 204, 702. [Google Scholar] [CrossRef]
- Calazans, G.F.; da Silva, J.C.; Delabeneta, M.F.; Paris, A.P.; Yassuda Filho, P.; Auler, M.E.; Menolli, R.A.; Paula, C.R.; Simão, R.C.G.; Gandra, R.F. Antimicrobial activity of Wickerhamomyces anomalus mycocins against strains of Staphylococcus aureus isolated from meats. Food Sci. Technol. 2020, 41, 388–394. [Google Scholar] [CrossRef]
- Rosseto, L.R.B.; Martelli, E.C.; da Silva, J.C.; Nascimento, B.L.; Junges, D.S.B.; Delabeneta, M.F.; Paris, A.P.; Auler, M.E.; Menolli, R.A.; Simão, R.C.G.; et al. Susceptibility of Candida albicans Strains Isolated from Vaginal Secretion in Front of the Mycocins of Wickerhamomyces anomalus. Probiotics Antimicrob. Proteins 2022, 14, 595–601. [Google Scholar] [CrossRef]
- Li, B.; Zhang, H.; Shi, L.; Li, R.; Luo, Y.; Deng, Y.; Li, S.; Li, R.; Liu, Z. Saccharomyces boulardii alleviates DSS-induced intestinal barrier dysfunction and inflammation in humanized mice. Food Funct. 2022, 13, 102–112. [Google Scholar] [CrossRef]
- Bastos, T.S.; Souza, C.M.M.; Legendre, H.; Richard, N.; Pilla, R.; Suchodolski, J.S.; de Oliveira, S.G.; Lesaux, A.A.; Félix, A.P. Effect of Yeast Saccharomyces cerevisiae as a Probiotic on Diet Digestibility, Fermentative Metabolites, and Composition and Functional Potential of the Fecal Microbiota of Dogs Submitted to an Abrupt Dietary Change. Microorganisms 2023, 11, 506. [Google Scholar] [CrossRef]
- Kamiya, S.; Ohga, S.; Yonezawa, M.; Lida, T.; Kodama, Y.; Saito, T.; Ando, A. Saccharomyces boulardii modulates intestinal immunity in vitro and in vivo via toll-like receptor 4 signaling. FEMS Immunol. Med. Microbiol. 2016, 76, 189–197. [Google Scholar]
- Smith, I.M.; Christensen, J.E.; Arneborg, N.; Jespersen, L. Yeast modulation of human dendritic cell cytokine secretion: An in vitro study. PLoS ONE 2014, 9, e96595. [Google Scholar] [CrossRef]
- Smith, I.M.; Baker, A.; Christensen, J.E.; Boekhout, T.; Frøkiær, H.; Arneborg, N.; Jespersen, L. Kluyveromyces marxianus and Saccharomyces boulardii Induce Distinct Levels of Dendritic Cell Cytokine Secretion and Significantly Different T Cell Responses In Vitro. PLoS ONE 2016, 11, e0167410. [Google Scholar] [CrossRef] [PubMed]
- Okada, Y.; Tsuzuki, Y.; Sugihara, N.; Nishii, S.; Shibuya, N.; Mizoguchi, A.; Itoh, S.; Tanemoto, R.; Inaba, K.; Hanawa, Y.; et al. Novel probiotic yeast from Miso promotes regulatory dendritic cell IL-10 production and attenuates DSS-induced colitis in mice. J. Gastroenterol. 2021, 56, 829–842. [Google Scholar] [CrossRef] [PubMed]
- Miranda, V.C.; Santos, S.S.; Assis, H.C.; Faria, A.M.C.; Quintanilha, M.F.; Morão, R.P.; Nicoli, J.R.; Cara, D.C.; Martins, F.S. Effect of Saccharomyces cerevisiae UFMG A-905 in a murine model of food allergy. Benef. Microbes 2020, 11, 255–268. [Google Scholar] [CrossRef]
- Fonseca, V.M.B.; Milani, T.M.S.; Prado, R.; Bonato, V.L.D.; Ramos, S.G.; Martins, F.S.; Vianna, E.O.; Borges, M.C. Oral administration of Saccharomyces cerevisiae UFMG A-905 prevents allergic asthma in mice. Respirology 2017, 22, 905–912. [Google Scholar] [CrossRef]
- Sharma, G.; Im, S.H. Probiotics as a Potential Immunomodulating Pharmabiotics in Allergic Diseases: Current Status and Future Prospects. Allergy Asthma Immunol. Res. 2018, 10, 575–590. [Google Scholar] [CrossRef]
- Azad, M.A.K.; Sarker, M.; Li, T.; Yin, J. Probiotic Species in the Modulation of Gut Microbiota: An Overview. Biomed. Res. Int. 2018, 2018, 9478630. [Google Scholar] [CrossRef]
- Gou, H.Z.; Zhang, Y.L.; Ren, L.F.; Li, Z.J.; Zhang, L. How do intestinal probiotics restore the intestinal barrier? Front. Microbiol. 2022, 13, 929346. [Google Scholar] [CrossRef] [PubMed]
- Filidou, E.; Kolios, G. Probiotics in Intestinal Mucosal Healing: A New Therapy or an Old Friend? Pharmaceuticals 2021, 14, 1181. [Google Scholar] [CrossRef]
- D‘Souza, A.L.; Rajkumar, C.; Cooke, J.; Bulpitt, C.J. Probiotics in prevention of antibiotic associated diarrhoea: Meta-analysis. BMJ 2002, 324, 1361. [Google Scholar] [CrossRef]
