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Effects of Probiotic Enterococcus faecium from Yak on the Intestinal Microflora and Metabolomics of Mice with Salmonella Infection

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Abstract

Salmonella spp. are pathogenic bacteria that cause diarrhea, abortion, and death in yak and severely harm livestock breeding. Therefore, it is vital to identify a probiotic that effectively antagonizes Salmonella. To the best of our knowledge, few prior studies have investigated the efficacy of Enterococcus faecium against Salmonella. Here, we evaluated the enteroprotective mechanism of E. faecium in a mouse Salmonella infection model using hematoxylin-eosin (H&E) staining, quantitative real-time polymerase chain reaction (Q-PCR) technology, microbial diversity sequencing, and metabonomics. Enterococcus faecium inhibited the proinflammatory cytokines IL-1β, IL-6, TNF-α, and IFN-γ and promoted the anti-inflammatory cytokine IL-10. The Firmicutes/Bacteroidota (F/B) ratio and the abundances of Firmicutes and Akkermansia were significantly higher in the E. faecium than in the Salmonella group. Metabonomics and microbial diversity sequencing disclosed five different metabolites with variable importance in the projection (VIP) > 3 that were characteristic of both the Salmonella and E. faecium groups. Combined omics revealed that Lactobacillus and Bacteroides were negatively and positively correlated, respectively, with cholic acid, while Desulfovibrio was positively correlated with lipids in both the control and Salmonella groups. Desulfovibrio was also positively correlated with lipids in both the Salmonella and E. faecium groups. Enterococcus faecium antagonizes Salmonella by normalizing the abundance of the intestinal microorganisms and modulating their metabolic pathways. Hence, it may efficaciously protect the host intestine against Salmonella infection.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Denkel LA, Horst SA, Rouf SF, Kitowski V, Böhm OM, Rhen M, Jäger T, Bange FC (2011) Methionine sulfoxide reductases are essential for virulence of Salmonella typhimurium. PloS one 6(11):e26974. https://doi.org/10.1371/journal.pone.0026974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Wasylnka JA, Moore MM (2002) Uptake of Aspergillus fumigatus Conidia by phagocytic and nonphagocytic cells in vitro: quantitation using strains expressing green fluorescent protein. Infect Immun 70(6):3156–3163. https://doi.org/10.1128/IAI.70.6.3156-3163.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Luan DQ, Chang GB, Sheng ZW, Zhang Y, Zhou W, Li ZZ, Liu Y, Chen GH (2012) Analysis of gene expression responses to a salmonella infection in rugao chicken intestine using GeneChips. Asian Australas J Anim Sci 25(2):278–285. https://doi.org/10.5713/ajas.2011.11174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Medina FA, de Almeida CJ, Dew E, Li J, Bonuccelli G, Williams TM, Cohen AW, Pestell RG, Frank PG, Tanowitz HB, Lisanti MP (2006) Caveolin-1-deficient mice show defects in innate immunity and inflammatory immune response during Salmonella enterica serovar Typhimurium infection. Infect Immun 74(12):6665–6674. https://doi.org/10.1128/IAI.00949-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Fu X, Feng L, Kong L, Li C, Zhao X, Li H, Cui P, Yan W, Zhai Y, Zhang L, Li H, Wang H, Yang X (2021) Prevalence, characterization, and pathogenicity of Salmonella enterica subspecies enterica serovar derby from yaks in the Aba tibetan autonomous prefecture, China. Animals 11(8):2397. https://doi.org/10.3390/ani11082397

    Article  PubMed  PubMed Central  Google Scholar 

  6. Frieri M, Kumar K, Boutin A (2017) Antibiotic resistance. J Infect Public Health 10(4):369–378. https://doi.org/10.1016/j.jiph.2016.08.007

    Article  PubMed  Google Scholar 

  7. Rao S, Ihara Y, Sukegawa S, Arakawa F, Fujimura T, Murakami H, Morimatsu F (2013) Characterization of probiotic properties of Enterococcus faecium NHRD IHARA isolated from porcine feces. Biosci Biotechnol Biochem 77(9):1967–1969. https://doi.org/10.1271/bbb.130252

    Article  CAS  PubMed  Google Scholar 

  8. Boirivant M, Strober W (2007) The mechanism of action of probiotics. Curr Opin Gastroenterol 23(6):679–692. https://doi.org/10.1097/MOG.0b013e3282f0cffc

