Effect of probiotic yeast Pichia kudriavzevii 2P10 and mannan-oligosaccharide on the intestine health of rat infected with Salmonella Typhimurium

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Vol. 26 No. 1 (2025)
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RAHAYU WULAN
Doctoral Program of Microbiology, Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Raya Dramaga, Bogor 16680, West Java, Indonesia
RIKA INDRI ASTUTI
Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Agatis, IPB Dramaga Campus, Bogor 16680, West Java, Indonesia
YAYA RUKAYADI
Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia. Persiaran Asam Jawa, Serdang 43400, Selangor, Malaysia
SRI ESTUNINGSIH
Department of Reproductive Pathology Clinic, Faculty of Veterinary Clinic, Institut Pertanian Bogor. Jl. Agatis, Kampus IPB Dramaga IPB Dramaga Campus, Bogor 16680, West Java, Indonesia
ANJA MERYANDINI ♥
Department of Biology, Faculty of Mathematics and Natural Sciences, Institut Pertanian Bogor. Jl. Agatis, IPB Dramaga Campus, Bogor 16680, West Java, Indonesia

Abstract

Abstract. Wulan R, Astuti RI, Rukayadi Y, Estuningsih S, Meryandini A. 2025. Effect of probiotic yeast Pichia kudriavzevii 2P10 and mannan-oligosaccharide on the intestine health of rat infected with Salmonella Typhimurium. Biodiversitas 26: 335-344. Recent evidence suggests that probiotic yeast is efficacious against bacterial infections. This study evaluated the effects of dietary supplementation with the live yeast probiotic Pichia kudriavzevii 2P10, Mannan-Oligosaccharide (MOS), and their combination on the growth performance and intestinal health of male Sprague-Dawley (SD) rats infected with Salmonella Typhimurium ATCC 14028 (ST). Two groups were studied: one without ST infection, including P. kudriavzevii 2P10 (PRO), MOS, and their combination (PMOS), and one with ST infection, including CONTROL.ST, PRO.ST, MOS.ST, and PMOS.ST. A diet of 108 CFU/mL PRO and 5% MOS was administered orally for 15 days, followed by a challenge with 108 CFU/mL ST in the ST group. After three days of challenge, the parameters were observed. The findings of this research are that ST infection in rats can cause colonization of ST in the ileum, causing a decrease in white blood cells, necrosis of epithelial cells, and an increased villous-to-crypt ratio (VCR) as a response to inflammation. The administration of PRO, MOS, and their combinations prevents inflammation, as proven by the absence of necrosis and epithelial desquamation. PRO, MOS, and their combinations stimulate intestinal health by increasing villus height, width, and VCR. MOS was found to be the best for increasing lactic acid bacteria. During ST infection, P. kudriavzevii 2P10 can coagulate with ST in the ileum, with this yeast-bacteria binding mechanism allowing free Salmonella Typhimurium cells to bind more to P. kudriavzevii 2P10 cells than to intestinal epithelial cells so that bacterial infection can be prevented. In conclusion, P. kudriavzevii 2P10 administration was the best for stimulating growth performance and intestinal health and preventing severe ST infection in male SD rats, offering promising avenues for further research and potential practical applications in human and animal nutrition and health.

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References
Alkalbani NS, Osaili TM, Al-Nabulsi AA, Olaimat AN, Liu SQ, Shah NP, Apostolopoulos V, Ayyash MM. 2022. Assessment of yeasts as potential probiotics: A review of gastrointestinal tract conditions and investigation methods. J Fungi 8: 365. DOI: 10.3390/JOF8040365/S1.
Anderson CJ, Kendall MM. 2017. Salmonella enterica serovar Typhimurium strategies for host adaptation. Front Microbiol 8: 1983. DOI: 10.3389/fmicb.2017.01983.
Argüello H, Estellé J, Zaldívar-López S, Jiménez-Marín Á, Carvajal A, López-Bascón MA, Crispie F, O’Sullivan O, Cotter PD, Priego-Capote F, Morera L, Garrido JJ. 2018. Early Salmonella Typhimurium infection in pigs disrupts microbiome composition and functionality principally at the ileum mucosa. Sci Rep 8 (1): 7788. DOI: 10.1038/s41598-018-26083-3.