- Villarruel, G.; Rubio, D.M.; Lopez, F.; Cintioni, J.; Gurevech, R.; Romero, G.; Vandenplas, Y. Saccharomyces boulardii in acute childhood diarrhoea: A randomized, placebo-controlled study. Acta Paediatr. 2007, 96, 538–541. [Google Scholar] [CrossRef] [PubMed]
- Kelesidis, T.; Pothoulakis, C. Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therap Adv. Gastroenterol. 2012, 5, 111–125. [Google Scholar] [CrossRef]
- McFarland, L.V. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J. Gastroenterol. 2010, 16, 2202–2222. [Google Scholar] [CrossRef]
- Mourey, F.; Decherf, A.; Jeanne, J.F.; Clément-Ziza, M.; Grisoni, M.L.; Machuron, F.; Legrain-Raspaud, S.; Bourreille, A.; Desreumaux, P. Saccharomyces cerevisiae I-3856 in irritable bowel syndrome with predominant constipation. World J. Gastroenterol. 2022, 28, 2509–2522. [Google Scholar] [CrossRef]
- Cayzeele-Decherf, A.; Pélerin, F.; Leuillet, S.; Douillard, B.; Housez, B.; Cazaubiel, M.; Jacobson, G.K.; Jüsten, P.; Desreumaux, P. Saccharomyces cerevisiae CNCM I-3856 in irritable bowel syndrome: An individual subject meta-analysis. World J. Gastroenterol. 2017, 23, 336–344. [Google Scholar] [CrossRef] [PubMed]
- Moslehi-Jenabian, S.; Pedersen, L.L.; Jespersen, L. Beneficial effects of probiotic and food borne yeasts on human health. Nutrients 2010, 2, 449–473. [Google Scholar] [CrossRef]
- Markowiak, P.; Śliżewska, K. Effects of Probiotics, Prebiotics, and Synbiotics on Human Health. Nutrients 2017, 9, 1021. [Google Scholar] [CrossRef]
- Shang, Q.; Sun, Z.; Liu, X.; Tian, H.; Shen, J.; Jing, H. Saccharomyces boulardii modulates gut microbiota in weaned piglets. Front. Microbiol. 2018, 9, 1403. [Google Scholar] [CrossRef]
- den Besten, G.; van Eunen, K.; Groen, A.K.; Venema, K.; Reijngoud, D.J.; Bakker, B.M. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013, 54, 2325–2340. [Google Scholar] [CrossRef] [PubMed]
- Staniszewski, A.; Kordowska-Wiater, M. Probiotic Yeasts and How to Find Them-Polish Wines of Spontaneous Fermentation as Source for Potentially Probiotic Yeasts. Foods 2023, 12, 3392. [Google Scholar] [CrossRef] [PubMed]
- Astuti, R.I.; Prastya, M.E.; Wulan, R.; Anam, K.; Meryandini, A. Current trends and future perspective of probiotic yeasts research in Indonesia. FEMS Yeast Res. 2023, 23, foad013. [Google Scholar] [CrossRef] [PubMed]
- Homayouni-Rad, A.A.A.; Oroojzadeh, P.; Pourjafar, H. Kluyveromyces marxianus as a Probiotic Yeast: A Mini-review. Curr. Nutr. Food Sci. 2020, 16, 1163–1169. [Google Scholar] [CrossRef]
- Kurtzman, C.; Fell, J.W.; Boekhout, T. (Eds.) The Yeasts: A Taxonomic Study, 5th ed.; Elsevier: Amsterdam, The Netherlands, 2011. [Google Scholar]
- Peromingo, B.; Andrade, M.J.; Delgado, J.; Sánchez-Montero, L.; Núñez, F. Biocontrol of aflatoxigenic Aspergillus parasiticus by native Debaryomyces hansenii in dry-cured meat products. Food Microbiol. 2019, 82, 269–276. [Google Scholar] [CrossRef] [PubMed]
- Ochangco, H.S.; Gamero, A.; Smith, I.M.; Christensen, J.E.; Jespersen, L.; Arneborg, N. In vitro investigation of Debaryomyces hansenii strains for potential probiotic properties. World J. Microbiol. Biotechnol. 2016, 32, 141. [Google Scholar] [CrossRef] [PubMed]
- Karim, A.; Gerliani, N.; Aïder, M. Kluyveromyces marxianus: An emerging yeast cell factory for applications in food and biotechnology. Int. J. Food Microbiol. 2020, 333, 108818. [Google Scholar] [CrossRef] [PubMed]
- Cui, Y.; Guo, P.; Ning, M.; Yue, Y.; Yuan, Y.; Yue, T. Kluyveromyces marxianus supplementation ameliorates alcohol-induced liver injury associated with the modulation of gut microbiota in mice. Food Funct. 2023, 14, 9920–9935. [Google Scholar] [CrossRef]
- Nag, D.; Goel, A.; Padwad, Y.; Singh, D. In Vitro Characterisation Revealed Himalayan Dairy Kluyveromyces marxianus PCH397 as Potential Probiotic with Therapeutic Properties. Probiotics Antimicrob. Proteins 2023, 15, 761–773. [Google Scholar] [CrossRef]
