kluyveromyces marxianus benefits

A number of genome engineering tools have been The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb.2022.842097/full#supplementary-material, National Library of Medicine Screening of potential probiotic properties of Lactobacillus fermentum isolated from traditional dairy products. 2-Phenethylethanol is associated with descriptors such as flowery and honey-like (Czerny et al. Kluyveromyces marxianus has a promising enological potential because of strong extracellular pectinase activity and the copious production of specific higher alcohols and esters. The beetroot juice was prepared by grinding the vegetable with water in the ratio 1:1 (w:v). Modulation of the intestinal microbiota of dogs by Kefir as a functional dairy product. Effect of phenol concentration on the growth of the Kluyveromyces marxianus strains and Saccharomyces boulardii MYA-796. the highest transformation efficiency among the native strains All experiments were performed in triplicate. The first aim of this study was to obtain four ethanol-tolerant K. marxianus CCT 7735 strains (ETS1, ETS2, ETS3, and ETS4) by adaptive laboratory evolution. Food Bioprod Process 88:253258, Rajkowska K, Kunicka-Styczynsk A (2010) Probiotic properties of yeasts isolated from chicken feces and kefirs. Culture: Colonies (SDA) white to cream-coloured smooth, glabrous, yeast-like. Homayouni-Rad Aziz , Azizi Aslan , Oroojzadeh Parvin *, Pourjafar Hadi *, Kluyveromyces marxianus as a Probiotic Yeast: A Mini-review, Current Nutrition & Food Science 2020; 16(8) Saccharomyces cerevisiae. J Funct Foods 34:408421, Siebert TE, Smyth HE, Capone DL, Neuwhoner C, Pardon KH, Skouroumounis GK, Herderich MJ, Sefton MA, Pollnitz AP (2005) Stable isotope dilution analysis of wine fermentation products by HS-SPME-GC-MS. Anal Bioanal Chem 381:937947, Soares RD, Welke JE, Nicolli, KP, Zanus M (2015) Monitoring the evolution of volatile compounds using gas chromatography during the stages of production of Moscatel sparkling wine. In: Querol A, Fleet G, Eds Yeasts in food and beverages. Herein, the survivability of five kefir-isolated K. marxianus strains (Km A1-A5) in a simulated gastrointestinal (GI) environment was evaluated and compared with those of commercial probiotic yeast . Nutr Res Rev 17:259275, Guyton AC, Hall JE (2011) Tratado de Fisiologia Mdica. This is a food-grade yeast with various beneficial traits, such as rapid growth rate and . Microbiologyopen 7:e00533. The site is secure. Broad conservation of milk utilization genes in. The probiotic Saccharomyces boulardii showed a survival rate of 79.29%, while six (B9, C3, C5, C16, D19, B7) of the tested strains showed higher (Scott-Knott p<0.05) values (Table 1). Microbiol. This compound is commonly associated with aroma descriptors Citrus-like, soapy (Czerny et al. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. 2008). Kluyveromyces marxianus accounts for > 90% of the yeast population of kefir, and recently, its probiotic potential has been actively explored with a focus on its health benefits and safety. Keywords: PubMed Central Kluyveromyces marxianus is an ascomycetous yeast which has shown promising results in cellulosic ethanol and renewable chemicals production. The yeast strains were exposed to the simulated gastric fluid adjusted to pH 2.0 and 3.0 and incubated with agitation for 2 h at 37C, respectively. The OD was read in a spectrophotometer at 420nm. This compound has aroma descriptors wax, tallow, rancid, soap (Meilgaard 1975). Flavanol monomer-induced changes to the human faecal microflora. In our work, all the tested K. lactis strains showed resistance above 82% after 90min of exposure to simulated gastric juice. Briefly, the primer pair sequences for ITS sequencing are as follows: ITS1: 5- TCC GTA GGT GAA CCT GCG G-3 and ITS4: 5- TCC TCC GCT TAT TGA TAT GC-3. J Funct Foods 2015; 16: 278-88. Supplemental K. marxianus at high dose (2.5 g/kg) was more effective for feed efficiency and intestinal health of broilers, while the innate immunity was optimized at a medium dose (1.0 g/kg). 