863
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Faecal metabolome responses to an altered dietary protein:carbohydrate ratio in adult dogs

, , , , &
Pages 1-10 | Received 03 Jul 2023, Accepted 17 Oct 2023, Published online: 28 Oct 2023

References

  • Andre A, Leriche I, Chaix G, Thorin C, Burger M, Nguyen P. 2017. Recovery of insulin sensitivity and optimal body composition after rapid weight loss in obese dogs fed a high-protein medium-carbohydrate diet. J Anim Physiol Anim Nutr. 101 Suppl 1(S1):21–30. doi: 10.1111/jpn.12744.
  • Apper E, Privet L, Taminiau B, Le Bourgot C, Svilar L, Martin JC, Diez M. 2020. Relationships between gut microbiota, metabolome, body weight, and glucose homeostasis of obese dogs fed with diets differing in prebiotic and protein content. Microorganisms. 8(4):513. doi: 10.3390/microorganisms8040513.
  • Athenstaedt K, Daum G. 2006. The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci. 63(12):1355–1369. doi: 10.1007/s00018-006-6016-8.
  • Bentinger M, Tekle M, Dallner G. 2010. Coenzyme Q–biosynthesis and functions. Biochem Biophys Res Commun. 396(1):74–79. doi: 10.1016/j.bbrc.2010.02.147.
  • Bermingham EN, Maclean P, Thomas DG, Cave NJ, Young W. 2017. Key bacterial families (Clostridiaceae, Erysipelotri­chaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs. PeerJ. 5:e3019. doi: 10.7717/peerj.3019.
  • Bermudez Sanchez S, Pilla R, Sarawichitr B, Gramenzi A, Marsilio F, Steiner JM, Lidbury JA, Woods GRT, Suchodolski JS, German AJ, et al. 2021. Untargeted fecal metabolome analysis in obese dogs after weight loss achieved by feeding a high-fiber-high-protein diet. Metabolomics. 17(7):66. doi: 10.1007/s11306-021-01815-1.
  • Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 73(4):1073–1078. doi: 10.1128/AEM.02340-06.
  • Ephraim E, Cochrane CY, Jewell DE. 2020. Varying protein levels influence metabolomics and the gut microbiome in healthy adult dogs. Toxins. 12(8):517. doi: 10.3390/toxins12080517.
  • Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 104(34):13780–13785. doi: 10.1073/pnas.0706625104.
  • Galler AI, Suchodolski JS, Steiner JM, Sung CH, Hittmair KM, Richter B, Burgener IA. 2022. Microbial dysbiosis and fecal metabolomic perturbations in Yorkshire Terriers with chronic enteropathy. Sci Rep. 12(1):12977. doi: 10.1038/s41598-022-17244-6.
  • Garavito MF, Narváez-Ortiz HY, Zimmermann BH. 2015. Pyrimidine metabolism: dynamic and versatile pathways in pathogens and cellular development. J Genet Genomics. 42(5):195–205. doi: 10.1016/j.jgg.2015.04.004.
  • German AJ, Holden SL, Bissot T, Morris PJ, Biourge V. 2010. A high protein high fibre diet improves weight loss in obese dogs. Vet J. 183(3):294–297. doi: 10.1016/j.tvjl.2008.12.004.
  • Guard BC, Barr JW, Reddivari L, Klemashevich C, Jayaraman A, Steiner JM, Vanamala J, Suchodolski JS. 2015. Characterization of microbial dysbiosis and metabolomic changes in dogs with acute diarrhea. PLOS One. 10(5):e0127259. doi: 10.1371/journal.pone.0127259.
  • Guo Z, Zhang J, Wang Z, Ang KY, Huang S, Hou Q, Su X, Qiao J, Zheng Y, Wang L, et al. 2016. Intestinal microbiota distinguish gout patients from healthy humans. Sci Rep. 6:20602. doi: 10.1038/srep20602.
  • Han S, Van Treuren W, Fischer CR, Merrill BD, DeFelice BC, Sanchez JM, Higginbottom SK, Guthrie L, Fall LA, Dodd D, et al. 2021. A metabolomics pipeline for the mechanistic interrogation of the gut microbiome. Nature. 595(7867):415–420. doi: 10.1038/s41586-021-03707-9.