- Reyes-Becerril, M.; Alamillo, E.; Angulo, C. Probiotic and Immunomodulatory Activity of Marine Yeast Yarrowia lipolytica Strains and Response Against Vibrio parahaemolyticus in Fish. Probiotics Antimicrob. Proteins 2021, 13, 1292–1305. [Google Scholar] [CrossRef] [PubMed]
- Miller, K.K.; Alper, H.S. Yarrowia lipolytica: More than an oleaginous workhorse. Appl. Microbiol. Biotechnol. 2019, 103, 9251–9262. [Google Scholar] [CrossRef] [PubMed]
- Guardiola, F.A.; Esteban, M.Á.; Angulo, C. Yarrowia lipolytica, health benefits for animals. Appl. Microbiol. Biotechnol. 2021, 105, 7577–7592. [Google Scholar] [CrossRef] [PubMed]
- Shruthi, B.; Deepa, N.; Somashekaraiah, R.; Adithi, G.; Divyashree, S.; Sreenivasa, M.Y. Exploring biotechnological and functional characteristics of probiotic yeasts: A review. Biotechnol. Rep. 2022, 34, e00716. [Google Scholar] [CrossRef] [PubMed]
- Licona-Jain, A.; Campa-Córdova, Á.; Luna-González, A.; Racotta, I.S.; Tello, M.; Angulo, C. Dietary supplementation of marine yeast Yarrowia lipolytica modulates immune response in Litopenaeus vannamei. Fish Shellfish Immunol. 2020, 105, 469–476. [Google Scholar] [CrossRef] [PubMed]
- Madzak, C.; Poiret, S.; Salomé Desnoulez, S.; Foligné, B.; Lafont, F.; Daniel, C. Study of the persistence and dynamics of recombinant mCherry-producing Yarrowia lipolytica strains in the mouse intestine using fluorescence imaging. Microb. Biotechnol. 2023, 16, 618–631. [Google Scholar] [CrossRef] [PubMed]
- Czech, A.; Smolczyk, A.; Ognik, K.; Wlazło, Ł.; Nowakowicz-Dębek, B.; Kiesz, M. Effect of dietary supplementation with Yarrowia lipolytica or Saccharomyces cerevisiae yeast and probiotic additives on haematological parameters and the gut microbiota in piglets. Res. Vet. Sci. 2018, 119, 221–227. [Google Scholar] [CrossRef] [PubMed]
- Fernández-Pacheco, P.; Ramos Monge, I.M.; Fernández-González, M.; Poveda Colado, J.M.; Arévalo-Villena, M. Safety Evaluation of Yeasts With Probiotic Potential. Front. Nutr. 2021, 8, 659328. [Google Scholar] [CrossRef] [PubMed]
- Ganapathiwar, S.; Bhukya, B. In vitro assessment for the probiotic potential of Pichia kudriavzevii. Bioinformation 2023, 19, 441–444. [Google Scholar] [CrossRef]
- Greppi, A.; Saubade, F.; Botta, C.; Humblot, C.; Guyot, J.P.; Cocolin, L. Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiol. 2017, 62, 169–177. [Google Scholar] [CrossRef]
- Alakeji, T.P.; Oloke, J. Association of probiotic potential of strains of Pichia kudriavzevii isolated from “ogi” with the number of open reading frame (ORF) in the nucleotide sequences. Afr. J. Biotechnol. 2020, 19, 148–155. [Google Scholar] [CrossRef]
- Agarbati, A.; Canonico, L.; Marini, E.; Zannini, E.; Ciani, M.; Comitini, F. Potential Probiotic Yeasts Sourced from Natural Environmental and Spontaneous Processed Foods. Foods 2020, 9, 287. [Google Scholar] [CrossRef] [PubMed]
- Diguță, C.F.; Mihai, C.; Toma, R.C.; Cîmpeanu, C.; Matei, F. In Vitro Assessment of Yeasts Strains with Probiotic Attributes for Aquaculture Use. Foods 2022, 12, 124. [Google Scholar] [CrossRef] [PubMed]
- Tyumentseva, M.; Tyumentsev, A.; Akimkin, V. CRISPR/Cas9 Landscape: Current State and Future Perspectives. Int. J. Mol. Sci. 2023, 24, 16077. [Google Scholar] [CrossRef]
- Bouyx, C.; Schiavone, M.; François, J.M. FLO11, a Developmental Gene Conferring Impressive Adaptive Plasticity to the Yeast Saccharomyces cerevisiae. Pathogens 2021, 10, 1509. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.J.; Kong, I.I.; Zhang, G.C.; Jayakody, L.N.; Kim, H.; Xia, P.F.; Kwak, S.; Sung, B.H.; Sohn, J.H.; Walukiewicz, H.E.; et al. Metabolic Engineering of Probiotic Saccharomyces boulardii. Appl. Environ. Microbiol. 2016, 82, 2280–2287. [Google Scholar] [CrossRef]
- Hudson, L.E.; Fasken, M.B.; McDermott, C.D.; McBride, S.M.; Kuiper, E.G.; Guiliano, D.B.; Corbett, A.H.; Lamb, T.J. Functional Heterologous Protein Expression by Genetically Engineered Probiotic Yeast Saccharomyces boulardii. PLoS ONE 2014, 9, e112660. [Google Scholar] [CrossRef]