2010; Chen et al. Ferrero R. L., Hazell S. L., Lee A. Briefly, five K. marxianus and Sb MYA-796 were each suspended in potato dextrose broth (PDB; Difco, Detroit, MI, United States) and adjusted to 2.5 McFarland [approximately 105 colony forming units (CFU)/mL]. Process Biochem 45:954960, Spohner SC, Schaum V, Quitmann H, Czermak P (2016) Kluyveromyces lactis: an emerging tool in biotechnology. Easy. Homayouni Rad A, Torab R, Mortazavian AM, Mehrabany EV, Mehrabany LV. Compounds were identified using the NIST library 2011 and the quantification performed using internal calibration with 4-nonanol at a final concentration of 125g/L (Duarte et al. Organic Materials Review Institute [OMRI] (2014). The group of acids was composed only by 4 compounds, octanoic, decanoic, dodecanoic, and hexadecenoic acids (Table 5). will also be available for a limited time. 2003). Short chain fatty acids acetate and propionate also increased following the yeast supplementation. Int J Microbiol Res 5:390398, Wootton-Beard PC, Ryan L (2011) A beetroot juice shot is a significant and convenient source of bioaccessible antioxidants. The yeast Kluyveromyces marxianus and its biotechnological potential. The plates were incubated for 2h at 4C to allow the diffusion of the supernatant and then incubated at 37C for 48h. In the gas production antagonism test, two compartment plates were inoculated with a yeast culture in one compartment and with the pathogen cultures in another compartment. Food Control 2013; 30(1): 206-13. In both cases of total phenolics and antioxidant activity, it is possible to note that the results are proportionally to the used amount of beetroot juice. This higher fructose content can impact the taste of the beverages since this sugar has a sweetness 2 times greater than, for example, glucose. Yeast 32, (1996). Mirzaei M, Mirdamadi S, Ehsani MR, Aminlari M. Production of antioxidant and ACE-inhibitory peptides from Kluyveromyces marxianus protein hydrolysates: purification and molecular docking. Urease is considered a stress response that counteracts the effects of low pH environments and modulates intracellular and extracellular pH in some bacteria (Mora et al., 2004). Another study suggested that, under simulated gastric conditions (pH 3.0) and duodenum juice, K. marxianus NS1KM2, 14KM1, and 6688 KM isolated from Fiore Sardo cheese had better survival (decrease by 017%) than S. boulardii CODEX SB1 (decrease by 64.5%) (Fadda et al., 2017). In both cases of diluted (NW) and concentrated (CW) cheese whey, at the end of fermentation, yeast completely consumed the sugar content (Table 4), highlighting the efficient activity of -galactosidase produced by K. lactis B9. Food Res Int 43:23032314, Escudero-Lpez B, Cerrillo I, Gil-Izquierdo , Hornero-Mndez D, Herrero-Martn G, Bern G, Fernndez-Pachn MS (2016) Effect of thermal processing on the profile of bioactive compounds and antioxidant capacity of fermented orange juice. organisms have been used to produce food products and beverages including bread and beer. Google Scholar, Czerny M, Christbauer M, Christbauer M, Fischer A, Granvogl M, Hammer M, Hartl C, Hernandez NM, Schieberle P (2008) Re-investigation on odour thresholds of key food aroma compounds and development of an aroma language based on odour qualities of defined aqueous odorant solutions. Biochemical characteristics, virulence traits and antifungal resistance of two major yeast species isolated from Kefir: Liu H., Xie Y. H., Xiong L. X., Dong R. T., Pan C. L., Teng G. X., et al. (8 votes) Very easy. This study investigated the cancer chemopreventive, the antiradical, and the antiproliferative properties of polysaccharides extracts from cell wall of Saccharomyces boulardii and Kluyveromyces marxianus. Food Res Int 48:1620, Richards LB, Li M, Van Esch BCAM, Garssen J, Folkerts G (2016) The effects of short-chain fatty acids on the cardiovascular system. 