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Unique Probiotic Properties and Bioactive Metabolites of Saccharomyces boulardii

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Abstract

Saccharomyces boulardii (S. boulardii) is a probiotic and is widely used to improve the nutritional and functional value of food. This study aimed to compare the probiotic properties of S. boulardii and Saccharomyces cerevisiae. A series of in vitro probiotic experiments was performed, including simulated gastrointestinal digestion, bile salt tolerance, hydrophobicity, self-aggregation, and antioxidant and antibacterial properties. Self-aggregation and hydrophobic properties of S. boulardii were relatively poor, but they showed high tolerance, antioxidant properties, and broad antibacterial properties. In addition, non-targeted metabolomics was used to comprehensively analyze the active metabolites of S. boulardii and the metabolic differences between S. boulardii and S. cerevisiae were compared. Saccharomyces boulardii produced many bioactive metabolites, which generally showed antioxidant, antibacterial, antitumor, anti-inflammatory, and other properties. In contrast to S. cerevisiae, S. boulardii produced phenyllactic acid and 2-hydroxyisocaproic acid. There were also significant differences in their metabolic pathways. These results may be of great significance in the medical and food industries and provide a basis for understanding the metabolism of S. boulardii. It also shows that metabolomics is an effective and novel method for screening microbial functional metabolites and identifying functional differences between similar microorganisms.

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References

  1. Canani RB, Cucchiara S, Cuomo R, Pace F, Papale F (2011) Saccharomyces boulardii: a summary of the evidence for gastroenterology clinical practice in adults and children. Eur Rev Med Pharmaco 15(7):809–822. PMID: 21780551

    Google Scholar 

  2. Rodrigues ACP, Nardi RM, Bambirra EA, Vieira EC, Nicoli JR (1996) Effect of Saccharomyces boulardii against experimental oral infection with Salmonella typhimurium and Shigella flexneri in conventional and gnotobiotic mice. J Appl Bacteriol 81:251–256. https://doi.org/10.1111/j.1365-2672.1996.tb04325.x

    Article  CAS  PubMed  Google Scholar 

  3. Pothoulakis C, Kelly CP, Joshi MA, Gao N, O’Keane CJ, Castagliuolo I et al (1993) Saccharomyces boulardii inhibits Clostridium difficile toxin A binding and enterotoxicity in rat ileum. Gastroenterology 104:1108–1115. https://doi.org/10.1016/0016-5085(93)90280-P

    Article  CAS  PubMed  Google Scholar 

  4. Buts JP, Dekeyser N, Stilmant C, Delem E, Smets F, Sokal E (2006) Saccharomyces boulardii produces in rat small intestine a novel protein phosphatase that inhibits Escherichia coli endotoxin by dephosphorylation. Pediatr Res 60:24–29. https://doi.org/10.1203/01.pdr.0000220322.31940.29

    Article  CAS  PubMed  Google Scholar 

  5. Buts JP, De Keyser N, Marandi S, Hermans D, Sokal EM, Chae YH et al (1999) Saccharomyces boulardii upgrades cellular adaptation after proximal enterectomy in rats. Gut 45:89–96. https://doi.org/10.1136/gut.45.1.89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lazo-Vélez MA, Serna-Saldívar SO, Rosales-Medina MF, Tinoco-Alvear M, an Briones-García, M. (2018) Application of Saccharomyces cerevisiae var. boulardii in food processing: A review. J Appl Microbiol 125:943–951. https://doi.org/10.1111/jam.14037

    Article  PubMed  Google Scholar 

  7. Rekha CR, Vijayalakshmi G (2010) Bioconversion of isoflavone glycosides to aglycones, mineral bioavailability and vitamin B complex in fermented soymilk by probiotic bacteria and yeast. J Appl Microbiol 109:1198–1208. https://doi.org/10.1111/j.1365-2672.2010.04745.x