- Kim, J.; Cheong, Y.E.; Yu, S.; Jin, Y.S.; Kim, K.H. Strain engineering and metabolic flux analysis of a probiotic yeast Saccharomyces boulardii for metabolizing L-fucose, a mammalian mucin component. Microb. Cell Fact. 2022, 21, 204. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Wu, J.; Jin, Y.; Huang, K.; Zhang, Y.; Liang, Z. Both Saccharomyces boulardii and Its Postbiotics Alleviate Dextran Sulfate Sodium-Induced Colitis in Mice, Association with Modulating Inflammation and Intestinal Microbiota. Nutrients 2023, 15, 1484. [Google Scholar] [CrossRef]
- Li, L.; Pan, Y.; Zhang, S.; Yang, T.; Li, Z.; Wang, B.; Sun, H.; Zhang, M.; Li, X. Quorum sensing: Cell-to-cell communication in Saccharomyces cerevisiae. Front. Microbiol. 2023, 14, 1250151. [Google Scholar] [CrossRef]
- Czerucka, D.; Piche, T.; Rampal, P. Review article: Yeast as probiot ics—Saccharomyces boulardii. Aliment. Pharmacol. Ther. 2007, 26, 767–778. [Google Scholar] [CrossRef] [PubMed]
- Lane, M.M.; Morrissey, J.P. Kluyveromyces marxianus: A yeast emerging from its sister’s shadow. Fungal Biol. Rev. 2010, 24, 17–26. [Google Scholar] [CrossRef]
- Fonseca, G.G.; Heinzle, E.; Wittmann, C.; Gombert, A.K. The yeast Kluyveromyces marxianus and its biotechnological potential. Appl. Microbiol. Biotechnol. 2008, 79, 339–354. [Google Scholar] [CrossRef] [PubMed]
- Ledesma-Amaro, R.; Nicaud, J.M. Metabolic Engineering for Expanding the Substrate Range of Yarrowia lipolytica. Trends Biotechnol. 2016, 34, 798–809. [Google Scholar] [CrossRef] [PubMed]
- Groenewald, M.; Boekhout, T.; Neuvéglise, C.; Gaillardin, C.; van Dijck, P.W.; Wyss, M. Yarrowia lipolytica: Safety assessment of an oleaginous yeast with a great industrial potential. Crit. Rev. Microbiol. 2014, 40, 187–206. [Google Scholar] [CrossRef] [PubMed]
- Madzak, C. Yarrowia lipolytica strains and their biotechnological applications: How natural biodiversity and metabolic engineering could contribute to cell factories improvement. J. Fungi 2021, 7, 548. [Google Scholar] [CrossRef] [PubMed]
- Madzak, C. Yarrowia lipolytica: Recent achievements in heterologous protein expression and pathway engineering. Appl. Microbiol. Biotechnol. 2015, 99, 4559–4577. [Google Scholar] [CrossRef] [PubMed]
- Chu, Y.; Li, M.; Jin, J.; Dong, X.; Xu, K.; Jin, L.; Qiao, Y.; Ji, H. Advances in the Application of the Non-Conventional Yeast Pichia kudriavzevii in Food and Biotechnology Industries. J. Fungi 2023, 9, 170. [Google Scholar] [CrossRef] [PubMed]
- Pongcharoen, P. The ability of Pichia kudriavzevii to tolerate multiple stresses makes it promising for developing improved bioethanol production processes. Lett. Appl. Microbiol. 2022, 75, 36–44. [Google Scholar] [CrossRef]
- Corbu, V.; Csutak, O. Biodiversity studies on Pichia kudriavzevii from romanian spontaneous fermented products. AgroLife Sci. J. 2020, 9, 104–113. [Google Scholar]
- Li, Y.; Mo, X.; Xiong, J.; Huang, K.; Zheng, M.; Jiang, Q.; Su, G.; Ou, Q.; Pan, H.; Jiang, C. Deciphering the probiotic properties and safety assessment of a novel multi-stress-tolerant aromatic yeast Pichia kudriavzevii HJ2 from marine mangroves. Food Biosci. 2023, 56, 103248. [Google Scholar] [CrossRef]
- Ulya, D.; Astuti, R.I.; Meryandini, A. The ethanol production activity of indigenous thermotolerant yeast Pichia kudriavzevii 1P4. Microbiol. Ind. 2020, 14, 1. [Google Scholar] [CrossRef]
- Benito, S. The impact of Torulaspora delbrueckii yeast in winemaking. Appl. Microbiol. Biotechnol. 2018, 102, 3081–3094. [Google Scholar] [CrossRef] [PubMed]
- Helmy, E.A.; Abdel-Fadeel, R.H.; Yosri, M.; Hassan, E. Does Torulaspora delbrueckii has some probiotic capabilities? In vitro and in vivo assessment. Nutrire 2024, 49, 15. [Google Scholar] [CrossRef]
- Abu-Mejdad, N.M.J.A.; Al-Saadoon, A.H.; Al-Badran, A.I.; Minati, M.H. Optimum conditions of killer toxins produced by Torulaspora delbrueckii and Wickerhamomyces anomalus and their action as antifungal agents. Bull. Natl. Res. Cent. 2020, 44, 148. [Google Scholar] [CrossRef]