2006). The secretion performances were analyzed in the host K. marxianus L3 in the range between 5C and 40C by means of 3 . Fleet G. The commercial and community significance of yeasts in food and beverage production. This study did not involve human participants or animals. In addition, the five K. marxianus strains and S. boulardii MYA-796 displayed different assimilation of lactose, xylitol, D-sorbitol, and DL-lactate, indicating that K. marxianus metabolized a wide range of substances and, thus, might be more feasible to nourish themselves in the host GI tract for survival. Lukondeh T, Ashbolt NJ, Rogers PL. Int J Food Microbiol 2008; 126(3): 321-6. 1 Conclusion: It can be concluded that K. marxianus may be considered as a probiotic micro organism with a variety of commercial and medical applications. Cells were stained with 0.1% (w/v) crystal violet (100 L; Sigma-Aldrich, St. Louis, MO, United States) for 15 min at room temperature (2025C) and rinsed twice with PBS (Sigma-Aldrich). Chandra R, Castillo-Zacarias C, Delgado P, Parra-Saldvar R. A biorefinery approach for dairy wastewater treatment and product recovery towards establishing a biorefinery complexity index. Screening and characterization of in-vitro probiotic criteria of Saccharomyces and Kluyveromyces strains. Moreover, these urease-positive microorganisms share the environmental benefit of a temporal local pH increase with urease-negative microorganisms (Arioli et al., 2010). Lentilactobacillus kefiri, Kluyveromyces marxianus, and Saccharomyces unisporus) were given to 11 metabolic syndrome patients and 180 mL/day of unfermented milk to 11 metabolic syndrome patients. Perspectives for the biotechnological Mixed culture of Kluyveromyces marxianus and Candida krusei for single-cell protein production and organic load removal from whey. (2017) and Fadda et al. Effect and mechanism of cholesterol-lowering by. Km A1A5 showed a difference in sensitivity for different phenol concentrations but overall could tolerate the tested phenol concentrations. ISSN (Print): 1573-4013 This is also a requirement for probiotic yeasts candidates. K. marxianus strains showed a greater hydrophobicity of cell surface, abilities to biofilm formation and auto-aggregation, and phenol tolerance than S. boulardii MYA-796, suggesting greater potential for survival in the host GI tract. Colony: Malt agar: puffy, creamish-brown, flat, spreading, dull round colony. Kefir is a traditional dairy product containing multiple probiotic microorganisms, primarily lactic acid bacteria, such as Lactobacillus kefiranofaciens and Lactobacillus kefiri, and yeasts including Kluyveromyces marxianus and Saccharomyces unisporus (Kim et al., 2019a). 7H2O, 0.3% K2HPO4) (Song et al. The PubMed Other esters and acetates were also measured in high concentration (Table 5). To the best of our knowledge, few studies have demonstrated the survivability and survival affecting factors of K. marxianus isolated from kefir in vitro with the most renowned probiotic yeast, S. boulardii, as a reference. J Agric Food Chem 2014; 62(7): 1609-16. Potential probiotic characterization and effect of encapsulation of probiotic yeast strains on survival in simulated gastrointestinal tract condition. A major limitation of this study is that we did not simulate the biological nor the physical conditions such as microbiome and lack of oxygen. The lysed sample was then transferred to a plastic vessel containing 50 L of magnetic silica and subjected to automatic magnetic bead separation. production of ethyl acetate by yeasts. Daz-Vergara L, Pereyra CM, Montenegro M, Pena GA, Aminahuel CA, Cavaglieri LR. Food Res Int 69:331340, CAS (2018), in cheese, esters are desirable volatile compounds because they have fruity and high volatility. The yeast Kluyveromyces marxianus was permitted for direct addition to food and shown antagonistic ability against some pathogens. The oven was maintained at 200C and the carrier gas flow was 1.1mL/min. bulgaricus and L. helveticus for sourdough