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Volume 49 Issue 2
Mar.  2022
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Article Contents

The role of genotype and diet in shaping gut microbiome in a genetic vitamin A deficient mouse model

doi: 10.1016/j.jgg.2021.08.015
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This study was funded by the KCL and PKUHSC Joint Institute for Medical Research Fund (BMU2020KCL003), the National Natural Science Foundation of China (No. 81900984, 81991501, 81870747, 82000496, 82070566, and 81870387), the Beijing Municipal Natural Science Foundation (No. 7182184 and 7214267), Capital's Funds for Health Improvement and Research (2020-2Z-40813), and Peking University Clinical Medicine Plus X-Young Scholars Project (PKU2021LCXQ003).

  • Received Date: 2021-05-05
  • Accepted Date: 2021-08-26
  • Rev Recd Date: 2021-08-25
  • Publish Date: 2021-09-16
  • Multifactors have been reported to affect the gut microbiome, including genotype, age, diet, and nutrition. However, few reports have investigated the relative capacity of different factors to shape the gut microbiome in a single study. Our design used a genetic vitamin A-deficient mouse model, the Rbp4 mouse, feeding with the low vitamin A diets at different ages of initiation (4 or 7 weeks) for 28 days. Fecal samples were collected for bacterial profiling at seven time points after diet controlling. With Rbp4 depletion, Akkermansia decreased and Bacteroides increased, whereas Desulfovibrio, Barnesiella, Clostridium_XlVa, and Lactobacillus fluctuated. The bacterial community swiftly adjusted with the vitamin A-deficient diet administration and gradually changed (e.g., decrease of Barnesiella and increase of Desulfovibrio). Age exerted a relatively weaker but long-last influence. At an earlier age to feed a vitamin A-deficient diet, a higher microbial dysbiosis index will be valued. Of note, the shaping effects of diet and age on the bacterial community varied with the difference of genotype, which might indicate a greater role of genotype than diet and age in shaping the gut microbiome.
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  • Aron-Wisnewsky, J., Vigliotti, C., Witjes, J., Le, P., Holleboom, A.G., Verheij, J., Nieuwdorp, M.,Clement, K., 2020. Gut microbiota and human nafld:Disentangling microbial signatures from metabolic disorders. Nat Rev Gastroenterol Hepatol 17, 279-297
    Backhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., et al., 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690-703
    Blaner, W.S., 2019. Vitamin a signaling and homeostasis in obesity, diabetes, and metabolic disorders. Pharmacol Ther 197, 153-178
    Bonder, M.J., Kurilshikov, A., Tigchelaar, E.F., Mujagic, Z., Imhann, F., Vila, A.V., Deelen, P., Vatanen, T., Schirmer, M., Smeekens, S.P., et al., 2016. The effect of host genetics on the gut microbiome. Nat Genet 48, 1407-1412
    Chou, C.M., Nelson, C., Tarle, S.A., Pribila, J.T., Bardakjian, T., Woods, S., Schneider, A.,Glaser, T., 2015. Biochemical basis for dominant inheritance, variable penetrance, and maternal effects in rbp4 congenital eye disease. Cell 161, 634-646
    Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., Brown, C.T., Porras-Alfaro, A., Kuske, C.R.,Tiedje, J.M., 2014. Ribosomal database project:Data and tools for high throughput rrna analysis. Nucleic Acids Res 42, D633-642
    David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., et al., 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563
    Edgar, R.C., 2013. Uparse:Highly accurate otu sequences from microbial amplicon reads. Nat Methods 10, 996-998
    Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C.,Knight, R., 2011. Uchime improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200
    Fan, Y.,Pedersen, O., 2020. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol
    Gevers, D., Kugathasan, S., Denson, L.A., Vazquez-Baeza, Y., Van Treuren, W., Ren, B., Schwager, E., Knights, D., Song, S.J., Yassour, M., et al., 2014. The treatment-naive microbiome in new-onset crohn's disease. Cell Host Microbe 15, 382-392
    Goodrich, J.K., Davenport, E.R., Waters, J.L., Clark, A.G.,Ley, R.E., 2016. Cross-species comparisons of host genetic associations with the microbiome. Science 352, 532-535