- Fernandes, T.; Silva-Sousa, F.; Pereira, F.; Rito, T.; Soares, P.; Franco-Duarte, R.; Sousa, M.J. Biotechnological Importance of Torulaspora delbrueckii: From the Obscurity to the Spotlight. J. Fungi 2021, 7, 712. [Google Scholar] [CrossRef] [PubMed]
- Ogawa, H.; Fujimura, M.; Tofuku, Y. Allergic Bronchopulmonary Fungal Disease Caused by Saccharomyces cerevisiae. J. Asthma 2004, 41, 223–228. [Google Scholar] [CrossRef]
- Nittner-Marszalska, M.; Wójcicka-Kustrzeba, I.; Bogacka, E.; Patkowski, J.; Dobek, R. Skin prick test response to enzyme enolase of the baker’s yeast (Saccharomyces cerevisiae) in diagnosis of respiratory allergy. Med. Sci. Monit. 2001, 7, 121–124. [Google Scholar] [PubMed]
- Ellis, A.K.; Day, J.H. Allergenic microorganisms and hypersensitivity. In Microorganisms in Home and Indoor Work Environments: Diversity, Health Impacts, Investigation and Control, 2nd ed.; Flannigan, B., Samson, R.A., Miller, J.D., Eds.; CRC Press: Boca Raton, FL, USA, 2011; pp. 147–182. [Google Scholar]
- Yamamoto, Y.; Osanai, S.; Fujiuchi, S.; Yamazaki, K.; Nakano, H.; Ohsaki, Y.; Kikuchi, K. Extrinsic allergic alveolitis induced by the yeast Debaryomyces hansenii. Eur. Respir. J. 2002, 20, 1351–1353. [Google Scholar] [CrossRef]
- EFSA Panel on Food Contact Materials, Enzymes and Processing Aids (CEP); Lambré, C.; Barat Baviera, J.M.; Bolognesi, C.; Cocconcelli, P.S.; Crebelli, R.; Gott, D.M.; Grob, K.; Lampi, E.; Mengelers, M.; et al. Safety evaluation of the food enzyme β-galactosidase from the genetically modified Kluyveromyces lactis strain KLA. EFSA J. 2022, 20, e07575. [Google Scholar] [CrossRef]
- Tran, K.D.; Le-Thi, L.; Vo, H.H.; Dinh-Thi, T.V.; Nguyen-Thi, T.; Phan, N.H.; Nguyen, K.U. Probiotic Properties and Safety Evaluation in the Invertebrate Model Host Galleria mellonella of the Pichia kudriavzevii YGM091 Strain Isolated from Fermented Goat Milk. Probiotics Antimicrob. Proteins 2023, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Fu, W.; Xue, W.; Liu, C.; Tian, Y.; Zhang, K.; Zhu, Z. Screening of Lactic Acid Bacteria and Yeasts from Sourdough as Starter Cultures for Reduced Allergenicity Wheat Products. Foods 2020, 9, 751. [Google Scholar] [CrossRef] [PubMed]
- Hernandez-Montiel, L.G.; Droby, S.; Preciado-Rangel, P.; Rivas-García, T.; González-Estrada, R.R.; Gutiérrez-Martínez, P.; Ávila-Quezada, G.D. A Sustainable Alternative for Postharvest Disease Management and Phytopathogens Biocontrol in Fruit: Antagonistic Yeasts. Plants 2021, 10, 2641. [Google Scholar] [CrossRef] [PubMed]
- Freimoser, F.M.; Rueda-Mejia, M.P.; Tilocca, B.; Migheli, Q. Biocontrol yeasts: Mechanisms and applications. World J. Microbiol. Biotechnol. 2019, 35, 154. [Google Scholar] [CrossRef] [PubMed]
- Sui, Y.; Wisniewski, M.; Droby, S.; Piombo, E.; Wu, X.; Yue, J. Genome Sequence, Assembly, and Characterization of the Antagonistic Yeast Candida oleophila Used as a Biocontrol Agent Against Post-harvest Diseases. Front. Microbiol. 2020, 11, 295. [Google Scholar] [CrossRef] [PubMed]
- Tejero, P.; Martín, A.; Rodríguez, A.; Galván, A.I.; Ruiz-Moyano, S.; Hernández, A. In Vitro Biological Control of Aspergillus flavus by Hanseniaspora opuntiae L479 and Hanseniaspora uvarum L793, Producers of Antifungal Volatile Organic Compounds. Toxins 2021, 13, 663. [Google Scholar] [CrossRef] [PubMed]
- Contarino, R.; Brighina, S.; Fallico, B.; Cirvilleri, G.; Parafati, L.; Restuccia, C. Volatile organic compounds (VOCs) produced by biocontrol yeasts. Food Microbiol. 2019, 82, 70–74. [Google Scholar] [CrossRef] [PubMed]
- Parafati, L.; Vitale, A.; Polizzi, G.; Restuccia, C.; Cirvilleri, G. Understanding the mechanism of biological control of postharvest phytopathogenic moulds promoted by food isolated yeasts. Acta Hortic. 2016, 1144, 93–100. [Google Scholar] [CrossRef]
- Aksu, Z.; Eren, A.T. Production of carotenoids by the isolated yeast of Rhodotorula glutinis. Biochem. Eng. J. 2007, 35, 107–113. [Google Scholar] [CrossRef]