    Article  CAS  PubMed  Google Scholar 

  8. Ryan EP, Heuberger AL, Weir TL, Barnett B, Broeckling CD, Prenni JE (2011) Rice bran fermented with Saccharomyces boulardii generates novel metabolite profiles with bioactivity. J Agric Food Chem 59:1862–1870. https://doi.org/10.1021/jf1038103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Değirmencioğlu N, Gurbuz O, Şahan Y (2016) The monitoring, via an in vitro digestion system, of the bioactive content of vegetable juice fermented with Saccharomyces cerevisiae and Saccharomyces boulardii. J Food Process Preserv 40:798–811. https://doi.org/10.1111/jfpp.12704

    Article  CAS  Google Scholar 

  10. Hennequin C, Thierry A, Richard GF, Lecointre G, Nguyen HV, Gaillardin C et al (2001) Microsatellite typing as a new tool for identification of Saccharomyces cerevisiae Strains. J Clin Microbiol 39:551–559. https://doi.org/10.1128/JCM.39.2.551-559.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mills DR (1941) Differential staining of living and dead yeast cells. J Food Sci 6:361–371. https://doi.org/10.1111/j.1365-2621.1941.tb16295.x

    Article  Google Scholar 

  12. Diana C-R, Humberto H-S, Jorge YF (2015) Probiotic properties of leuconostoc mesenteroides isolated from Aguamiel of Agave salmiana. Probiotics Antimicro 7(2):107–117. https://doi.org/10.1007/s12602-015-9187-5

    Article  CAS  Google Scholar 

  13. Datta S, Timson DJ, Annapure US (2017) Antioxidant properties and global metabolite screening of the probiotic yeast Saccharomyces cerevisiae var. boulardii. J Sci Food Agr 97(9):3039–3049. https://doi.org/10.1002/jsfa.8147

    Article  CAS  Google Scholar 

  14. Wang Z, Zheng L, Li C, Wu S, Xiao Y (2017) Preparation and antimicrobial activity of sulfopropyl chitosan in an ionic liquid aqueous solution. J Appl Polym Sci 134(26). https://doi.org/10.1002/app.44989

  15. Cai Y, Weng K, Guo Y, Peng J, Zhu Z-J (2015) An integrated targeted metabolomic platform for high-throughput metabolite profiling and automated data processing. Metabolomics 11:1575–1586. https://doi.org/10.1007/s11306-015-0809-4

    Article  CAS  Google Scholar 

  16. Wang J, Zhang T, Shen X, Liu J, Zhao D, Sun Y et al (2016) Serum metabolomics for early diagnosis of esophageal squamous cell carcinoma by UHPLC-QTOF/MS. Metabolomics 12:116. https://doi.org/10.1007/s11306-016-1050-5

    Article  CAS  Google Scholar 

  17. Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G (2006) XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787. https://doi.org/10.1021/ac051437y

    Article  CAS  PubMed  Google Scholar 

  18. 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 

  19. Goktas H, Dertli E, Sagdic O (2021) Comparison of functional characteristics of distinct Saccharomyces boulardii strains isolated from commercial food supplements. LWT- Food Sci Technol 136(2):110340. https://doi.org/10.1016/j.lwt.2020.110340

    Article  CAS  Google Scholar 

  20. Nagashima AI, Pansiera PE, Baracat MM, Gomez RJHC (2013) Development of effervescent products, in powder and tablet form, supplemented with probiotics Lactobacillus acidophilus and Saccharomyces boulardii. Food Sci Technol 33(4):605–611. https://doi.org/10.1590/S0101-20612013000400002

    Article  Google Scholar 

  21. Motey GA, Johansen PG, Owusu-Kwarteng J, Ofori LA, Obiri-Danso K, Siegumfeldt H, Larsen N, Jespersen L (2020) Probiotic potential of Saccharomyces cerevisiae and Kluyveromyces marxianus isolated from West African spontaneously fermented cereal and milk products. Yeast 37:403–412. https://doi.org/10.1002/yea.3513

    Article  CAS  PubMed  Google Scholar 

  22. Pereira RP, Jadhav R, Baghela A et al (2021) In vitro assessment of probiotic potential of Saccharomyces cerevisiae DABRP5 isolated from Bollo batter, a traditional goan fermented food. Probiotics & Antimicro Prot 13:796–808. https://doi.org/10.1007/s12602-020-09734-8

