The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Probiotic Potential of Yeasts Isolated from Fermented Beverages: Assessment of Antagonistic Strategies Against Salmonella enterica Serovar Enteritidis
Abstract
Global concern about pathogenic resistance to antibiotics is prompting interest in probiotics as a strategy to prevent or inhibit infections. Fermented beverages are promising sources of probiotic yeasts. This study aimed to evaluate the antagonistic effects of Kluyveromyces marxianus, Wickerhamomyces anomalus, and Pichia manshurica strains from kefir and wine against Salmonella enterica serovar Enteritidis in intestinal epithelial cells. The ability of these yeasts to adhere to Caco-2/TC-7 cells was evaluated, as well as their influence on the ability of Salmonella to associate and invade these cells. The behavior of the pathogen was analyzed by (a) incubation of enterocytes with yeast before adding Salmonella, (b) co-incubation of Salmonella with yeast before contact with the enterocytes, and (c) incubation of Salmonella with yeast metabolites before contact with enterocytes. All yeast strains demonstrated adherence to Caco-2/TC-7 cells (33–100%) and effectively inhibited Salmonella invasion. Among the treatments, co-culture showed the greatest effect, reducing Salmonella association and invasion by more than 50%. Additionally, these yeasts modulated the epithelial immune response, significantly decreasing CCL20-driven luminescence by 60–81% (p < 0.0001). These results highlight the potential of yeasts from fermented beverages as probiotics to counteract Salmonella infections, offering a promising alternative in the fight against antibiotic resistance.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592
Gut inflammation provides a respiratory electron acceptor for Salmonella
Winter, S. E., Thiennimitr, P., Winter, M. G., Butler, B. P., Huseby, D. L., Crawford, R. W., Russell, J. M., Bevins, C. L., Adams, L. G., Tsolis, R. M., et al. (2010) · Nature · doi:10.1038/nature09415 · Cited by 1,290
Host-Derived Nitrate Boosts Growth of E. coli in the Inflamed Gut
Winter, S. E., Winter, M. G., Xavier, M. N., Thiennimitr, P., Poon, V., Keestra, A. M., Laughlin, R. C., Gomez, G., Wu, J., Lawhon, S. D., et al. (2013) · Science · doi:10.1126/science.1232467 · Cited by 1,019
Esteve-Zarzoso, B., Belloch, C., Uruburu, F., & Querol, A. (1999) · International Journal of Systematic and Evolutionary Microbiology · doi:10.1099/00207713-49-1-329 · Cited by 970
Kos, B., Šušković, J., Vuković, S., Šimpraga, M., Frece, J., & Matošić, S. (2003) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2003.01915.x · Cited by 880
Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota
Thiennimitr, P., Winter, S. E., Winter, M. G., Xavier, M. N., Tolstikov, V., Huseby, D. L., Sterzenbach, T., Tsolis, R. M., Roth, J. R., & Bäumler, A. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107857108 · Cited by 619
Flocculation, adhesion and biofilm formation in yeasts
Verstrepen, K. J., & Klis, F. M. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05072.x · Cited by 589
The role of microbiota in infectious disease
Stecher, B., & Hardt, W.-D. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2007.12.008 · Cited by 535
Tight Junction Proteins and Signaling Pathways in Cancer and Inflammation: A Functional Crosstalk
Bhat, A. A., Uppada, S., Achkar, I. W., Hashem, S., Yadav, S. K., Shanmugakonar, M., Al-Naemi, H. A., Haris, M., & Uddin, S. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01942 · Cited by 400
Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches
Papadimitriou, K., Zoumpopoulou, G., Foligné, B., Alexandraki, V., Kazou, M., Pot, B., & Tsakalidou, E. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00058 · Cited by 384
Chemical and microbiological characterisation of kefir grains