    Article  PubMed  Google Scholar 

  9. Bednorz C, Guenther S, Oelgeschläger K, Kinnemann B, Pieper R, Hartmann S, Tedin K, Semmler T, Neumann K, Schierack P, Bethe A, Wieler LH (2013) Feeding the probiotic Enterococcus faecium strain NCIMB 10415 to piglets specifically reduces the number of Escherichia coli pathotypes that adhere to the gut mucosa. Appl Environ Microbiol 79(24):7896–7904. https://doi.org/10.1128/AEM.03138-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Szabó I, Wieler LH, Tedin K, Scharek-Tedin L, Taras D, Hensel A, Appel B, Nöckler K (2009) Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DT104 infection in a porcine animal infection model. Appl Environ Microbiol 75(9):2621–2628. https://doi.org/10.1128/AEM.01515-0811

    Article  PubMed  PubMed Central  Google Scholar 

  11. García-Galaz A, Pérez-Morales R, Díaz-Cinco M, Acedo-Félix E (2004) Resistance of Enterococcus strains isolated from pigs to gastrointestinal tract and antagonistic effect against Escherichia coli K88. Rev Latinoam Microbiol 46(1–2):5–11

    PubMed  Google Scholar 

  12. Daye M, Klepac-Ceraj V, Pajusalu M, Rowland S, Farrell-Sherman A, Beukes N, Tamura N, Fournier G, Bosak T (2019) Light-driven anaerobic microbial oxidation of manganese. Nature 576(7786):311–314. https://doi.org/10.1038/s41586-019-1804-0

    Article  CAS  PubMed  Google Scholar 

  13. Mo J, Sun L, Cheng J, Lu Y, Wei Y, Qin G, Liang J, Lan G (2021) Non-targeted metabolomics reveals metabolic characteristics of porcine atretic follicles. Front Vet Sci 8:679947. https://doi.org/10.3389/fvets.2021.679947

    Article  PubMed  PubMed Central  Google Scholar 

  14. Wang Q, Ou Y, Hu G, Wen C, Yue S, Chen C, Xu L, Xie J, Dai H, Xiao H, Zhang Y, Qi R (2020) Naringenin attenuates non-alcoholic fatty liver disease by down-regulating the NLRP3/NF-κB pathway in mice. Br J Pharmacol 177(8):1806–1821. https://doi.org/10.1111/bph.14938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Chen D, Liang J, Jiang C, Wu D, Huang B, Teng X, Tang Y (2023) Mitochondrion participated in effect mechanism of manganese poisoning on heat shock protein and ultrastructure of testes in chickens. Biol Trace Elem Res 201(3):1432–1441. https://doi.org/10.1007/s12011-022-03259-7

    Article  CAS  PubMed  Google Scholar 

  16. Cui Y, Xiao Q, Yuan Y, Zhuang Y, Hao W, Jiang J, Meng Q, Wei X (2023) 1,4-Naphthoquinone-coated black carbon, a kind of atmospheric fine particulate matter, affects macrophage fate: new insights into crosstalk between necroptosis and macrophage extracellular traps. Environ Sci Technol 57(15):6095–6107. https://doi.org/10.1021/acs.est.2c08791

    Article  CAS  PubMed  Google Scholar 

  17. Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England) 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560

    Article  CAS  PubMed  Google Scholar 

  18. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England) 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  PubMed  Google Scholar 

  19. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  20. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. https://doi.org/10.1128/AEM.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hamilton KA, Chen A, de-Graft Johnson E, Gitter A, Kozak S, Niquice C, Zimmer-Faust AG, Weir MH, Mitchell J, Gurian P (2018) Salmonella risks due to consumption of aquaculture-produced shrimp. Microb Risk Anal 9:22–32. https://doi.org/10.1016/j.mran.2018.04.001

    Article  PubMed  PubMed Central  Google Scholar 

  23. Smith GW, Alley ML, Foster DM, Smith F, Wileman BW (2014) Passive immunity stimulated by vaccination of dry cows with a Salmonella bacterial extract. J Vet Intern Med 28(5):1602–1605. https://doi.org/10.1111/jvim.12396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Akbari MR, Haghighi HR, Chambers JR, Brisbin J, Read LR, Sharif S (2008) Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica serovar typhimurium. Clin Vacc Immunol 15(11):1689–1693. https://doi.org/10.1128/CVI.00242-08