    Article  CAS  Google Scholar 

  23. Chelliah R, Kim EJ, Daliri BM, Antony U, Oh DH (2021) In vitro probitotic evaluation of Saccharomyces boulardii with antimicrobial spectrum in a caenorhabditis elegans model. Foods 10(6):1428. https://doi.org/10.3390/foods10061428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Begley M, Hill C, Gahan CG (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bi J, Liu S, Du G, Chen J (2016) Bile salt tolerance of lactococcus lactis is enhanced by expression of bile salt hydrolase thereby producing less bile acid in the cells. Biotechnol Lett 38(4):659–665. https://doi.org/10.1007/s10529-015-2018-7

    Article  CAS  PubMed  Google Scholar 

  26. Fernández-Pacheco P, Ramos Monge IM, Fernández-González M, Poveda Colado JM, Arévalo-Villena M (2021) Safety evaluation of yeasts with probiotic potential. Front Nutr 8:659328. https://doi.org/10.3389/fnut.2021.659328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hernández-Gómez JG, López-Bonilla A, Trejo-Tapia G, Ávila-Reyes SV, Jiménez-Aparicio AR, Hernández-Sánchez H (2021) In vitro bile salt hydrolase (BSH) activity screening of different probiotic microorganisms. Foods 10:674. https://doi.org/10.3390/foods10030674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Naito Y, Tohda H, Okuda K, Takazoe I (1993) Adherence and hydrophobicity of invasive and noninvasive strains of porphyromonas gingivalis. Mol Oral Microbiol. https://doi.org/10.1111/j.1399-302X.1993.tb00559.x

    Article  Google Scholar 

  29. Brückner S, Mösch HU (2012) Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS microbiol rev 36(1):25–58. https://doi.org/10.1111/j.1574-6976.2011.00275.x

    Article  CAS  PubMed  Google Scholar 

  30. Kelesidis T, Pothoulakis C (2012) Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Ther adv in gastroenter 5:111–125. https://doi.org/10.1177/1756283X11428502

    Article  Google Scholar 

  31. Hanano A, Shaban M, Almousally I, Al-Ktaifani M (2015) Saccharomyces cerevisiae SHSY detoxifies petroleum n-alkanes by an induced CYP52A58 and an enhanced order in cell surface hydrophobicity. Chemosphere 135:418–426. https://doi.org/10.1016/j.chemosphere.2014.11.011

    Article  CAS  PubMed  Google Scholar 

  32. Ichikawa T, Hirata C, Takei M, Tagami N, Ikeda R (2017) Cell surface hydrophobicity and colony morphology of trichosporon asahii clinical isolates. Yeast 34(3):129–137. https://doi.org/10.1002/yea.3220

    Article  CAS  PubMed  Google Scholar 

  33. Shiradhone AB, Ingle SS, Zore GB (2018) Microenvironment responsive modulations in the fatty acid content, cell surface hydrophobicity, and adhesion of candida albicans cells. J Fungi (Basel, Switzerland) 4(2):47. https://doi.org/10.3390/jof4020047

    Article  CAS  Google Scholar 

  34. Rosa SD, Cirillo P, Paglia A, Sasso L, Palma VD, Chiariello M (2010) Reactive oxygen species and antioxidants in the pathophysiology of cardiovascular disease: does the actual knowledge justify a clinical approach? Curr Vasc Pharmacol 8:259–275. https://doi.org/10.2174/157016110790887009

    Article  PubMed  Google Scholar 

  35. Shobharani P, Prakash M, Halami PM (2015) Probiotic bacillus spp. In soy‐curd: nutritional, rheological, sensory, and antioxidant properties. J Food Sci 80(10–12):M2247–M2256. https://doi.org/10.1111/1750-3841.13004

    Article  CAS  PubMed  Google Scholar 

  36. Feng T, Wang J (2020) Oxidative stress tolerance and antioxidant capacity of lactic acid bacteria as probiotic: a systematic review. Gut Microbes 12(1):1801944. https://doi.org/10.1080/19490976.2020.1801944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Golubev WI, Pfeiffer I, Golubeva EW (2006) Mycocin production in pseudozyma tsukubaensis. Mycopathologia 162(4):313–316. https://doi.org/10.1007/s11046-006-0065-2