GARROTE, G. L., ABRAHAM, A. G., & DE ANTONI, G. L. (2001) · Journal of Dairy Research · doi:10.1017/s0022029901005210 · Cited by 332
Self-citationRoles for motility in bacterial–host interactions
Ottemann, K. M., & Miller, J. F. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.4281787.x · Cited by 323
Assessment of cell surface properties and adhesion potential of selected probiotic strains
Xu, H., Jeong, H. S., Lee, H. Y., & Ahn, J. (2009) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2009.02684.x · Cited by 267
The Integral Role of Tight Junction Proteins in the Repair of Injured Intestinal Epithelium
Slifer, Z. M., & Blikslager, A. T. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030972 · Cited by 251
Lopez, C. A., Winter, S., Rivera-Chávez, F., Byndloss, M. X., Poon, V., Nuccio, S., Tsolis, R. M., & Bäumler, A. J. (2012) · mBio · doi:10.1128/mbio.00143-12 · Cited by 242
Prabhurajeshwar, C., & Chandrakanth, R. K. (2017) · Biomedical Journal · doi:10.1016/j.bj.2017.06.008 · Cited by 223
Salmonella infection – prevention and treatment by antibiotics and probiotic yeasts: a review
Gut, A. M., Vasiljevic, T., Yeager, T. R., & Donkor, O. N. (2018) · Microbiology · doi:10.1099/mic.0.000709 · Cited by 220
Screening of Dairy Yeast Strains for Probiotic Applications
Kumura, H., Tanoue, Y., Tsukahara, M., Tanaka, T., & Shimazaki, K. (2004) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(04)73546-8 · Cited by 217
Yeasts from kefir grains: isolation, identification, and probiotic characterization
Diosma, G., Romanin, D., Rey-Burusco, M. F., Londero, A., & Garrote, G. L. (2013) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-013-1419-9 · Cited by 203
Self-citationRespiration of Microbiota-Derived 1,2-propanediol Drives Salmonella Expansion during Colitis
Faber, F., Thiennimitr, P., Spiga, L., Byndloss, M. X., Litvak, Y., Lawhon, S. D., Andrews‐Polymenis, H. L., Winter, S., & Bäumler, A. J. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006129 · Cited by 188
Probiotic and Potentially Probiotic Yeasts—Characteristics and Food Application
Staniszewski, A., & Kordowska‐Wiater, M. (2021) · Foods · doi:10.3390/foods10061306 · Cited by 186
Ayyash, M. M., Abdalla, A. K., Alkalbani, N. S., Baig, M. A., Turner, M. S., Liu, S., & Shah, N. P. (2021) · Journal of Dairy Science · doi:10.3168/jds.2021-20398 · Cited by 184
Salmonella Uses Energy Taxis to Benefit from Intestinal Inflammation
Rivera-Chávez, F., Winter, S., Lopez, C. A., Byndloss, M. X., Winter, M. G., Nuccio, S., Russell, J. M., Laughlin, R. C., Lawhon, S. D., Sterzenbach, T., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003267 · Cited by 179
Yeasts as probiotics: Mechanisms, outcomes, and future potential
Sen, S., & Mansell, T. J. (2020) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2020.103333 · Cited by 176
Nempont, C., Cayet, D., Rumbo, M., Bompard, C., Villeret, V., & Sirard, J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.3.2036 · Cited by 161
Maccaferri, S., Klinder, A., Brigidi, P., Cavina, P., & Costabile, A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.06385-11 · Cited by 158
Menezes, A. G. T., Ramos, C. L., Cenzi, G., Melo, D. D. S., Dias, D. R., & Schwan, R. F. (2019) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-019-9518-z · Cited by 139
Exploring biotechnological and functional characteristics of probiotic yeasts: A review
Shruthi, B., Deepa, N., Somashekaraiah, R., Adithi, G., Divyashree, S., & Sreenivasa, M. Y. (2022) · Biotechnology Reports · doi:10.1016/j.btre.2022.e00716 · Cited by 126
Wang, G., Song, Q., Huang, S., Wang, Y., Cai, S., Yu, H., Ding, X., Zeng, X., & Zhang, J. (2020) · Animals · doi:10.3390/ani10020345 · Cited by 124
Down-regulation of intestinal epithelial innate response by probiotic yeasts isolated from kefir
Romanin, D., Serradell, M. D. L. Á., Maciel, D. G., Lausada, N., Garrote, G. L., & Rumbo, M. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.04.014 · Cited by 120