  • Hang I, Heilmann RM, Grützner N, Suchodolski JS, Steiner JM, Atroshi F, Sankari S, Kettunen A, de Vos WM, Zentek J, et al. 2013. Impact of diets with a high content of greaves-meal protein or carbohydrates on faecal characteristics, volatile fatty acids and faecal calprotectin concentrations in healthy dogs. BMC Vet Res. 9(1):201. doi: 10.1186/1746-6148-9-201.
  • Hang I, Rinttila T, Zentek J, Kettunen A, Alaja S, Apajalahti J, Harmoinen J, de Vos WM, Spillmann T. 2012. Effect of high contents of dietary animal-derived protein or carbohydrates on canine faecal microbiota. BMC Vet Res. 8(1):90. doi: 10.1186/1746-6148-8-90.
  • He M. 2006. Pipecolic acid in microbes: biosynthetic routes and enzymes. J Ind Microbiol Biotechnol. 33(6):401–407. doi: 10.1007/s10295-006-0078-3.
  • Herstad KMV, Gajardo K, Bakke AM, Moe L, Ludvigsen J, Rudi K, Rud I, Sekelja M, Skancke E. 2017. A diet change from dry food to beef induces reversible changes on the faecal microbiota in healthy, adult client-owned dogs. BMC Vet Res. 13(1):147. doi: 10.1186/s12917-017-1073-9.
  • Jackson MI, Jewell DE. 2019. Balance of saccharolysis and proteolysis underpins improvements in stool quality induced by adding a fiber bundle containing bound polyphenols to either hydrolyzed meat or grain-rich foods. Gut Microbes. 10(3):298–320. doi: 10.1080/19490976.2018.1526580.
  • Jones DA. 2009. Rosacea, reactive oxygen species, and azelaic acid. J Clin Aesthet Dermatol. 2:26.
  • Kamleh MA, Ebbels TM, Spagou K, Masson P, Want EJ. 2012. Optimizing the use of quality control samples for signal drift correction in large-scale urine metabolic profiling studies. Anal Chem. 84(6):2670–2677. doi: 10.1021/ac202733q.
  • Kim E, Kim DB, Park JY. 2016. Changes of mouse gut microbiota diversity and composition by modulating dietary protein and carbohydrate contents: a pilot study. Prev Nutr Food Sci. 21(1):57–61. doi: 10.3746/pnf.2016.21.1.57.
  • Kim H-J, Kim JH, Noh S, Hur HJ, Sung MJ, Hwang J-T, Park JH, Yang HJ, Kim M-S, Kwon DY, et al. 2011. Metabolomic analysis of livers and serum from high-fat diet induced obese mice. J Proteome Res. 10(2):722–731. doi: 10.1021/pr100892r.
  • Lawrence YA, Bishop MA, Honneffer JB, Cook AK, Rodrigues-Hoffmann A, Steiner JM, Suchodolski JS, Lidbury JA. 2019. Untargeted metabolomic profiling of serum from dogs with chronic hepatic disease. J Vet Intern Med. 33(3):1344–1352. doi: 10.1111/jvim.15479.
  • Leonardi R, Jackowski S. 2007. Biosynthesis of pantothenic acid and coenzyme A. EcoSal Plus. 2(2):11–28. doi: 10.1128/ecosalplus.3.6.3.4.
  • Li M, Liu B, Li R, Yang P, Leng P, Huang Y. 2023. Exploration of the link between gut microbiota and purinergic signalling. Purinergic Signal. 19(1):315–327. doi: 10.1007/s11302-022-09891-1.
  • Li Q, Laflamme DP, Bauer JE. 2020. Serum untargeted metabolomic changes in response to diet intervention in dogs with preclinical myxomatous mitral valve disease. PLOS One. 15(6):e0234404. doi: 10.1371/journal.pone.0234404.
  • Li X, Zhang B, Hu Y, Zhao Y. 2021. New insights into gut-bacteria-derived indole and its derivatives in intestinal and liver diseases. Front Pharmacol. 12:769501. doi: 10.3389/fphar.2021.769501.
  • Lin R, Liu W, Piao M, Zhu H. 2017. A review of the relationship between the gut microbiota and amino acid metabolism. Amino Acids. 49(12):2083–2090. doi: 10.1007/s00726-017-2493-3.