    Article  CAS  PubMed  Google Scholar 

  38. Rima H, Steve L, Ismail F (2012) Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol 3:421. https://doi.org/10.3389/fmicb.2012.00421

    Article  Google Scholar 

  39. Offei B, Vandecruys P, Graeve SD, Foulquié-Moreno MR, Thevelein JM (2019) Unique genetic basis of the distinct antibiotic potency of high acetic acid production in the probiotic yeast Saccharomyces cerevisiae var. boulardii. Genome Res 29:1478–1494. http://www.genome.org/cgi/doi/10.1101/gr.243147.118

  40. 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 

  41. Witkin JM, Tortella FC (1991) Modulators of N-methyl-D-aspartate protect against diazepam- or phenobarbital-resistant cocaine convulsions. Life Sci 48:L51–L56. https://doi.org/10.1016/0024-3205(91)90516-E

    Article  Google Scholar 

  42. Fossom LH, Von Lubitz DKJE, Lin RCS, Skolnick P (1995) Neuroprotective actions of 1-aminocyclopropanecarboxylic acid (ACPC): a partial agonist at strychnine-insensitive glycine sites. Neurol Res 17:265–269

    Article  CAS  PubMed  Google Scholar 

  43. Nahum-Levy R, Fossom LH, Skolnick P, Benveniste M (1999) Putative partial agonist 1-aminocyclopropanecarboxylic acid acts concurrently as a glycine-site agonist and a glutamate-site antagonist at N-methyl-D-aspartate receptors. Mol Pharmacol 56:1207–1218. https://doi.org/10.1124/mol.56.6.1207

    Article  CAS  PubMed  Google Scholar 

  44. Popik P, Holuj M, Nikiforuk A, Kos T, Skolnick P (2014) 1-Aminocyclopropanecarboxylic acid (acpc) produces procognitive but not antipsychotic-like effects in rats. Psychopharmacology 232: 1025–1038. https://doi.org/10.1007/s00213-014-3738-4

  45. Sakko M, Tjäderhane L, Sorsa T, Hietala P, Järvinen A, Bowyer P et al (2012) 2-Hydroxyisocaproic acid (HICA): a new potential topical antibacterial agent. Int J Antimicrob Agents 39:539–540. https://doi.org/10.1016/j.ijantimicag.2012.02.006

    Article  CAS  PubMed  Google Scholar 

  46. Sakko M, Moore C, Novak-Frazer L, Rautemaa V, Sorsa T, Hietala P et al (2014) 2-hydroxyisocaproic acid is fungicidal for Candida and Aspergillus species. Mycoses 57:214–221. https://doi.org/10.1111/myc.12145

    Article  CAS  PubMed  Google Scholar 

  47. Wu C, Huang Y, Lai X, Lai R, Zhao W, Zhang M et al (2014) Study on quality components and sleep-promoting effect of GABA Maoyecha tea. J Funct Foods 7:180–190. https://doi.org/10.1016/j.jff.2014.02.013

    Article  CAS  Google Scholar 

  48. Masuda K, Guo XF, Uryu N, Hagiwara T, Watabe S (2008) Isolation of marine yeasts collected from the Pacific Ocean showing a high production of γ-aminobutyric acid. Biosci Biotechnol Biochem 72:3265–3272. https://doi.org/10.1271/bbb.80544

    Article  CAS  PubMed  Google Scholar 

  49. Song NE, Baik SH (2014) Identification and characterization of high GABA and low biogenic amine producing indigenous yeasts isolated from Korean traditional fermented Bokbunja (Rubus coreanus Miquel) wine. J Biotechnol 185:S83. https://doi.org/10.1016/j.jbiotec.2014.07.285

    Article  Google Scholar 

  50. Zhang Q, Sun Q, Tan X, Zhang S, Zeng L, Tang J et al (2020) Characterization of γ-aminobutyric acid (GABA)-producing Saccharomyces cerevisiae and coculture with Lactobacillus plantarum for mulberry beverage brewing. J Biosci Bioeng 129:447–453. https://doi.org/10.1016/j.jbiosc.2019.10.001