- Kheireddine, A.; Palmieri, D.; Vitullo, D.; Barberio, A.; Zouaoui, M.; De Curtis, F.; Sadfi-Zouaoui, N.; Lima, G. Characterization of new yeast isolates collected from different fruits in Tunisia and biocontrol activity against Penicillium expansum on apples. J. Plant Pathol. 2021, 103, 1169–1184. [Google Scholar] [CrossRef]
- Fredlund, E.; Druvefors, U.; Boysen, M.E.; Lingsten, K.J.; Schnürer, J. Physiological characteristics of the biocontrol yeast Pichia anomala J121. FEMS Yeast Res. 2002, 2, 395–402. [Google Scholar] [CrossRef] [PubMed]
- Tayel, A.A.; El-Tras, W.F.; Moussa, S.H.; El-Agamy, M.A. Antifungal action of Pichia anomala against aflatoxigenic Aspergillus flavus and its application as a feed supplement. J. Sci. Food Agric. 2013, 93, 3259–3263. [Google Scholar] [CrossRef] [PubMed]
- Demirgul, F.; Simsek, O.; Sagdic, O. Amino acid, mineral, vitamin B contents and bioactivities of extracts of yeasts isolated from sourdough. Food Biosci. 2022, 50, 102040. [Google Scholar] [CrossRef]
- Ansari, F.; Alian Samakkhah, S.; Bahadori, A.; Jafari, S.M.; Ziaee, M.; Khodayari, M.T.; Pourjafar, H. Health-promoting properties of Saccharomyces cerevisiae var. boulardii as a probiotic; characteristics, isolation, and applications in dairy products. Crit. Rev. Food Sci. Nutr. 2023, 63, 457–485. [Google Scholar] [CrossRef] [PubMed]
- Alkalbani, N.S.; Osaili, T.M.; Al-Nabulsi, A.A.; Olaimat, A.N.; Liu, S.Q.; Shah, N.P.; Apostolopoulos, V.; Ayyash, M.M. Assessment of Yeasts as Potential Probiotics: A Review of Gastrointestinal Tract Conditions and Investigation Methods. J. Fungi 2022, 8, 365. [Google Scholar] [CrossRef] [PubMed]
- Dahiya, D.; Nigam, P.S. Biotherapy Using Probiotics as Therapeutic Agents to Restore the Gut Microbiota to Relieve Gastrointestinal Tract Inflammation, IBD, IBS and Prevent Induction of Cancer. Int. J. Mol. Sci. 2023, 24, 5748. [Google Scholar] [CrossRef] [PubMed]
- Hatoum, R.; Labrie, S.; Fliss, I. Antimicrobial and probiotic properties of yeasts: From fundamental to novel applications. Front. Microbiol. 2012, 3, 421. [Google Scholar] [CrossRef]
- Merenstein, D.; Pot, B.; Leyer, G.; Ouwehand, A.C.; Preidis, G.A.; Elkins, C.A.; Hill, C.; Lewis, Z.T.; Shane, A.L.; Zmora, N.; et al. Emerging issues in probiotic safety: 2023 perspectives. Gut Microbes 2023, 15, 2185034. [Google Scholar] [CrossRef]
- Long, S.; He, T.; Kim, S.W.; Shang, Q.; Kiros, T.; Mahfuz, S.U.; Wang, C.; Piao, X. Live Yeast or Live Yeast Combined with Zinc Oxide Enhanced Growth Performance, Antioxidative Capacity, Immunoglobulins and Gut Health in Nursery Pigs. Animals 2021, 11, 1626. [Google Scholar] [CrossRef]
- Angulo, M.; Reyes-Becerril, M.; Medina-Córdova, N.; Tovar-Ramírez, D.; Angulo, C. Probiotic and nutritional effects of Debaryomyces hansenii on animals. Appl. Microbiol. Biotechnol. 2020, 104, 7689–7699. [Google Scholar] [CrossRef]
- Sadeghi, A.; Ebrahimi, M.; Shahryari, S.; Kharazmi, M.S.; Jafari, S.M. Food applications of probiotic yeasts; focusing on their techno-functional, postbiotic and protective capabilities. Trends Food Sci. Technol. 2022, 128, 278–295. [Google Scholar] [CrossRef]
- González-Orozco, B.D.; Kosmerl, E.; Jiménez-Flores, R.; Alvarez, V.B. Enhanced probiotic potential of Lactobacillus kefiranofaciens OSU-BDGOA1 through co-culture with Kluyveromyces marxianus bdgo-ym6. Front. Microbiol. 2023, 14, 1236634. [Google Scholar] [CrossRef] [PubMed]
- de Jesus Cassimiro, D.M.; Batista, N.N.; Fonseca, H.C.; Naves, J.A.O.; Dias, D.R.; Schwan, R.F. Coinoculation of lactic acid bacteria and yeasts increases the quality of wet fermented Arabica coffee. Int. J. Food Microbiol. 2022, 369, 109627. [Google Scholar] [CrossRef]