  • Liu Y, Hou Y, Wang G, Zheng X, Hao H. 2020. Gut microbial metabolites of aromatic amino acids as signals in host–microbe interplay. Trends Endocrinol Metab. 31(11):818–834. doi: 10.1016/j.tem.2020.02.012.
  • Lyu Y, Liu D, Nguyen P, Peters I, Heilmann RM, Fievez V, Hemeryck LY, Hesta M. 2022. Differences in metabolic profiles of healthy dogs fed a high-fat vs. a high-starch diet. Front Vet Sci. 9:801863. doi: 10.3389/fvets.2022.801863.
  • Ma L, Ni Y, Wang Z, Tu W, Ni L, Zhuge F, Zheng A, Hu L, Zhao Y, Zheng L, et al. 2020. Spermidine improves gut barrier integrity and gut microbiota function in diet-induced obese mice. Gut Microbes. 12(1):1–19. doi: 10.1080/19490976.2020.1832857.
  • Makarov MV, Trammell SA, Migaud ME. 2019. The chemistry of the vitamin B3 metabolome. Biochem Soc Trans. 47(1):131–147. doi: 10.1042/BST20180420.
  • Martin SA. 1996. Hexose phosphorylation by the ruminal bacterium Selenomonas ruminantium. J Dairy Sci. 79(4):550–556. doi: 10.3168/jds.S0022-0302(96)76399-3.
  • Matsumoto M, Benno Y. 2007. The relationship between microbiota and polyamine concentration in the human intestine: a pilot study. Microbiol Immunol. 51(1):25–35. doi: 10.1111/j.1348-0421.2007.tb03887.x.
  • Meganathan R. 2001. Ubiquinone biosynthesis in microorganisms. FEMS Microbiol Lett. 203(2):131–139. doi: 10.1111/j.1574-6968.2001.tb10831.x.
  • Mels C, Jansen van Rensburg P, van der Westhuizen FH, Pretorius PJ, Erasmus E. 2011. Increased excretion of c4-carnitine species after a therapeutic acetylsalicylic acid dose: evidence for an inhibitory effect on short-chain fatty acid metabolism. ISRN Pharmacol. 2011:851870. doi: 10.5402/2011/851870.
  • Muthulakshmi S, Saravanan R. 2013. Protective effects of azelaic acid against high-fat diet-induced oxidative stress in liver, kidney and heart of C57BL/6J mice. Mol Cell Biochem. 377(1–2):23–33. doi: 10.1007/s11010-013-1566-1.
  • National Research Council. 2006. Energy. In: Nutrient requirements of dogs and cats. Washington (DC): National Academies; p. 28–48.
  • Pinna C, Vecchiato CG, Bolduan C, Grandi M, Stefanelli C, Windisch W, Zaghini G, Biagi G. 2018. Influence of dietary protein and fructooligosaccharides on fecal fermentative end-products, fecal bacterial populations and apparent total tract digestibility in dogs. BMC Vet Res. 14(1):106. doi: 10.1186/s12917-018-1436-x.
  • Plekhova V, De Paepe E, Van Renterghem K, Van Winckel M, Hemeryck LY, Vanhaecke L. 2021. Disparities in the gut metabolome of post-operative Hirschsprung’s disease patients. Sci Rep. 11(1):16167. doi: 10.1038/s41598-021-95589-0.
  • Qi Y, Jiang C, Cheng J, Krausz KW, Li T, Ferrell JM, Gonzalez FJ, Chiang JYL. 2015. Bile acid signaling in lipid metabolism: metabolomic and lipidomic analysis of lipid and bile acid markers linked to anti-obesity and anti-diabetes in mice. Biochim Biophys Acta. 1851(1):19–29. doi: 10.1016/j.bbalip.2014.04.008.
  • Reaves ML, Young BD, Hosios AM, Xu YF, Rabinowitz JD. 2013. Pyrimidine homeostasis is accomplished by directed overflow metabolism. Nature. 500(7461):237–241. doi: 10.1038/nature12445.
  • Rolland F, Wanke V, Cauwenberg L, Ma P, Boles E, Vanoni M, et al. 2001. The role of hexose transport and phosphorylation in cAMP signalling in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 1:33–45.