    Article  CAS  PubMed  Google Scholar 

  51. Nascimento Fraga L, Karoline de Souza Oliveira A, Pinheiro Aragão B, Alves de Souza D, Willian Propheta Dos Santos E, Alves Melo J et al (2021) Mass spectrometry characterization, antioxidant activity, and cytotoxicity of the peel and pulp extracts of Pitomba. Food Chem 340:127929. https://doi.org/10.1016/j.foodchem.2020.127929

    Article  CAS  PubMed  Google Scholar 

  52. Ueda Y, Tsubuku T, Miyajima R (1994) Composition of sulfur-containing components in onion and their flavor characters. Biosci Biotechnol Biochem 58:108–110. https://doi.org/10.1271/bbb.58.108

    Article  CAS  PubMed  Google Scholar 

  53. Xiaogen Y, Elisabetta L,  Harry R, Alexander TP, Stephan H, Xinping L, Xun F (2013) Flavour modifying compounds. WO/2013/010991 http://www.freepatentsonline.com/WO2013010991.html

  54. Li Y, Bionda N, Yongye A, Geer P, Stawikowski M, Cudic P et al (2013) Dissociation of antimicrobial and hemolytic activities of gramicidin S through N-methylation modification. Chem Med Chem 8:1865–1872. https://doi.org/10.1002/cmdc.201300232

    Article  CAS  PubMed  Google Scholar 

  55. Valerio F, Lavermicocca P, Pascale M, Visconti A (2004) Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett 233:289–295. https://doi.org/10.1111/j.1574-6968.2004.tb09494.x

    Article  CAS  PubMed  Google Scholar 

  56. Kluczyk A, Popek T, Kiyota T, de Macedo P, Stefanowicz P, Lazar C et al (2002) Drug evolution: p-aminobenzoic acid as a building block. Curr Med Chem (CMC) 9:1871–1892. https://doi.org/10.2174/0929867023368872

    Article  CAS  Google Scholar 

  57. Casadey R, Challier C, Altamirano M, Spesia MB, Criado S (2020) Antioxidant and antimicrobial properties of tyrosol and derivative-compounds in the presence of vitamin b2. Assays of synergistic antioxidant effect with commercial food additives. Food Chem 335(8):127576. https://doi.org/10.1016/j.foodchem.2020.127576

    Article  CAS  PubMed  Google Scholar 

  58. Boronat A, Mateus J, Soldevila-Domenech N, Guerra M, Rodríguez-Morató J, Varon C, Muñoz D, Barbosa F, Morales JC, Gaedigk A, Langohr K, Covas M-I, Pérez-Mañá C, Fitó M, Tyndale RF, de la Torre R (2019) Cardiovascular benefits of tyrosol and its endogenous conversion into hydroxytyrosol in humans. A randomized, controlled trial. Free Radical Bio Med 143:471–481. https://doi.org/10.1016/j.freeradbiomed.2019.08.032

    Article  CAS  Google Scholar 

  59. Dieuleveux V, Van Der Pyl D, Chataud J, Gueguen M (1998) Purification and characterization of anti-listeria compounds produced by Geotrichum candidum. Appl Environ Microbiol 64:800–803. https://doi.org/10.1128/AEM.64.2.800-803.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dao Y, Zhang K, Lu X, Lu Z, Liu C, Liu M et al (2019) The role of glucose and 2-oxoglutarate/malate translocator (OMT1) in the production of phenyllactic acid and p hydroxyphenyllactic acid, two food-borne pathogen inhibitors. J Agric Food Chem 67:5820–5826. https://doi.org/10.1021/acs.jafc.9b01444

    Article  CAS  PubMed  Google Scholar 

  61. Wang JP, Yoo JS, Lee JH, Jang HD, Kim HJ, Shin SO et al (2009) Effects of phenyllactic acid on growth performance, nutrient digestibility, microbial shedding, and blood profile in pigs. J Anim Sci 87:3235–3243. https://doi.org/10.2527/jas.2008-1555