- Kunyeit, L.; Kurrey, N.K.; Anu-Appaiah, K.A.; Rao, R.P. Probiotic Yeasts Inhibit Virulence of Non-albicans Candida Species. mBio 2019, 10, e02307-19. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, A.D.; Viljoen, B.C. Yeasts as adjunct starters in matured Cheddar cheese. Int. J. Food Microbiol. 2003, 86, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Gori, K.; Sørensen, L.M.; Petersen, M.A.; Jespersen, L.; Arneborg, N. Debaryomyces hansenii strains differ in their production of flavor compounds in a cheese-surface model. MicrobiologyOpen 2012, 1, 161–168. [Google Scholar] [CrossRef] [PubMed]
- Breuer, U.; Harms, H. Debaryomyces hansenii—An extremophilic yeast with biotechnological potential. Yeast 2006, 23, 415–437. [Google Scholar] [CrossRef] [PubMed]
- Gabrić, A. Interactions among Yeasts and Probiotic Bacteria and Inhibition of the Growth of Bacillus clausii by Debaryomyces hansenii. Ph.D. Thesis, University of Zagreb, Faculty of Food Technology and Biotechnology, Department of Chemistry and Biochemistry, Laboratory for Biochemistry, Zagreb, Croatia, 2023. Available online: https://repozitorij.unizg.hr/islandora/object/pbf:4771 (accessed on 9 July 2024).
- Wang, B.; Rutherfurd-Markwick, K.; Zhang, X.X.; Mutukumira, A.N. Isolation and characterisation of dominant acetic acid bacteria and yeast isolated from Kombucha samples at point of sale in New Zealand. Curr. Res. Food Sci. 2022, 5, 835–844. [Google Scholar] [CrossRef] [PubMed]
- Teoh, A.L.; Heard, G.; Cox, J. Yeast ecology of Kombucha fermentation. Int. J. Food Microbiol. 2004, 95, 119–126. [Google Scholar] [CrossRef]
- Marsh, A.J.; O‘Sullivan, O.; Hill, C.; Ross, R.P.; Cotter, P.D. Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol. 2014, 38, 171–178. [Google Scholar] [CrossRef]
- Thierry, A.; Maillard, M.; Yvon, M. Conversion of l-Leucine to Isovaleric Acid by Propionibacterium freudenreichii TL 34 and ITGP23. Appl. Environ. Microbiol. 2002, 68, 608–615. [Google Scholar] [CrossRef] [PubMed]
- Gänzle, M.G. Lactic metabolism revisited: Metabolism of lactic acid bacteria in food fermentations and food spoilage. Curr. Opin. Sci. 2015, 2, 106–117. [Google Scholar] [CrossRef]
- Gänzle, M.G.; Ehmann, M.; Hammes, W.P. Modeling of Growth of Lactobacillus sanfranciscensis and Candida milleri in Response to Process Parameters of Sourdough Fermentation. Appl. Environ. Microbiol. 1998, 64, 2616–2623. [Google Scholar] [CrossRef]
- Pihurov, M.; Păcularu-Burada, B.; Cotârleţ, M.; Vasile, M.A.; Bahrim, G.E. Novel Insights for Metabiotics Production by Using Artisanal Probiotic Cultures. Microorganisms 2021, 9, 2184. [Google Scholar] [CrossRef] [PubMed]
- Tamang, J.P.; Lama, S. Probiotic properties of yeasts in traditional fermented foods and beverages. J. Appl. Microbiol. 2022, 132, 3533–3542. [Google Scholar] [CrossRef] [PubMed]
- Tamang, J.P.; Lama, S. Diversity of yeasts in Indian fermented foods and alcoholic beverages. FEMS Yeast Res. 2023, 23, foad011. [Google Scholar] [CrossRef] [PubMed]
- Fernández-Pacheco, P.; Ramos Monge, I.M.; Poveda, J.M.; Díaz-Maroto, M.C.; Arévalo-Villena, M. Use of probiotic yeasts with biocontrol activity for fermentation of ewe’s milk. J. Sci. Food Agric. 2023, 103, 4107–4118. [Google Scholar] [CrossRef] [PubMed]
- Tullio, V. Yeast Genomics and Its Applications in Biotechnological Processes: What Is Our Present and Near Future? J. Fungi 2022, 8, 752. [Google Scholar] [CrossRef]
- Murali, S.K.; Mansell, T.J. Next generation probiotics: Engineering live biotherapeutics. Biotechnol. Adv. 2024, 72, 108336. [Google Scholar] [CrossRef]
Yeast Strain | Probiotic/Biocontrol Properties | Limitations | Genetic Engineering Tools and Genome Editing Technologies | Examples of Genetic Engineering Applications | Refs. |
---|---|---|---|---|---|
Saccharomyces boulardii | Antimicrobial activity Immunomodulation Gut health improvement (diarrhea treatment) | Not suitable for immunocompromised individuals (risk of fungemia) Variable individual responses | CRISPR/Cas9, TALENs, ZFNs, Homologous recombination | Engineering for enhanced stress tolerance, adhesion to intestinal cells and metabolic efficiency | [35,36,72] |
