Multispecies probiotics alter fecal short-chain fatty acids and lactate levels in weaned pigs by modulating gut microbiota |
Oh, Ju Kyoung
(Department of Microbiology, Tumor and Cell Biology, Centre for Translational Microbiome Research (CTMR), Karolinska Institute)
Vasquez, Robie (Department of Animal Resources Science, Dankook University) Kim, Sang Hoon (Department of Animal Resources Science, Dankook University) Hwang, In-Chan (Department of Animal Resources Science, Dankook University) Song, Ji Hoon (Department of Animal Resources Science, Dankook University) Park, Jae Hong (Department of Animal Resources Science, Dankook University) Kim, In Ho (Department of Animal Resources Science, Dankook University) Kang, Dae-Kyung (Department of Animal Resources Science, Dankook University) |
1 | De Baere S, Eeckhaut V, Steppe M, De Maesschalck C, De Backer P, Van Immerseel F, et al. Development of a HPLC-UV method for the quantitative determination of four short-chain fatty acids and lactic acid produced by intestinal bacteria during in vitro fermentation. J Pharm Biomed Anal. 2013;80:107-15. https://doi.org/10.1016/j.jpba.2013.02.032 DOI |
2 | Slizewska K, Markowiak-Kopec P, Zbikowski A, Szeleszczuk P. The effect of synbiotic preparations on the intestinal microbiota and her metabolism in broiler chickens. Sci Rep. 2020;10:4281. https://doi.org/10.1038/s41598-020-61256-z DOI |
3 | Wang Y, Dilidaxi D, Wu Y, Sailike J, Sun X, Nabi X. Composite probiotics alleviate type 2 diabetes by regulating intestinal microbiota and inducing GLP-1 secretion in db/db mice. Biomed Pharmacother. 2020;125:109914. https://doi.org/10.1016/j.biopha.2020.109914 DOI |
4 | Joseph N, Vasodavan K, Saipudin NA, Yusof BNM, Kumar S, Nordin SA. Gut microbiota and short-chain fatty acids (SCFAs) profiles of normal and overweight school children in Selangor after probiotics administration. J Funct Foods. 2019;57:103-11. https://doi.org/10.1016/j.jff.2019.03.042 DOI |
5 | Lu X, Zhang M, Zhao L, Ge K, Wang Z, Jun L, et al. Growth performance and post-weaning diarrhea in piglets fed a diet supplemented with probiotic complexes. J Microbiol Biotechnol. 2018;28:1791-9. https://doi.org/10.4014/jmb.1807.07026 DOI |
6 | Balasubramanian B, Lee SI, Kim IH. Inclusion of dietary multi-species probiotic on growth performance, nutrient digestibility, meat quality traits, faecal microbiota and diarrhoea score in growing-finishing pigs. Ital J Anim Sci. 2018;17:100-6. https://doi.org/10.1080/1828051X.2017.1340097 DOI |
7 | Wang K, Chen G, Cao G, Xu Y, Wang Y, Yang C. Effects of Clostridium butyricum and Enterococcus faecalis on growth performance, intestinal structure, and inflammation in lipopolysaccharide-challenged weaned piglets. J Anim Sci. 2019;97:4140-51. https://doi.org/10.1093/jas/skz235 DOI |
8 | Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67:1613-7. https://doi.org/10.1099/ijsem.0.001755 DOI |
9 | Wang C, Li W, Wang H, Ma Y, Zhao X, Zhang X, et al. Saccharomyces boulardii alleviates ulcerative colitis carcinogenesis in mice by reducing TNF-α and IL-6 levels and functions and by rebalancing intestinal microbiota. BMC Microbiol. 2019;19:246. https://doi.org/10.1186/s12866-019-1610-8 DOI |
10 | Deda O, Chatziioannou AC, Fasoula S, Palachanis D, Raikos N, Theodoridis GA, et al. Sample preparation optimization in fecal metabolic profiling. J Chromatogr B. 2017;1047:115-23. https://doi.org/10.1016/j.jchromb.2016.06.047 DOI |
11 | Sun Y, O'Riordan MXD. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv Appl Microbiol. 2013;85:93-118. https://doi.org/10.1016/B978-0-12-407672-3.00003-4 DOI |
12 | Li F, Wang M, Wang J, Li R, Zhang Y. Alterations to the gut microbiota and their correlation with inflammatory factors in chronic kidney disease. Front Cell Infect Microbiol. 2019;9:206. https://doi.org/10.3389/fcimb.2019.00206 DOI |
13 | Kang X, Zhan L, Lu X, Song J, Zhong Y, Wang Y, et al. Characteristics of gastric microbiota in GK rats with spontaneous diabetes: a comparative study. Diabetes Metab Syndr Obes. 2020;13:1435-47. https://doi.org/10.2147/DMSO.S242698 DOI |