bread making. (2010). The plates were incubated at 37C for 48h. For all of these experiments, the presence or absence of zones of inhibition was inspected after the incubation periods. NW 1:1, non-concentrated fermented cheese whey added to beetroot juice in a ratio of 1:1 (v:v); NW 1:3 (v:v), non-concentrated fermented cheese whey added to beetroot juice in the ratio of 1:3 (v:v); CW 1:1, concentrated fermented cheese whey added to beetroot juice in the ratio of 1:1 (v:v); CW 1:3, concentrated fermented cheese whey added to beetroot juice in the ratio of 1:3 (v:v). (2016) with slight modifications. Changes in the number of viable cells of the five Kluyveromyces marxianus strains isolated from kefir and Saccharomyces boulardii MYA-796 at pH 2.0 to 7.5, 2.0 to 8.5, 3.0 to 7.5, and 3.0 to 8.5. several K. marxianus isolates was evaluated (Cernak, Colonization of Helicobacter pylori in the stomach has been related to the presence of bacterial urease and urea metabolism (Ferrero et al., 1988). The tested K. lactis strains were isolated from samples of milk, Canastra cheese, cheese whey, and pingo (endogenous starter), which are naturally low pH environments, a condition that may have favored the resistance of the yeasts to the acidity of the stomach. 1). The highest production of esters and acetates agrees with the expected, considering the use of K. lactis, a known yeast for its efficiency for the production of these compounds. 4th ed. (1988). Background: Yeasts play diverse roles in human life. Food Res Int 91:7279, Beards E, Tuohy K, Gibson G (2010) Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Google Scholar, Andrade RP, Melo CN, Genisheva Z, Schwan RF, Duarte WF (2017) Yeasts from Canastra cheese production process: isolation and evaluation of their potential for cheese whey fermentation. metabolize a wide range of sugars, and are fast growing, thus they Kluyveromyces marxianus as a host Food Chem 2008; 106(3): 985-90. 5). Spore: smooth spores ranging from spheroidal to bean or crescent . London, Ontario, Canada 2002; p. 30. Aloglu HS, Ozer ED, Oner Z (2016) Assimilation of cholesterol and probiotic characterization of yeast strains isolated from raw milk and fermented foods. The lactose hydrolysis by microorganisms is important considering the benefit in cases of lactose intolerance, whether by the production of -galactosidase in the intestinal lumen or by the use of microorganism to manufacture free-lactose dairy foods. Van der Walt, J.P. 1965. Error bars represent standard deviations. Some of the species, such as K. marxianus, are the teleomorphs of Candida species.. In general, Km A4 and A5 showed the highest survivability among Km strains tested. The biofilm-forming ability of Km A1-A5 was significantly different from that of Sb MYA-796 after 24 h at 37C (p < 0.05; Figure 4A). After comparison with a previous study, the biofilm formation ability of K. marxianus strains (Km A1-A5) isolated from kefir was superior to that of K. marxianus S-2-05 isolated from a traditional French cheese. Biochemical activities of five K. marxianus strains and S. boulardii MYA-796 differing at the strain level. [4] Fantes PA. Control of cell size and cycle time in Schizosaccharomyces [22] Pinheiro R, Belo I, Mota M. Oxidative stress response of Kluyveromyces pombe. J Dairy Sci 87:40504056, Ledauphin J, Guichard H, Saint-Clair JF, Picoche B, Barillier D (2003) Chemical and sensorial aroma characterization of freshly distilled calvados. Snchez B., Delgado S., Blanco-Mguez A., Loureno A., Gueimonde M., Margolles A. Serum and intestine samples were collected at 21 d of age. Relatively few studies have been conducted focusing on the survivability and the factors involved in the survival of the K. marxianus strains compared to the studies on the same aspects of S. boulardii. (1996). Part of 3). Therefore, the -galactosidase produced by strain B9 has optimum activity at neutral and alkaline pH. The fermentation process started with 1.5108cells/mL and this population remained stable (7.9108cells/mL) during the shelf life test up to 21days. Xanthopoulos V., Litopoulou-Tzanetaki E., Tzanetakis N. (2000). statement and The identities of the isolates were determined on the highest BLAST score. yeast Kluyveromyces marxianus for the biotechnological Homayoni Rad A, Mehrabany EV, Alipoor B, Mehrabany LV, Javadi M. Do probiotics act more efficiently in foods than in supplements? Lactococcus lactis subsp. 