Debaryomyces hansenii | Antimicrobial activity (organic acids, VOCs, killer toxins). Tolerance to salinity Enzymatic activity (lipases, proteases) | Limited safety studies Regulatory approval not widely obtained | CRISPR/Cas9, Homologous recombination, Plasmid-based expression | Engineering for enhanced lipase production for industrial applications | [15,16,45,46,47] |
Kluyveromyces marxianus | Lactose utilization (beneficial for lactose intolerance) Enzymatic production (β-galactosidase) | Limited human studies Regulatory hurdles | CRISPR/Cas9, Homologous recombination, Plasmid-based expression | Engineering for improved lactose utilization and enhanced production of bioethanol | [73,74] |
Yarrowia lipolytica | Lipid metabolism Stress resistance | Potential opportunistic pathogen Requires comprehensive safety and efficacy studies | CRISPR/Cas9, TALENs, Homologous recombination, Plasmid-based expression | Engineering for the production of higher levels of essential vitamins and for enhanced lipid accumulation for biofuel production | [75,76,77,78] |
Pichia kudriavzevii | Stress resistance (acid and bile tolerance) Antimicrobial compounds | Pathogenicity concerns Regulatory and safety concerns | CRISPR/Cas9, Homologous recombination | Engineering for improved tolerance to environmental stresses and production of valuable metabolites | [79,80,81,82,83] |
Torulaspora delbrueckii | Acid and bile tolerance Pathogen inhibition (bioactive compounds) | Limited research and clinical trials Strain-specific effects | CRISPR/Cas9, Homologous recombination | Engineering for improved fermentation efficiency and pathogen resistance | [63,84,85,86,87] |
Yeast Strain | Probiotic/Biocontrol Properties | Limitations | Genetic Engineering Tools and Genome Editing Technologies | Examples of Genetic Engineering Applications | Refs. |
---|---|---|---|---|---|
Candida oleophila | Produces antifungal compounds Effective against post-harvest pathogens like Penicillium and Botrytis | Potential pathogenicity in humans Requires stringent regulatory approval | CRISPR/Cas9, Homologous recombination | Engineering for enhanced antifungal compound production and stress tolerance | [95,96,97] |
Hanseniaspora uvarum | Inhibits a wide range of plant pathogens Produces volatile organic compounds | Can ferment at low temperatures Limited data on safety for human consumption | CRISPR/Cas9, Homologous recombination | Engineering for improved pathogen inhibition and enhanced fermentation characteristics | [98,99] |
Metschnikowia pulcherrima | Produces pulcherrimin an iron-binding pigment Effective against various plant pathogens | Limited understanding of long-term effects Needs more studies on application in food systems | CRISPR/Cas9, Homologous recombination | Engineering for increased pulcherrimin production and improved biocontrol efficacy | [100] |
Rhodotorula glutinis | Produces carotenoids and enzymes with antimicrobial properties Effective in biocontrol of post-harvest diseases | Opportunistic pathogen in immunocompromised individuals Regulatory and safety concerns | CRISPR/Cas9, Homologous recombination, Plasmid-based expression | Engineering for enhanced carotenoid production and stress tolerance | [101,102] |
Pichia anomala | Broad-spectrum antifungal activity Effective in controlling spoilage molds and mycotoxin producers | Potential to produce harmful by-products Limited commercial application data | CRISPR/Cas9, Homologous recombination | Engineering for improved antifungal activity and reduced production of harmful by-products. Modifying strains for safer and more efficient use in commercial biocontrol products | [103,104] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tullio, V. Probiotic Yeasts: A Developing Reality? J. Fungi 2024, 10, 489. https://doi.org/10.3390/jof10070489
Tullio V. Probiotic Yeasts: A Developing Reality? Journal of Fungi. 2024; 10(7):489. https://doi.org/10.3390/jof10070489
Chicago/Turabian StyleTullio, Vivian. 2024. "Probiotic Yeasts: A Developing Reality?" Journal of Fungi 10, no. 7: 489. https://doi.org/10.3390/jof10070489