Bakkeren E, Huisman JS, Fattinger SA, Hausmann A, Furter M, Egli A, Slack E, Sellin ME, Bonhoeffer S, Regoes RR, Diard M, Hardt WD. 2019. Salmonella persisters promote the spread of antibiotic resistance plasmids in the gut. Nature 573 (7773): 276-280. DOI: 10.1038/s41586-019-1521-8.
Berutu CAM, Fahrurrozi F, Meryandini A. 2017. Pectinase production and clarification treatments of apple (Malus domestica) juice. Ann Bogorienses 21: 63-68. DOI: 10.14203/ann.bogor.2017.v21.n2.63-68.
Carstensen JW, Chehri M, Schønning K, Rasmussen SC, Anhøj J, Godtfredsen NS, Andersen CØ, Petersen AM. 2018. Use of prophylactic Saccharomyces boulardii to prevent Clostridium difficile infection in hospitalized patients: A controlled prospective intervention study. Eur J Clin Microbiol Infect Dis 37 (8): 1431-1439. DOI: 10.1007/s10096-018-3267-x.
Chowdhury R, Pavinski Bitar PD, Chapman HM, Altier C. 2023. Salmonella invasion is controlled by competition between intestinal chemical signals. MBio 14: e00012-23. DOI: 10.1128/mbio.00012-23.
Crowley SM, Han X, Allaire JM, Stahl M, Rauch I, Knodler LA, Vallance BA. 2020. Intestinal restriction of Salmonella Typhimurium requires caspase-1 and caspase-11 epithelial intrinsic inflammasomes. PLoS Pathog 16 (4): e1008498. DOI: 10.1371/journal.ppat.1008498.
Delwatta SL, Gunatilake M, Baumans V, Seneviratne MD, Dissanayaka MLB, Batagoda SS, Udagedara AH, Walpola PB. 2018. Reference values for selected hematological, biochemical and physiological parameters of Sprague?Dawley rats at the Animal House, Faculty of Medicine, University of Colombo, Sri Lanka. Anim Model Exp Med 1 (4): 250-251. DOI: 10.1002/AME2.12041.
Duarte ME, Tyus J, Kim SW. 2020. Synbiotic effects of enzyme and probiotics on intestinal health and growth of newly weaned pigs challenged with enterotoxigenic F18+ Escherichia coli. Front Vete 7: 573. DOI: 10.3389/fvets.2020.00573.
Fàbrega A, Vila J. 2013. Salmonella enterica serovar Typhimurium skills to succeed in the host: Virulence and regulation. Clin Microbiol Rev 26 (2): 308-341. DOI: 10.1128/CMR.00066-12.
Federer W. 1967. Experimental Design: Theory and Application. IBH Publishing Company, Oxford.
García-Quintanilla M, Casadesús J. 2011. Virulence plasmid interchange between strains ATCC 14028, LT2, and SL1344 of Salmonella enterica serovar Typhimurium. Plasmid 65 (2): 169-175. DOI: 10.1016/j.plasmid.2010.12.001.
Gart EV, Suchodolski JS, Welsh THJ, Alaniz RC, Randel RD, Lawhon SD. 2016. Salmonella Typhimurium and multidirectional communication in the gut. Front Microbiol 7: 1827. DOI: 10.3389/FMICB.2016.01827.
Geng J, Ni Q, Sun W, Li L, Feng X. 2022. The links between gut microbiota and obesity and obesity related diseases. Biomed Pharmacother 147: 112678. DOI: 10.1016/J.BIOPHA.2022.112678.
Gut AM, Vasiljevic T, Yeager T, Donkor ON. 2018. Salmonella infection - prevention and treatment by antibiotics and probiotic yeasts: A review. Microbiology 164: 1327-1344. DOI: 10.1099/mic.0.000709.
Jahromi MF, Shokryazdan P, Idrus Z, Ebrahimi R, Bashokouh F, Liang JB. 2017. Modulation of immune function in rats using oligosaccharides extracted from palm kernel cake. Biomed Res Intl 2017 (1): 2576921. DOI: 10.1155/2017/2576921.