1987). 2010) and incubated at 30C/200rpm for 48h. After, 500mg of biomass was harvested and used for the cell permeabilization with the addition of 5mL of isoamyl alcohol, 25mL of phosphate buffer, and glass bead (1mm) followed by vortexing for 5min and incubation under stirring for a further 15min at room temperature. First, 120L of the centrifuged beverages (10,000rpm, 10min, 4C) and 600L of methanol were mixed. government site. J Funct Foods 3:329334, Wruss J, Waldenberger G, Huemer S, Uygun P, Lanzerstorfer P, Mller U, Weghuber J (2015) Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. Ceugniez A., Coucheney F., Jacques P., Daube G., Delcenserie V., Drider D. (2017). Food Microbiol 52:177184, Ceugniez A, Coucheney F, Jacques P, Daube G, Delcenserie V, Drider D (2017) Anti-Salmonella activity and probiotic trends of Kluyveromyces marxianus S-2-05 and Kluyveromyces lactis S-3-05 isolated from a French cheese, TommedOrchies. UK: Springer 2006; pp. DemirkesenBiak H: Probiotics from food products and gastrointestinal health dietary interventions in gastrointestinal diseases. The -galactosidase activity of selected K. lactis (B9) at different pH. The hydrophobicity of the five K. marxianus strains and Sb MYA-796 was evaluated using the microbial adhesion to solvent (MATS) method described by Bellon-Fontaine et al. 2. J Appl Microbiol 2017; 123(6): 1360-72. This study was financially supported by the Coordenao de Aperfeioamento de Pessoal de Nvel SuperiorBrasil (CAPES)Finance Code 001, Conselho Nacional de Desenvolvimento Cientfico e Tecnolgico do Brasil (CNPq), and Fundao de Amparo Pesquisa de MG (FAPEMIG). This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). J Biotechnol 222:104116, Syal P, Vohra A (2013) Probiotic potential of yeasts isolated from traditional Indian fermented foods. RG-1 organism. Fonseca H. C., de Sousa Melo D., Ramos C. L., Dias D. R., Schwan R. F. (2021). SSF experiments were carried out using the yeast Kluyveromyces marxianus as the inoculum and oil palm wastes as the substrate, in order to obtain glucose and ethanol concentration data. K. marxianus NRRL Y-1190 (ATCC 8635, DSM 5421), had Moderate. Hydrophobicity of eleven different K. lactis strains. Ileal bacterial communities between K. marxianus-treated and untreated groups formed distinctly different clusters. which may contribute to the reputed health benefits of kefir (Guzel-Seydim et al. Maccaferri S, Klinder A, Brigidi P, Cavina P, Costabile A. Self-cleavage of polyprotein with FMDV P2A in K. marxianus. Our results indicate that K. marxianus strains isolated from kefir have greater hydrophobicity, biofilm formation, and auto-aggregation properties than the probiotic Sb MYA-796. Appl. The pancreatic secretion contains multiple enzymes to digest all three major food groups (proteins, carbohydrates, and fats) (Guyton and Hall 2011). Strains were grown on PDA at 30C for 24 h, and the cells were then sub-cultured twice under aerobic conditions. Conclusion: It can be concluded that K. marxianus may be considered as a probiotic micro organism Kluyveromyces marxianus accounts for > 90% of the yeast population of kefir, and recently, its probiotic potential has been actively explored with a focus on its health benefits and safety. Srum de llet (Europa i altres) Lactococcus lactis subsp. Sb MYA-796 was used as a control strain since it is the most studied and only clinically demonstrated probiotic yeast strain (Sazawal et al., 2006). The total content of polyphenols was determined using the method of Folin-Ciocalteu, according to