  • Schmidt M, Unterer S, Suchodolski JS, Honneffer JB, Guard BC, Lidbury JA, Steiner JM, Fritz J, Kölle P. 2018. The fecal microbiome and metabolome differs between dogs fed bones and raw food (BARF) diets and dogs fed commercial diets. PLOS One. 13(8):e0201279. doi: 10.1371/journal.pone.0201279.
  • Schymanski EL, Jeon J, Gulde R, Fenner K, Ruff M, Singer HP, Hollender J. 2014. Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ Sci Technol. 48(4):2097–2098. doi: 10.1021/es5002105.
  • Soto-Martin EC, Warnke I, Farquharson FM, Christodoulou M, Horgan G, Derrien M, Faurie J-M, Flint HJ, Duncan SH, Louis P, et al. 2020. Vitamin biosynthesis by human gut butyrate-producing bacteria and cross-feeding in synthetic microbial communities. mBio. 11(4):e00886-20. doi: 10.1128/mBio.00886-20.
  • Szymańska E, Saccenti E, Smilde AK, Westerhuis JA. 2012. Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies. Metabolomics. 8(Suppl 1):3–16. doi: 10.1007/s11306-011-0330-3.
  • Todea A, Deganutti C, Spennato M, Asaro F, Zingone G, Milizia T, Gardossi L. 2021. Azelaic acid: a bio-based building block for biodegradable polymers. Polymers. 13(23):4091. doi: 10.3390/polym13234091.
  • Van De Velde H,Janssens GPJ,Rochus K,Duchateau L,Scharek-Tedin L,Zentek J,Nguyen P,Cox E,Buyse J,Biourge V, et al. 2013. Proliferation capacity of T-lymphocytes is affected transiently after a long-term weight gain in Beagle dogs. Vet Immunol Immunopathol. 152(3-4):237–244. 10.1016/j.vetimm.2012.12.011. 23333192
  • van Iterson M, ‘t Hoen PA, Pedotti P, Hooiveld GJ, den Dunnen JT, van Ommen GJ, Boer JM, Menezes RX. 2009. Relative power and sample size analysis on gene expression profiling data. BMC Genom. 10:439.
  • Vanden Bussche J, Marzorati M, Laukens D, Vanhaecke L. 2015. Validated high resolution mass spectrometry-based approach for metabolomic fingerprinting of the human gut phenotype. Anal Chem. 87(21):10927–10934. doi: 10.1021/acs.analchem.5b02688.
  • Wang K, Peng X, Yang A, Huang Y, Tan Y, Qian Y, Lv F, Si H. 2022. Effects of diets with different protein levels on lipid metabolism and gut microbes in the host of different genders. Front Nutr. 9:940217. doi: 10.3389/fnut.2022.940217.
  • Weber M, Bissot T, Servet E, Sergheraert R, Biourge V, German AJ. 2007. A high‐protein, high‐fiber diet designed for weight loss improves satiety in dogs. J Vet Intern Med. 21(6):1203–1208. doi: 10.1111/j.1939-1676.2007.tb01939.x.
  • Wolfe AJ. 2015. Glycolysis for microbiome generation. Microbiol Spectr. 3(3):3. doi: 10.1128/microbiolspec.MBP-0014-2014.
  • Xu J, Verbrugghe A, Lourenço M, Cools A, Liu DJX, Van de Wiele T, Marzorati M, Eeckhaut V, Van Immerseel F, Vanhaecke L, et al. 2017. The response of canine faecal microbiota to increased dietary protein is influenced by body condition. BMC Vet Res. 13(1):374. doi: 10.1186/s12917-017-1276-0.
  • Yin J, Ren W, Huang X, Deng J, Li T, Yin Y. 2018. Potential mechanisms connecting purine metabolism and cancer therapy. Front Immunol. 9:1697. doi: 10.3389/fimmu.2018.01697.
  • Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, Schloss PD. 2013. The gut microbiome modulates colon tumorigenesis. mBio. 4(6):e00692-13. doi: 10.1128/mBio.00692-13.
  • Zhu Q, Jin Z, Wu W, Gao R, Guo B, Gao Z, Yang Y, Qin H. 2014. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLOS One. 9(6):e90849. doi: 10.1371/journal.pone.0090849.