14 | Tamanai-Shacoori Z, Smida I, Bousarghin L, Loreal O, Meuric V, Fong SB, et al. Roseburia spp.: a marker of health? Future Microbiol. 2017;12:157-70. https://doi.org/10.2217/fmb2016-0130 DOI |
15 | Hua X, Zhu J, Yang T, Guo M, Li Q, Chen J, et al. The gut microbiota and associated metabolites are altered in sleep disorder of children with autism spectrum disorders. Front Psychiatry. 2020;11:855. https://doi.org/10.3389/fpsyt.2020.00855 DOI |
16 | Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT. Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr. 2006;96:570-7. https://doi.org/10.1079/BJN20061853 DOI |
17 | Zhuang M, Shang W, Ma Q, Strappe P, Zhou Z. Abundance of probiotics and butyrate-production microbiome manages constipation via short-chain fatty acids production and hormones secretion. Mol Nutr Food Res. 2019;63:1801187. https://doi.org/10.1002/mnfr.201801187 DOI |
18 | Pi Y, Hu J, Bai Y, Wang Z, Wu Y, Ye H, et al. Effects of dietary fibers with different physicochemical properties on fermentation kinetics and microbial composition by fecal inoculum from lactating sows in vitro. J Sci Food Agric. 2021;101:907-17. https://doi.org/10.1002/jsfa.10698 DOI |
19 | Feng G, Mikkelsen D, Hoedt EC, Williams BA, Flanagan BM, Morrison M, et al. In vitro fermentation outcomes of arabinoxylan and galactoxyloglucan depend on fecal inoculum more than substrate chemistry. Food Funct. 2020;11:7892-904. https://doi.org/10.1039/D0FO01103G DOI |
20 | Moser AM, Spindelboeck W, Halwachs B, Strohmaier H, Kump P, Gorkiewicz G, et al. Effects of an oral synbiotic on the gastrointestinal immune system and microbiota in patients with diarrhea-predominant irritable bowel syndrome. Eur J Nutr. 2019;58:2767-78. https://doi.org/10.1007/s00394-018-1826-7 DOI |
21 | Rios-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilan CG, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185. https://doi.org/10.3389/fmicb.2016.00185 DOI |
22 | Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163:1360-74. https://doi.org/10.1016/j.cell.2015.11.004 DOI |
23 | Gomez-Garcia M, Sol C, de Nova PJG, Puyalto M, Mesas L, Puente H, et al. Antimicrobial activity of a selection of organic acids, their salts and essential oils against swine enteropathogenic bacteria. Porcine Health Manag. 2019;5:32. https://doi.org/10.1186/s40813-019-0139-4 DOI |
24 | Schautteet K, Vanrompay D. Chlamydiaceae infections in pig. Vet Res. 2011;42:29. https://doi.org/10.1186/1297-9716-42-29 DOI |
25 | Kraatz M, Wallace RJ, Svensson L. Olsenella umbonata sp. nov., a microaerotolerant anaerobic lactic acid bacterium from the sheep rumen and pig jejunum, and emended descriptions of Olsenella, Olsenella uli and Olsenella profusa. Int J Syst Evol Microbiol. 2011;61:795-803. https://doi.org/10.1099/ijs.0.022954-0 DOI |
26 | Li W, Zhang K, Yang H. Pectin alleviates high fat (lard) diet-induced nonalcoholic fatty liver disease in mice: possible role of short-chain fatty acids and gut microbiota regulated by pectin. J Agric Food Chem. 2018;66:8015-25. https://doi.org/10.1021/acs.jafc.8b02979 DOI |
27 | Mair C, Plitzner C, Domig KJ, Schedle K, Windisch W. Impact of inulin and a multispecies probiotic formulation on performance, microbial ecology and concomitant fermentation patterns in newly weaned piglets. J Anim Physiol Anim Nutr. 2010;94:e164-77. https://doi.org/10.1111/j.1439-0396.2010.01000.x DOI |
28 | Nagata S, Chiba Y, Wang C, Yamashiro Y. The effects of the Lactobacillus casei strain on obesity in children: a pilot study. Benefic Microbes. 2017;8:535-43. https://doi.org/10.3920/BM2016.0170 DOI |
29 | Chen L, Zhang L, Wang W, Qiu W, Liu L, Ning A, et al. Polysaccharides isolated from Cordyceps sinensis contribute to the progression of NASH by modifying the gut microbiota in mice fed a high-fat diet. PLOS ONE. 2020;15:e0232972. https://doi.org/10.1371/journal.pone.0232972 DOI |
30 | Buckel W, Barker HA. Two pathways of glutamate fermentation by anaerobic bacteria. J Bacteriol. 1974;117:1248-60. https://doi.org/10.1128/jb.117.3.1248-1260.1974 DOI |
31 | Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity. 2013;5:627-40. https://doi.org/10.3390/d5030627 DOI |
32 | Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498-504. https://doi.org/10.1101/gr.1239303 DOI |