    Article  CAS  Google Scholar 

  25. Shen ZH, Zhu CX, Quan YS, Yang ZY, Wu S, Luo WW, Tan B, Wang XY (2018) Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J Gastroenterol 24(1):5–14. https://doi.org/10.3748/wjg.v24.i1.5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Stojanov S, Berlec A, Štrukelj B (2020) The Influence of Probiotics on the Firmicutes/Bacteroidetes Ratio in the Treatment of Obesity and Inflammatory Bowel disease. Microorganisms 8(11):1715. https://doi.org/10.3390/microorganisms8111715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hou Q, Qian Z, Wu P, Shen M, Li L, Zhao W (2020) 1-Deoxynojirimycin from mulberry leaves changes gut digestion and microbiota composition in geese. Poult Sci 99(11):5858–5866. https://doi.org/10.1016/j.psj.2020.07.048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Qiao J, Sun Z, Liang D, Li H (2020) Lactobacillus salivarius alleviates inflammation via NF-κB signaling in ETEC K88-induced IPEC-J2 cells. J Anim Sci Biotechnol 11:76. https://doi.org/10.1186/s40104-020-00488-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nomura K, Ishikawa D, Okahara K, Ito S, Haga K, Takahashi M, Arakawa A, Shibuya T, Osada T, Kuwahara-Arai K, Kirikae T, Nagahara A (2021) Bacteroidetes species are correlated with disease activity in ulcerative colitis. J Clin Med 10(8):1749. https://doi.org/10.3390/jcm10081749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lei J, Ran X, Guo M, Liu J, Yang F, Chen D (2023) Screening, identification, and probiotic properties of Bacillus Pumilus from Yak. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-023-10054-w. (Advance online publication)

    Article  PubMed  Google Scholar 

  31. Reuben RC, Roy PC, Sarkar SL, Rubayet Ul Alam ASM, Jahid IK (2020) Characterization and evaluation of lactic acid bacteria from indigenous raw milk for potential probiotic properties. J Dairy Sci 103(2):1223–1237. https://doi.org/10.3168/jds.2019-17092

    Article  CAS  PubMed  Google Scholar 

  32. Rho JH, Wright DP, Christie DL, Clinch K, Furneaux RH, Roberton AM (2005) A novel mechanism for desulfation of mucin: identification and cloning of a mucin-desulfating glycosidase (sulfoglycosidase) from Prevotella strain RS2. J Bacteriol 187(5):1543–1551. https://doi.org/10.1128/JB.187.5.1543-1551.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54(Pt 5):1469–1476. https://doi.org/10.1099/ijs.0.02873-0

    Article  CAS  PubMed  Google Scholar 

  34. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Müller M, de Vos WM (2011) Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2:166. https://doi.org/10.3389/fmicb.2011.00166

    Article  PubMed  PubMed Central  Google Scholar 

  35. Guo CF, Zhang LW, Han X, Yi HX, Li JY, Tuo YF, Zhang YC, Du M, Shan YJ, Yang L (2012) Screening for cholesterol-lowering probiotic based on deoxycholic acid removal pathway and studying its functional mechanisms in vitro. Anaerobe 18(5):516–522. https://doi.org/10.1016/j.anaerobe.2012.08.003

    Article  CAS  PubMed  Google Scholar 

  36. Brahe LK, Le Chatelier E, Prifti E, Pons N, Kennedy S, Hansen T, Pedersen O, Astrup A, Ehrlich SD, Larsen LH (2015) Specific gut microbiota features and metabolic markers in postmenopausal women with obesity. Nutr Diabetes 5(6):e159. https://doi.org/10.1038/nutd.2015.9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bian X, Wu W, Yang L, Lv L, Wang Q, Li Y, Ye J, Fang D, Wu J, Jiang X, Shi D, Li L (2019) Administration of Akkermansia muciniphila ameliorates dextran sulfate sodium-induced ulcerative colitis in mice. Front Microbiol 10:2259. https://doi.org/10.3389/fmicb.2019.02259