Wootton-Beard and Ryan (2011) with adaptations. The OD of the suspension before (A0) and after 5 h incubation at 37C (At) were measured at a wavelength of 595 nm using a Multiskan FC (Thermo Fisher Scientific). The extracted compounds were analyzed in a GC-MS-QP2010 Plus (Shimadzu) chromatograph equipped with a Rts-5MS (30m 0.25mm 0.25m) column. Shehata M. G., El Sohaimy S. A., El-Sahn M. A., Youssef M. M. (2016). The highest values were found for Km A5, which exhibited an auto-aggregation value of 84.66%, whereas that of Sb MYA-796 was 68.67% (p < 0.05). Mladenovi K. G., Grujovi M. , Nikodijevi D., omi L. R. (2020). Differences were considered significant at p < 0.05. J Food Sci 72:M153M159, Meilgaard MC (1975) Flavor chemistry of beer: Part II: flavor and threshold of 239 aroma volatiles. (2022). To identify genes potentially involved in adhesion properties, a RT-qPCR analysis was performed. Also provided are the following, characterized by the use of the provided high-expression promoter; a recombinant polynucleotide containing said high-expression promoter; a vector containing said recombinant polynucleotide; a transformant obtained by introducing said recombinant . UK: Springer 2006; pp. Kluyveromyces marxianus strains are thermotolerant, can metabolize a wide range of sugars, and are fast growing, thus they have significant biotechnological potential (Gombert, 2016).K. Bastani P, Homayouni A, Norouzi-Panahi L. Working group report on drafting guidelines for the evaluation of probiotics in food. (2010). 2018; 71: pp. 2019; pp. To be considered probiotic, a bacterium must survive to pH2.0 and 3.0 during 3h (Park et al. Nutrition 2013; 29(5): 805-6. Divisekera D. M. W. D., Samarasekera J. K. R. R., Hettiarachchi C., Gooneratne J., Choudhary M. I., Gopalakrishnan S., et al. FEMS Microbiol Lett 1995; 127(3): 213-22. https://dx.doi.org/10.2174/1573401316666200217113230, Recent Advances in Food Nutrition & Agriculture, Capillary Electrophoresis in Food Analysis, Advances in Meat Processing Technologies: Modern Approaches to Meet Consumer Demand. 2017). The emendation of the genus Kluyveromyces v. d. Walt. Chem Biochem Eng Q 2002; 16(1): 13-6. Keywords: Clinical microbiology, food industry, Kluyveromyces marxianus, medicine, probiotic, yeast. Different lowercase letters indicate statistical difference (Scott-Knott test p<0.05) between the beverages at 0days of storage, Antioxidant potential (DPPH) of beverages at 0 and 21days of storage under refrigeration at 4 C. NW 1:1, non-concentrated fermented cheese whey added to beetroot juice in a ratio of 1:1 (v:v); NW 1:3 (v:v), non-concentrated fermented cheese whey added to beetroot juice in the ratio of 1:3 (v:v); CW 1:1, concentrated fermented cheese whey added to beetroot juice in the ratio of 1:1 (v:v); CW 1:3, concentrated fermented cheese whey added to beetroot juice in the ratio of 1:3 (v:v). The biofilm-forming ability of the yeast strains was evaluated as previously described (Jeong et al., 2018). Forty-four volatile compounds were identified in the produced beverages (Table 5). Pankova N. V., Polyudova T. V., Lemkina L. M., Korobov V. P. (2011). (Nurcholis, 2020). 55-62. UK: Springer 2017; pp. The hydrochloric acid excreted by the parietal cells is responsible for the acidity in the organism (which pH ranges from 1.5 to 3.5) and acts as a defense against pathogenic microorganism. Genetic basis of the highly efficient yeast Kluyveromyces marxianus: complete genome sequence and transcriptome analyses. The physiological concentration of bile salts in the small intestine ranges from 0.2 to 2.0%. Youn H. Y., Kim D. H., Kim H. J., Jang Y. S., Song K. Y., Bae D., et al. B., Kim H., Seo K. H. (2019). Front Microbiol 2012; 3: 421. Nutrients 2010; 2(4): 449-73. biotechnological tools for industrial applications of https://blast.ncbi.nlm.nih.gov/Blast.cgi. -Galactosidase activities presented as averages of three different temperatures (20, 30, and 45C).

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