33 | Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814-21. https://doi.org/10.1038/nbt.2676 DOI |
34 | Huang C, Qiao S, Li D, Piao X, Ren J. Effects of Lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian-Australas J Anim Sci. 2004;17:401-9. https://doi.org/10.5713/ajas.2004.401 DOI |
35 | Jaworski NW, Owusu-Asiedu A, Walsh MC, McCann JC, Loor JJ, Stein HH. Effects of a 3 strain Bacillus-based direct-fed microbial and dietary fiber concentration on growth performance and expression of genes related to absorption and metabolism of volatile fatty acids in weanling pigs. J Anim Sci. 2017;95:308-19. https://doi.org/10.2527/jas.2016.0557 DOI |
36 | Markowiak-Kopec P, Slizewska K. The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients. 2020;12:1107. https://doi.org/10.3390/nu12041107 DOI |
37 | Alcon-Giner C, Dalby MJ, Caim S, Ketskemety J, Shaw A, Sim K, et al. Microbiota supplementation with Bifidobacterium and Lactobacillus modifies the preterm infant gut microbiota and metabolome: an observational study. Cell Rep Med. 2020;1:100077. https://doi.org/10.1016/j.xcrm.2020.100077 DOI |
38 | Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11:577-91. https://doi.org/10.1038/nrendo.2015.128 DOI |
39 | Jha R, Leterme P. Feed ingredients differing in fermentable fibre and indigestible protein content affect fermentation metabolites and faecal nitrogen excretion in growing pigs. Animal. 2012;6:603-11. https://doi.org/10.1017/S1751731111001844 DOI |
40 | R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. |
41 | Tsugawa H, Kabe Y, Kanai A, Sugiura Y, Hida S, Taniguchi S, et al. Short-chain fatty acids bind to apoptosis-associated speck-like protein to activate inflammasome complex to prevent Salmonella infection. PLOS Biol. 2020;18:e3000813. https://doi.org/10.1371/journal.pbio.3000813 DOI |
42 | Basen M, Kurrer SE. A close look at pentose metabolism of gut bacteria. FEBS J. 2021;288:1804-8. https://doi.org/10.1111/febs.15575 DOI |
43 | Tanca A, Abbondio M, Palomba A, Fraumene C, Manghina V, Cucca F, et al. Potential and active functions in the gut microbiota of a healthy human cohort. Microbiome. 2017;5:79. https://doi.org/10.1186/s40168-017-0293-3 DOI |
44 | Dai ZL, Wu G, Zhu WY. Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front Biosci. 2011;16:1768-86. https://doi.org/10.2741/3820 DOI |
45 | Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123-4. https://doi.org/10.1093/bioinformatics/btu494 DOI |
46 | Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-6. https://doi.org/10.1038/nmeth.f.303 DOI |
47 | Oh JK, Amoranto MBC, Oh NS, Kim S, Lee JY, Oh YN, et al. Synergistic effect of Lactobacillus gasseri and Cudrania tricuspidata on the modulation of body weight and gut microbiota structure in diet-induced obese mice. Appl Microbiol Biotechnol. 2020;104:6273-85. https://doi.org/10.1007/s00253-020-10634-8 DOI |
48 | Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. https://doi.org/10.1186/gb2011-12-6-r60 DOI |
49 | Lahteinen T, Rinttila T, Koort JMK, Kant R, Levonen K, Jakava-Viljanen M, et al. Effect of a multispecies Lactobacillus formulation as a feeding supplement on the performance and immune function of piglets. Livest Sci. 2015;180:164-71. https://doi.org/10.1016/j.livsci.2015.07.016 DOI |
50 | Shimizu H, Masujima Y, Ushiroda C, Mizushima R, Taira S, Ohue-Kitano R, et al. Dietary short-chain fatty acid intake improves the hepatic metabolic condition via FFAR3. Sci Rep. 2019;9:16574. https://doi.org/10.1038/S41598-019-53242-x DOI |
51 | Zhong H, Abdullah, Deng L, Zhao M, Tang J, Liu T, et al. Probiotic-fermented blueberry juice prevents obesity and hyperglycemia in high fat diet-fed mice in association with modulating the gut microbiota. Food Funct. 2020;11:9192-207. https://doi.org/10.1039/D0FO00334D DOI |
52 | Walsh CJ, Healy S, O'Toole PW, Murphy EF, Cotter PD. The probiotic L. casei LC-XCAL™ improves metabolic health in a diet-induced obesity mouse model without altering the microbiome. Gut Microbes. 2020;12:1747330. https://doi.org/10.1080/19490976.2020.1747330 DOI |