    Article  CAS  PubMed  Google Scholar 

  62. Svanström Å, Boveri S, Boström E, Melin P (2013) The lactic acid bacteria metabolite phenyllactic acid inhibits both radial growth and sporulation of filamentous fungi. BMC Res Notes 6(1):1–9. https://doi.org/10.1186/1756-0500-6-464

    Article  CAS  Google Scholar 

  63. Prema P, Smila D, Palavesam A, Immanuel G (2010) Production and characterization of an antifungal compound (3-phenyllactic acid) produced by Lactobacillus plantarum strain. Food Bioprocess Technol 3:379–386. https://doi.org/10.1007/s11947-008-0127-1

    Article  CAS  Google Scholar 

  64. Yu S, Jiang H, Jiang B, Mu W (2012) Characterization of D-lactate dehydrogenase producing D-3-phenyllactic acid from Pediococcus pentosaceus. Biosci Biotechnol Biochem 76:853–855. https://doi.org/10.1271/bbb.110955

    Article  CAS  PubMed  Google Scholar 

  65. Kawamura T, Okubo T, Sato K, Fujita S, Goto K, Hamaoka T et al (2012) Glycerophosphocholine enhances growth hormone secretion and fat oxidation in young adults. Nutrition 28(11-12): 1122-1126. https://doi.org/10.1016/j.nut.2012.02.011

  66. Narukawa M, Kamiyoshihara A, Izu H, Fujii T, Misaka T (2020) Efficacy of long-term feeding of α-glycerophosphocholine for aging-related phenomena in old mice. Gerontology 66(3):1–11. https://doi.org/10.1159/000504962

    Article  CAS  Google Scholar 

  67. Bansal T, Alaniz RC, Wood TK, Jayaraman A (2010) The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. P Natl Acad of Sci US 107(1):228–233. https://doi.org/10.1073/pnas.0906112107

    Article  Google Scholar 

  68. Martin AM, Young RL, Leong L, Rogers GB, Spencer NJ, Jessup CF, Keating DJ (2017) The diverse metabolic roles of peripheral serotonin. Endocrinology 158:1049–1063. https://doi.org/10.1210/en.2016-1839

    Article  CAS  PubMed  Google Scholar 

  69. Surjana D, Damian DL (2011) Nicotinamide in dermatology and photoprotection. Skinmed 9(6):360–365. PMID: 22256624

    PubMed  Google Scholar 

  70. Joseph A, Bernardes CES, da Piedade MEM (2012) Heat capacity and thermodynamics of solid and liquid pyridine-3-carboxylic acid (nicotinic acid) over the temperature range 296 K to 531 K. J Chem Thermodyn 55:23–28. https://doi.org/10.1016/j.jct.2012.06.010

    Article  CAS  Google Scholar 

  71. Xie Z, Cao N, Wang C (2021) A review on β-carboline alkaloids and their distribution in foodstuffs: a class of potential functional components or not? Food Chem 348:129067. https://doi.org/10.1016/j.foodchem.2021.129067

    Article  CAS  PubMed  Google Scholar 

  72. Gallardo-Fernández M, Valls-Fonayet J, Valero E, Hornedo-Ortega R, Richard T, Troncoso AM, Garcia-Parrilla MC (2022) Isotopic labelling-based analysis elucidates biosynthesis pathways in Saccharomyces cerevisiae for melatonin, serotonin and hydroxytyrosol formation. Food Chem 374:131742. https://doi.org/10.1016/j.foodchem.2021.131742

    Article  CAS  PubMed  Google Scholar 

  73. Liu S, Bai M, Zhou J, Jin Z, Xu Y, Yang Q, Zhou J, Zhang S, Mao J (2022) Analysis of genes from Saccharomyces cerevisiae HJ01 participating in aromatic alcohols biosynthesis during huangjiu fermentation. LWT-Food Sci Technol 154:112705. https://doi.org/10.1016/j.lwt.2021.112705

    Article  CAS  Google Scholar 

  74. Chrzanowski G (2020) Saccharomyces cerevisiae-an interesting producer of bioactive plant polyphenolic metabolites. Int J Mol Sci 21: 7343. https://doi.org/10.3390/ijms21197343