    Article  PubMed  PubMed Central  Google Scholar 

  38. Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, Harmsen HJM, Faber KN, Hermoso MA (2019) Short Chain Fatty Acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 10:277. https://doi.org/10.3389/fimmu.2019.00277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rose DJ, DeMeo MT, Keshavarzian A, Hamaker BR (2007) Influence of dietary fiber on inflammatory bowel disease and colon cancer: importance of fermentation pattern. Nutr Rev 65(2):51–62. https://doi.org/10.1111/j.1753-4887.2007.tb00282.x

    Article  PubMed  Google Scholar 

  40. Yamakawa H, Hagiwara E, Hayashi M, Katano T, Isomoto K, Otoshi R, Shintani R, Ikeda S, Tanaka K, Ogura T (2017) A case of relapsed lung abscess caused by Eubacterium brachy infection following an initial diagnosis of pulmonary actinomycosis. Respir Med Case Rep 22:171–174. https://doi.org/10.1016/j.rmcr.2017.08.013

    Article  PubMed  PubMed Central  Google Scholar 

  41. Guijas C, Montenegro-Burke JR, Warth B, Spilker ME, Siuzdak G (2018) Metabolomics activity screening for identifying metabolites that modulate phenotype. Nat Biotechnol 36(4):316–320. https://doi.org/10.1038/nbt.4101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mon KKZ, Zhu Y, Chanthavixay G, Kern C, Zhou H (2020) Integrative analysis of gut microbiome and metabolites revealed novel mechanisms of intestinal Salmonella carriage in chicken. Sci Rep 10(1):4809. https://doi.org/10.1038/s41598-020-60892-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Deatherage Kaiser BL, Li J, Sanford JA, Kim YM, Kronewitter SR, Jones MB, Peterson CT, Peterson SN, Frank BC, Purvine SO, Brown JN, Metz TO, Smith RD, Heffron F, Adkins JN (2013) A multi-omic view of host-pathogen-commensal interplay in Salmonella-mediated intestinal infection. PloS one 8(6):e67155. https://doi.org/10.1371/journal.pone.0067155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Larkin TA, Astheimer LB, Price WE (2009) Dietary combination of soy with a probiotic or prebiotic food significantly reduces total and LDL cholesterol in mildly hypercholesterolaemic subjects. Eur J Clin Nutr 63(2):238–245. https://doi.org/10.1038/sj.ejcn.1602910

    Article  CAS  PubMed  Google Scholar 

  45. Gao Y, Liu Y, Ma F, Sun M, Song Y, Xu D, Mu G, Tuo Y (2021) Lactobacillus plantarum Y44 alleviates oxidative stress by regulating gut microbiota and colonic barrier function in Balb/C mice with subcutaneous d-galactose injection. Food Funct 12(1):373–386. https://doi.org/10.1039/d0fo02794d

    Article  CAS  PubMed  Google Scholar 

  46. Xie Q, Zhao H, Li N, Su L, Xu X, Hong Z (2018) Protective effects of timosaponin BII on oxidative stress damage in PC12 cells based on metabolomics. Biomed Chromatogr BMC 32(e10):4321. https://doi.org/10.1002/bmc.4321

    Article  CAS  Google Scholar 

  47. Zhang S, Zhuang J, Yue G, Wang Y, Liu M, Zhang B, Du Z, Ma Q (2017) Lipidomics to investigate the pharmacologic mechanisms of ginkgo folium in the hyperuricemic rat model. J Chromatogr B Anal Technol Biomed Life Sci 1060:407–415. https://doi.org/10.1016/j.jchromb.2017.06.037

    Article  CAS  Google Scholar 

  48. Vance JE, Tasseva G (2013) Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Biochem Biophys Acta 1831(3):543–554. https://doi.org/10.1016/j.bbalip.2012.08.016

    Article  CAS  PubMed  Google Scholar 

  49. Meshram MA, Bhise UO, Makhal PN, Kaki VR (2021) Synthetically-tailored and nature-derived dual COX-2/5-LOX inhibitors: structural aspects and SAR. Eur J Med Chem 225:113804. https://doi.org/10.1016/j.ejmech.2021.113804