Self-citationFadda, M. E., Mossa, V., Deplano, M., Pisano, M. B., & Cosentino, S. (2016) · LWT · doi:10.1016/j.lwt.2016.08.020 · Cited by 113
Adhesins of Yeasts: Protein Structure and Interactions
Willaert, R. (2018) · Journal of Fungi · doi:10.3390/jof4040119 · Cited by 111
Winter, S., Thiennimitr, P., Nuccio, S., Haneda, T., Winter, M. G., Wilson, R. P., Russell, J. M., Henry, T., Tran, Q. T., Lawhon, S. D., et al. (2009) · Infection and Immunity · doi:10.1128/iai.01341-08 · Cited by 106
Unique Probiotic Properties and Bioactive Metabolites of Saccharomyces boulardii
Fu, J., Liu, J., Wen, X., Zhang, G., Ji, C., Qiao, Z., An, Z., Zheng, J., & Li, L. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09953-1 · Cited by 99
Lymphotoxin β receptor signaling induces the chemokine CCL20 in intestinal epithelium
Rumbo, M., Sierro, F., Debard, N., Kraehenbühl, J.-P., & Finke, D. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.018 · Cited by 93
Inflammasomes of the intestinal epithelium
Sellin, M. E., Maslowski, K. M., Maloy, K. J., & Hardt, W. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.06.002 · Cited by 92
Diversity, Ecology, and Prevalence of Antimicrobials in Nature
Mullis, M. M., Rambo, I. M., Baker, B. J., & Reese, B. K. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02518 · Cited by 91
Invited review: Milk kefir microbiota—Direct and indirect antimicrobial effects
González‐Orozco, B. D., García‐Cano, I., Jiménez‐Flores, R., & Alvárez, V. B. (2022) · Journal of Dairy Science · doi:10.3168/jds.2021-21382 · Cited by 91
Singh, R. P., Shadan, A., & Ma, Y. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09992-8 · Cited by 87
Inhibition of in vitro cell adherence of Clostridium difficile by Saccharomyces boulardii
Tasteyre, A., Barc, M. C., Karjalainen, T. K., Bourlioux, P., & Collignon, A. (2002) · Microbial Pathogenesis · doi:10.1006/mpat.2002.0495 · Cited by 86
Screening for the potential probiotic yeast strains from raw milk to assimilate cholesterol
Chen, L., Ma, Y., Maubois, J., He, S., Chen, L., & Li, H. (2010) · Dairy Science and Technology · doi:10.1051/dst/2010001 · Cited by 83
A Salmonella Virulence Factor Activates the NOD1/NOD2 Signaling Pathway
Keestra, A. M., Winter, M. G., Klein-Douwel, D., Byndloss, M. X., Winter, S., Kim, A., Tsolis, R. M., & Bäumler, A. J. (2011) · mBio · doi:10.1128/mbio.00266-11 · Cited by 83
Tuo, Y., Song, X., Song, Y., Liu, W., Tang, Y., Gao, Y., Jiang, S., Qian, F., & Mu, G. (2018) · Journal of Dairy Science · doi:10.3168/jds.2017-13654 · Cited by 82
Probiotic properties of yeasts isolated from Brazilian fermented table olives
Simões, L. A., de Souza, A. C., Ferreira, I. V. A., Melo, D. D. S., Lopes, L. A. A., Magnani, M., Schwan, R. F., & Dias, D. R. (2021) · Journal of Applied Microbiology · doi:10.1111/jam.15065 · Cited by 81
Alkalbani, N. S., Osaili, T. M. I., Al‐Nabulsi, A. A., Olaimat, A. N., Liu, S., Shah, N. P., Apostolopoulos, V., & Ayyash, M. M. (2022) · Journal of Fungi · doi:10.3390/jof8040365 · Cited by 80
Bonatsou, S., Karamouza, M., Ζουμποπούλου, Γ., Mavrogonatou, E., Kletsas, D., Papadimitriou, K., Tsakalidou, E., Nychas, G. E., & Panagou, E. Ζ. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.02.018 · Cited by 79
The role of lactate on the immunomodulatory properties of the nonbacterial fraction of kefir
Iraporda, C., Romanin, D., Rumbo, M., Garrote, G. L., & Abraham, A. G. (2014) · Food Research International · doi:10.1016/j.foodres.2014.03.003 · Cited by 68
Self-citationRomanin, D., Llopis, S., Genovés, S., Martorell, P., Ramón, D., Garrote, G. L., & Rumbo, M. (2015) · Beneficial Microbes · doi:10.3920/bm2015.0066 · Cited by 67
Self-citationSu, X., Zhang, J., Wang, H., Xu, J., He, J., Liu, L., Zhang, T., Chen, R.-Y., & Kang, J. (2017) · Molecules · doi:10.3390/molecules22020312 · Cited by 64