  75. Fernández M, Zúñiga M (2006) Amino acid catabolic pathways of lactic acid bacteria. Crit Rev Mcrobip 32(3):155. https://doi.org/10.1080/10408410600880643

    Article  CAS  Google Scholar 

  76. Park B, Hwang H, Chang JY, Hong SW, Lee SH, Jung MY, Sohn SO, Park HW, Lee JH (2017) Identification of 2-hydroxyisocaproic acid production in lactic acid bacteria and evaluation of microbial dynamics during kimchi ripening. Sci Rep 7:10904. https://doi.org/10.1038/s41598-017-10948-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Loh LX, Ng DHJ, Toh M, Lu Y, Liu SQ (2021) Targeted and nontargeted metabolomics of amino acids and bioactive metabolites in probiotic-fermented unhopped beers using liquid chromatography high-resolution mass spectrometry. J Agr Food Chem 69:14024–14036. https://doi.org/10.1021/acs.jafc.1c03992

    Article  CAS  Google Scholar 

  78. Magnusson J (2003) Antifungal activity of lactic acid bacteria. Acta Universitatis Agriculturae Sueciae Agraria

  79. Li X, Ning Y, Liu D, Yan A, Wang Z, Wang S, Miao M, Zhu H, Jia Y (2015) Metabolic mechanism of phenyllactic acid naturally occurring in chinese pickles. Food Chem 186:265–270. https://doi.org/10.1016/j.foodchem.2015.01.145

    Article  CAS  PubMed  Google Scholar 

  80. Schmidt M, Lynch KM, Zannini E, Arendt EK (2017) Fundamental study on the improvement of the antifungal activity of lactobacillus reuteri r29 through increased production of phenyllactic acid and reuterin. Food Control 88:139–148. https://doi.org/10.1016/j.foodcont.2017.11.041

    Article  CAS  Google Scholar 

  81. Zheng Z, Ma C, Gao C, Li F, Qin J, Zhang H et al (2011) Efficient conversion of phenylpyruvic acid to phenyllactic acid by using whole cells of bacillus coagulans sdm. PLoS ONE 6(4):e19030. https://doi.org/10.1371/journal.pone.0019030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Liu F, Wang F, Du L, Zhao T, Doyle MP, Wang D et al (2017) Antibacterial and antibiofilm activity of phenyllactic acid against enterobacter cloacae. Food Control 84:442–448. https://doi.org/10.1016/j.foodcont.2017.09.004

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the College of Bioengineering, Sichuan University of Science & Engineering and Wuliangye Yibin Co, Ltd., for their assistance, and we also would like to thank Editage (www.editage.cn) for English language editing.

Funding

This work was financially supported by the solid-state Fermentation Resource Utilization Key Laboratory of Sichuan Province (No. 2018GTY002) and The Industry-Academia Collaborative Project of Wuliangye, China (CXY2020ZR001).

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Authors and Affiliations

  1. College of Biotechnology Engineering, Sichuan University of Science and Engineering, Yibin, 644000, China

    JunJie Fu, Jun Liu, XuePing Wen, Guirong Zhang, Ji Cai & Li Li

  2. Wuliangye Yibin Co, Ltd, 150, Yibin, 644000, China

    Zongwei Qiao, Zheming An & Jia Zheng

Authors
  1. JunJie Fu
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  2. Jun Liu
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  3. XuePing Wen
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  4. Guirong Zhang
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  5. Ji Cai
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  6. Zongwei Qiao
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  7. Zheming An
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  8. Jia Zheng
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  9. Li Li
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Contributions

J. Fu conceived the research. J. Cai and G. Zhang analyzed the data, X. Wen contributed by providing reagents or analytical tools, and Z. Qiao, Z. An, and J. Zheng provided research funding. J. Liu and L. Li designed and supervised the experimental work as indicated in the parentheses. J. Fu and L. Li wrote the manuscript. All authors read critically and approved the manuscript.

Corresponding author

Correspondence to Li Li.

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Fu, J., Liu, J., Wen, X. et al. Unique Probiotic Properties and Bioactive Metabolites of Saccharomyces boulardii. Probiotics & Antimicro. Prot. 15, 967–982 (2023). https://doi.org/10.1007/s12602-022-09953-1

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