    Article  CAS  PubMed  Google Scholar 

  50. Liu Y, Gao S, Zhang Y, Zhang Z, Wang Q, Xu Y, Wei J (2022) Transcriptomics and metabolomics analyses reveal defensive responses and flavonoid biosynthesis of Dracaena cochinchinensis (Lour.) S. C. Chen under wound stress in natural conditions. Molecules 27(14):4514. https://doi.org/10.3390/molecules27144514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Feng Y, Lievens J, Jacobs F, Hoekstra M, Van Craeyveld E, Gordts SC, Snoeys J, De Geest B (2010) Hepatocyte-specific ABCA1 transfer increases HDL cholesterol but impairs HDL function and accelerates atherosclerosis. Cardiovasc Res 88(2):376–385. https://doi.org/10.1093/cvr/cvq204

    Article  CAS  PubMed  Google Scholar 

  52. Thurm C, Schraven B, Kahlfuss S (2021) ABC transporters in T cell-mediated physiological and pathological immune responses. Int J Mol Sci 22(17):9186. https://doi.org/10.3390/ijms22179186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cai J, Sun L, Gonzalez FJ (2022) Gut microbiota-derived bile acids in intestinal immunity, inflammation, and tumorigenesis. Cell Host Microbe 30(3):289–300. https://doi.org/10.1016/j.chom.2022.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Taranto MP, Perez-Martinez G, Font de Valdez G (2006) Effect of bile acid on the cell membrane functionality of lactic acid bacteria for oral administration. Res Microbiol 157(8):720–725. https://doi.org/10.1016/j.resmic.2006.04.002

    Article  CAS  PubMed  Google Scholar 

  55. Quinn RA, Melnik AV, Vrbanac A, Fu T, Patras KA, Christy MP, Bodai Z, Belda-Ferre P, Tripathi A, Chung LK, Downes M, Welch RD, Quinn M, Humphrey G, Panitchpakdi M, Weldon KC, Aksenov A, da Silva R, Avila-Pacheco J, Clish C, Dorrestein PC (2020) Global chemical effects of the microbiome include new bile-acid conjugations. Nature 579(7797):123–129. https://doi.org/10.1038/s41586-020-2047-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Leavitt WD, Flynn TM, Suess MK, Bradley AS (2016) Transhydrogenase and growth substrate influence lipid hydrogen isotope ratios in Desulfovibrio alaskensis G20. Front Microbiol 7:918. https://doi.org/10.3389/fmicb.2016.00918

    Article  PubMed  PubMed Central  Google Scholar 

  57. Li X, Wang H, Wang T, Zheng F, Wang H, Wang C (2019) Dietary wood pulp-derived sterols modulation of cholesterol metabolism and gut microbiota in high-fat-diet-fed hamsters. Food Funct 10(2):775–785. https://doi.org/10.1039/c8fo02271b

    Article  CAS  PubMed  Google Scholar 

  58. Mu G, Gao Y, Tuo Y, Li H, Zhang Y, Qian F, Jiang S (2018) Assessing and comparing antioxidant activities of lactobacilli strains by using different chemical and cellular antioxidant methods. J Dairy Sci 101(12):10792–10806. https://doi.org/10.3168/jds.2018-14989

    Article  CAS  PubMed  Google Scholar 

  59. Liu Y, Gao Y, Ma F, Sun M, Mu G, Tuo Y (2020) The ameliorative effect of Lactobacillus plantarum Y44 oral administration on inflammation and lipid metabolism in obese mice fed with a high fat diet. Food Funct 11(6):5024–5039. https://doi.org/10.1039/d0fo00439a

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the Natural Science Foundation of Sichuan Province (No. 22NSFSC3161), the National Natural Science Foundation of China (No. 32202871), and the Innovation and Entrepreneurship Training Project of Southwest Minzu University (No. 320022230051).

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Xuan Ran and Xueer Xie summarized and analyzed the experimental data and wrote the manuscript. Xianhui Li and Jiangyin Lei generated the experimental data. Dechun Chen supervised the progress of the experiments and guided the writing of the manuscript. Falong Yang reviewed the manuscript.

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Correspondence to Dechun Chen.

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Ran, X., Li, X., Xie, X. et al. Effects of Probiotic Enterococcus faecium from Yak on the Intestinal Microflora and Metabolomics of Mice with Salmonella Infection. Probiotics & Antimicro. Prot. (2023). https://doi.org/10.1007/s12602-023-10102-5

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