Kango N, Jana UK, Choukade R, Nath S. 2022. Advances in prebiotic mannooligosaccharides. Curr Opin Food Sci 47: 100883. DOI: 10.1016/j.cofs.2022.100883.
Kim MS, Yoon YS, Seo JG, Lee HG, Chung MJ, Yum DY. 2013. A study on the prevention of Salmonella infection by using the aggregation characteristics of lactic acid bacteria. Toxicol Res 29 (2): 129-135. DOI: 10.5487/TR.2013.29.2.129.
Lee SM, Kim N, Park JH, Nam RH, Yoon K, Lee DH. 2018. Comparative analysis of ileal and cecal microbiota in aged rats. J Cancer Prev 23 (2): 70-76. DOI: 10.15430/JCP.2018.23.2.70.
Li D, Chen H, Mao B, Yang Q, Zhao J, Gu Z, Zhang H, Chen YQ, Chen W. 2017. Microbial biogeography and core microbiota of the rat digestive tract. Sci Rep 7 (1): 45840. DOI: 10.1038/srep45840.
Liu H, Whitehouse CA, Li B. 2018. Presence and persistence of Salmonella in water: The impact on microbial quality of water and food safety. Front Public Healt 6: 159. DOI: 10.3389/fpubh.2018.00159.
Madigan MT, Martinko JM, Stahl DA, Clark DP. 2022. Brock Biology of Microorganisms Sixteenth Edition. Pearson, Amsterdam.
Martins FS, Dalmasso G, Arantes RME, Doye A, Lemichez E, Lagadec P, Imbert V, Peyron JF, Rampal P, Nicoli JR, Czerucka D. 2010. Interaction of Saccharomyces boulardii with Salmonella enterica serovar Typhimurium protects mice and modifies T84 cell response to the infection. PLoS One 5: e8925. DOI: 10.1371/journal.pone.0008925.
Martins FS, Vieira AT, Elian SDA, Arantes RME, Tiago FCP, Sousa LP, Araújo HRC, Pimenta PF, Bonjardim CA, Nicoli JR, Teixeira MM. 2013. Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect 15 (4): 270-279. DOI: 10.1016/j.micinf.2012.12.007.
Mazkour S, Shekarforoush SS, Basiri S, Nazifi S, Yektaseresht A, Honarmand M. 2020. Effects of two probiotic spores of Bacillus species on hematological, biochemical, and inflammatory parameters in Salmonella Typhimurium infected rats. Sci Rep 10 (1): 8035. DOI: 10.1038/s41598-020-64559-3.
Ménard S, Lacroix-Lamandé S, Ehrhardt K, Yan J, Grassl GA, Wiedemann A. 2022. cross-talk between the intestinal epithelium and Salmonella Typhimurium. Front Microbiol 13: 906238. DOI: 10.3389/FMICB.2022.906238/BIBTEX.
Miki T, Okada N, Shimada Y, Danbara H. 2004. Characterization of Salmonella pathogenicity island 1 type III secretion-dependent hemolytic activity in Salmonella enterica serovar Typhimurium. Microb Pathog 37: 65-72. DOI: 10.1016/J.MICPATH.2004.04.006.
Moszak M, Pelczy Nska M, Wesoek A, Stenclik D, Bogda Nski P. 2023. Does gut microbiota affect the success of weight loss? Evidence and speculation. Nutrition 116: 112111. DOI: 10.1016/j.nut.2023.112111.
Nayebhashemi M, Enayati S, Zahmatkesh M, Madanchi H, Saberi S, Mostafavi E, Mirbzadeh Ardakani E, Azizi M, Khalaj V. 2023. Surface display of pancreatic lipase inhibitor peptides by engineered Saccharomyces boulardii: Potential as an anti-obesity probiotic. J Funct Foods 102: 105458. DOI: 10.1016/J.JFF.2023.105458.
Newson JP, Gaissmaier MS, McHugh SC, Hardt WD. 2023. Studying antibiotic persistence in vivo using the model organism Salmonella Typhimurium. Curr Opin Microbiol 70: 102224. DOI: 10.1016/j.mib.2022.102224.