Marine bacteria and fungi as promising source for new antibiotics
Wiese, J., & Imhoff, J. F. (2018) · Drug Development Research · doi:10.1002/ddr.21482 · Cited by 64
Role of Yeasts in Healthy and Impaired Gut Microbiota: The Gut Mycome
Ianiro, G., Bruno, G., Lopetuso, L. R., Beghella, F., Laterza, L., D’Aversa, F., Gigante, G. E., Cammarota, G., & Gasbarrini, A. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113196660723 · Cited by 62
Mechanisms ofSalmonellapathogenesis in animal models
Palmer, A. D., & Slauch, J. M. (2017) · Human and Ecological Risk Assessment An International Journal · doi:10.1080/10807039.2017.1353903 · Cited by 56
Zavala, L., Golowczyc, M. A., Hoorde, K. V., Medrano, M., Huys, G. R. B., Vandamme, P. A. R., & Abraham, A. G. (2016) · Beneficial Microbes · doi:10.3920/bm2015.0196 · Cited by 45
Ramos, J. M. D. O., dos Santos, C. A., Santana, D. G., Santos, D. D. A., Alves, P. B., & Thomazzi, S. M. (2013) · Revista Brasileira de Farmacognosia · doi:10.1590/s0102-695x2013005000045 · Cited by 42
González‐Orozco, B. D., Kosmerl, E., Jiménez‐Flores, R., & Alvárez, V. B. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1236634 · Cited by 40
Bonnet, V., Dupont, H., Glorion, S., Aupée, M., Kipnis, É., Gérard, J., Hanouz, J., & Fischer, M.-O. (2019) · Journal of Hospital Infection · doi:10.1016/j.jhin.2019.01.011 · Cited by 35
Bioprospecting of the probiotic potential of yeasts isolated from a wine environment
Vergara, S. C., Alaniz, M. J. L., Mestre, M. V., Vázquez, F., Mancha-Agresti, P. D. C., Nally, M. C., & Maturano, Y. P. (2022) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2022.103767 · Cited by 35
Self-citationMotey, G. A., Johansen, P. G., Owusu‐Kwarteng, J., Ofori, L. A., Obiri‐Danso, K., Siegumfeldt, H., Larsen, N., & Jespersen, L. (2020) · Yeast · doi:10.1002/yea.3513 · Cited by 26
Pendón, M. D., Madeira, J. V., Romanin, D., Rumbo, M., Gombert, A. K., & Garrote, G. L. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11278-y · Cited by 26
Self-citationInflammasome Signaling and Bacterial Infections
Backert, S. (2016) · Current topics in microbiology and immunology · doi:10.1007/978-3-319-41171-2 · Cited by 20
Non- saccharomyces yeast probiotics: revealing relevance and potential
Vergara, S. C., Alaniz, M. J. L., Mestre, M. V., Vázquez, F., Nally, M. C., & Maturano, Y. P. (2023) · FEMS Yeast Research · doi:10.1093/femsyr/foad041 · Cited by 18
Self-citationRole of Probiotics in Health and Diseases
Collado, M. C., Laparra, J. M., Frías, R., Lee, Y. K., Salminen, S., Lim, A., & Tan, H. (2008) · Wiley eBooks · doi:10.1002/9780470432624.ch4 · Cited by 15
Blumenberg, M., Shaaban, M. I., & Elgaml, A. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.82960 · Cited by 14
Walsham, A. D. S. (2016) · UEA Digital Repository (University of East Anglia) · Cited by 1
Research works printed but not linked: 1
- Kurtzman, C., Fell, J.W., and Boekhout, T. (2011). The Yeasts: A Taxonomic Study, Elsevier.
Cited by
Understanding the Functionality of Probiotics on the Edge of Artificial Intelligence (AI) Era
Asar, R., Erenler, S., Devecioglu, D., Ispirli, H., Karbancioglu-Guler, F., Ozturk, H. I., & Dertli, E. (2025) · Fermentation · doi:10.3390/fermentation11050259 · Cited by 37
Metadata
- Authors
- Alvarez, S. C. V., Pendón, M. D., Bengoa, A. A., Leiva Alaniz, M. J., Maturano, Y. P., & Garrote, G. L.
- Venue
- Journal of Fungi
- Publisher
- MDPI AG
- Published
- 2024-12-17
- Volume
- 10
- Issue
- 12
- Pages
- 878
- ISSN
- 2309-608X
- Cited by
- 9
- References
- 64
- Language
- en
- Funders
- Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) (PICT 2020-03973, PICT 2019-02866, PICTA 2021-0060, FITBA A09–2022)
- Ministry of Production, Science, and Technology from Provincia de Buenos Aires (PICT 2020-03973, PICT 2019-02866, PICTA 2021-0060, FITBA A09–2022)
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.