53 | Cao GT, Zhan XA, Zhang LL, Zeng XF, Chen AG, Yang CM. Modulation of broilers' caecal microflora and metabolites in response to a potential probiotic Bacillus amyloliquefaciens. J Anim Physiol Anim Nutr. 2018;102:e909-17. https://doi.org/10.1111/jpn.12856 DOI |
54 | Creus E, Perez JF, Peralta B, Baucells F, Mateu E. Effect of acidified feed on the prevalence of Salmonella in market-age pigs. Zoonoses Public Health. 2007;54:314-9. https://doi.org/10.1111/j.1863-2378.2007.01069.x DOI |
55 | Li G, Xie C, Lu S, Nichols RG, Tian Y, Li L, et al. Intermittent fasting promotes white adipose browning and decreases obesity by shaping the gut microbiota. Cell Metab. 2017;26:672-85.https://doi.org/10.1016/j.cmet.2017.08.019 DOI |
56 | Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915-23. https://doi.org/10.1079/BJN20041150 DOI |
57 | Garcia-Mantrana I, Selma-Royo M, Alcantara C, Collado MC. Shifts on gut microbiota associated to mediterranean diet adherence and specific dietary intakes on general adult population. Front Microbiol. 2018;9:890. https://doi.org/10.3389/fmicb.2018.00890 DOI |
58 | Krznaric Z, Vranesic Bender D, Mestrovic T. The Mediterranean diet and its association with selected gut bacteria. Curr Opin Clin Nutr Metab Care. 2019;22:401-6. https://doi.org/10.1097/MCO.0000000000000587 DOI |
59 | Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology. 2014;146:1513-24. https://doi.org/10.1053/j.gastro.2014.01.020 DOI |
60 | Ley RE. Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol. 2016;13:69-70. https://doi.org/10.1038/nrgastro.2016.4 DOI |
61 | Neveling DP, van Emmenes L, Ahire JJ, Pieterse E, Smith C, Dicks LMT. Effect of a multi-species probiotic on the colonisation of Salmonella in broilers. Probiotics Antimicrob Proteins. 2020;12:896-905. https://doi.org/10.1007/s12602-019-09593-y DOI |
62 | Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017;19:29-41. https://doi.org/10.1111/1462-2920.13589 DOI |
63 | Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016;7:189-200. https://doi.org/10.1080/19490976.2015.1134082 DOI |
64 | Granado-Serrano AB, Martin-Gari M, Sanchez V, Riart Solans M, Berdun R, Ludwig IA, et al. Faecal bacterial and short-chain fatty acids signature in hypercholesterolemia. Sci Rep. 2019;9:1772.https://doi.org/10.1038/s41598-019-38874-3 DOI |
65 | Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc Nutr Soc. 2003;62:67-72. https://doi.org/10.1079/PNS2002207 DOI |
66 | Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of shortchain fatty acids in health and disease. In: Alt FW, editor. Advances in immunology. Amsterdam: Academic Press; 2014. p. 91-119. |
67 | Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol. 2006;72:3593-9. https://doi.org/10.1128/AEM.72.5.3593-3599.2006 DOI |
68 | De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L, et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. 2016;65:1812-21. https://doi.org/10.1136/gutjnl-2015-309957 DOI |
69 | Hedemann MS, Bach Knudsen KE. Resistant starch for weaning pigs: effect on concentration of short chain fatty acids in digesta and intestinal morphology. Livest Sci. 2007;108:175-7. https://doi.org/10.1016/j.livsci.2007.01.045 DOI |
70 | De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 2010;107:14691-6. https://doi.org/10.1073/pnas.1005963107 DOI |
71 | Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5:14. https://doi.org/10.1186/s40168-016-0222-x DOI |
72 | Hu R, Zeng F, Wu L, Wan X, Chen Y, Zhang J, et al. Fermented carrot juice attenuates type 2 diabetes by mediating gut microbiota in rats. Food Funct. 2019;10:2935-46. https://doi.org/10.1039/C9FO00475K DOI |
73 | Li A, Ni W, Zhang Q, Li Y, Zhang X, Wu H, et al. Effect of cinnamon essential oil on gut microbiota in the mouse model of dextran sodium sulfate-induced colitis. Microbiol Immunol. 2020;64:23-32. https://doi.org/10.1111/1348-0421.12749 DOI |
74 | Michail S, Lin M, Frey MR, Fanter R, Paliy O, Hilbush B, et al. Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease. FEMS Microbiol Ecol. 2015;91:1-9. https://doi.org/10.1093/femsec/fiu002 DOI |
75 | Valeriano VDV, Balolong MP, Kang DK. Probiotic roles of Lactobacillus sp. in swine: insights from gut microbiota. J Appl Microbiol. 2017;122:554-67. https://doi.org/10.1111/jam.13364 DOI |