Piatek, J, Sommermeyer H, Bernatek M, Ciechelska-Rybarczyk A, Oleskow B, Mikkelsen LS, Barken KB. 2019. Persistent Infection by Salmonella enterica serovar Typhimurium: Are synbiotics a therapeutic option? - a case report. Benef Microbes 10 (2): 211-217. DOI: 10.3920/BM2018.0080.
Segu H, Jalševac F, Ard A, Terra X, Blay MT. 2022. Intestinal morphometric changes induced by a western-style diet in wistar rats and GSPE counter-regulatory effect. Nutrients 14 (13): 2608. DOI: 10.3390/nu14132608.
Seyyedin S, Nazem MN. 2017. Histomorphometric study of the effect of methionine on small intestine parameters in rat: An applied histologic study. Folia Morphol 76 (4): 620-629. DOI: 10.5603/FM.a2017.0044.
Shang Q. 2022. Editorial: Next-generation prebiotics and probiotics: Current status and future development. Front Nutr 9 (3): 1023011. DOI: 10.3389/fnut.2022.1023011.
Sivixay S, Bai G, Tsuruta T, Nishino N. 2021. Cecum microbiota in rats fed soy, milk, meat, fish, and egg proteins with prebiotic oligosaccharides. AIMS Microbiol 7: 1. DOI: 10.3934/MICROBIOL.2021001.
Terciolo C, Dapoigny M, Andre F. 2019. Beneficial effects of Saccharomyces boulardii CNCM I-745 on clinical disorders associated with intestinal barrier disruption. Clin Exp Gastroenterol 12: 67-82. DOI: 10.2147/CEG.S181590.
Wang H, Zhang X, Wang S, Li H, Lu Z, Shi J, Xu Z. 2018. Mannan-oligosaccharide modulates the obesity and gut microbiota in high-fat diet-fed mice. Food Funct 9: 3916-3929. DOI: 10.1039/c8fo00209f.
Wang X, Biswas S, Paudyal N, Pan H, Li X. 2019. Antibiotic resistance in Salmonella Typhimurium isolates recovered from the food chain through national antimicrobial resistance monitoring system between 1996 and 2016. Front Microbiol 10: 985. DOI: 10.3389/fmicb.2019.00985.
Waturangi DE, Wiratama E, Sabatini A. 2019. Prevalence and molecular characterization of Salmonella enterica serovar Typhimurium from ice and beverages in Jakarta, Indonesia. BMC Res Notes 12: 45. DOI: 10.1186/s13104-019-4065-y.
Wulan R, Astuti RI, Rukayadi Y, Meryandini A. 2021. Evaluation of indigenous Pichia kudriavzevii from cocoa fermentation for a probiotic candidate. Biodiversitas 22 (3): 1317-1325. DOI: 10.13057/biodiv/d220331.
Xie S, Li Y, Zhao S, Lv Y, Yu Q. 2020. Salmonella infection induced intestinal crypt hyperplasia through Wnt/?-catenin pathway in chicken. Res Vet Sci 130: 179-183. DOI: 10.1016/j.rvsc.2020.03.008.
Yulianto AB, Lamid M, Lokapirnasari WP, Sherasiya A, Marbun TD, Khairullah AR, Kurniawan SC, Hasib A, Silaen OSM, Rehman S, Ayuti SR. 2024. Hematological and performance variables of male broiler chickens fed with Moringa oleifera extract and probiotic in drinking water. Trop Anim Sci J 47 (2): 215-224. DOI: 10.5398/tasj.2024.47.2.215.
Zeiner S, Dwyer B, Clegg S. 2012. FimA, FimF, and FimH are necessary for assembly of type 1 fimbriae on Salmonella enterica serovar Typhimurium. Infect Immun 80: 3289-3296. DOI: 10.1128/IAI.00331-1.
Zha L, Garrett S, Sun J. 2019. Salmonella infection in chronic inflammation and gastrointestinal cancer. Diseases 7: 28. DOI: 10.3390/diseases7010028.