    Goodrich, J.K., Waters, J.L., Poole, A.C., Sutter, J.L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J.T., et al., 2014. Human genetics shape the gut microbiome. Cell 159, 789-799
    Grizotte-Lake, M., Zhong, G., Duncan, K., Kirkwood, J., Iyer, N., Smolenski, I., Isoherranen, N.,Vaishnava, S., 2018. Commensals suppress intestinal epithelial cell retinoic acid synthesis to regulate interleukin-22 activity and prevent microbial dysbiosis. Immunity 49, 1103-1115 e1106
    Hornby, S.J., Ward, S.J.,Gilbert, C.E., 2003. Eye birth defects in humans may be caused by a recessively-inherited genetic predisposition to the effects of maternal vitamin a deficiency during pregnancy. Med Sci Monit 9, HY23-26
    Kanehisa, M., Furumichi, M., Sato, Y., Ishiguro-Watanabe, M.,Tanabe, M., 2021. Kegg:Integrating viruses and cellular organisms. Nucleic Acids Res 49, D545-D551
    Kau, A.L., Ahern, P.P., Griffin, N.W., Goodman, A.L.,Gordon, J.I., 2011. Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336
    Kim, S.,Jazwinski, S.M., 2018. The gut microbiota and healthy aging:A mini-review. Gerontology 64, 513-520
    Kimura, I., Miyamoto, J., Ohue-Kitano, R., Watanabe, K., Yamada, T., Onuki, M., Aoki, R., Isobe, Y., Kashihara, D., Inoue, D., et al., 2020. Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science 367
    Kreznar, J.H., Keller, M.P., Traeger, L.L., Rabaglia, M.E., Schueler, K.L., Stapleton, D.S., Zhao, W., Vivas, E.I., Yandell, B.S., Broman, A.T., et al., 2017. Host genotype and gut microbiome modulate insulin secretion and diet-induced metabolic phenotypes. Cell Rep 18, 1739-1750
    Langille, M.G., Meehan, C.J., Koenig, J.E., Dhanani, A.S., Rose, R.A., Howlett, S.E.,Beiko, R.G., 2014. Microbial shifts in the aging mouse gut. Microbiome 2, 50
    Langille, M.G., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Vega Thurber, R.L., Knight, R., et al., 2013. Predictive functional profiling of microbial communities using 16s rrna marker gene sequences. Nat Biotechnol 31, 814-821
    Lavelle, A.,Sokol, H., 2020. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 17, 223-237
    Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.M., Kennedy, S., et al., 2013. Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541-546
    Leamy, L.J., Kelly, S.A., Nietfeldt, J., Legge, R.M., Ma, F., Hua, K., Sinha, R., Peterson, D.A., Walter, J., Benson, A.K., et al., 2014. Host genetics and diet, but not immunoglobulin a expression, converge to shape compositional features of the gut microbiome in an advanced intercross population of mice. Genome Biol 15, 552
    Lee, H.,Ko, G., 2016. Antiviral effect of vitamin a on norovirus infection via modulation of the gut microbiome. Sci Rep 6, 25835
    Liu, Y., Yang, K., Jia, Y., Shi, J., Tong, Z., Fang, D., Yang, B., Su, C., Li, R., Xiao, X., et al., 2021. Gut microbiome alterations in high-fat-diet-fed mice are associated with antibiotic tolerance. Nat Microbiol 6, 874-884
    Lloyd-Price, J., Arze, C., Ananthakrishnan, A.N., Schirmer, M., Avila-Pacheco, J., Poon, T.W., Andrews, E., Ajami, N.J., Bonham, K.S., Brislawn, C.J., et al., 2019. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature 569, 655-662
    Meckel, K.R.,Kiraly, D.D., 2020. Maternal microbes support fetal brain wiring. Nature 586, 203-205
    Meslier, V., Laiola, M., Roager, H.M., De Filippis, F., Roume, H., Quinquis, B., Giacco, R., Mennella, I., Ferracane, R., Pons, N., et al., 2020. Mediterranean diet intervention in overweight and obese subjects lowers plasma cholesterol and causes changes in the gut microbiome and metabolome independently of energy intake. Gut 69, 1258-1268
    Morais, L.H., Schreiber, H.L.t.,Mazmanian, S.K., 2020. The gut microbiota-brain axis in behaviour and brain disorders. Nat Rev Microbiol
    National Genomics Data Center, M.,Partners, 2020. Database resources of the national genomics data center in 2020. Nucleic Acids Res 48, D24-D33
    Ogbu, D., Xia, E.,Sun, J., 2020. Gut instincts:Vitamin d/vitamin d receptor and microbiome in neurodevelopment disorders. Open Biol 10, 200063
    Pein, H., Koeberle, S.C., Voelkel, M., Schneider, F., Rossi, A., Thurmer, M., Loeser, K., Sautebin, L., Morrison, H., Werz, O., et al., 2017. Vitamin a regulates akt signaling through the phospholipid fatty acid composition. FASEB J 31, 4566-4577
    Quadro, L., Hamberger, L., Gottesman, M.E., Wang, F., Colantuoni, V., Blaner, W.S.,Mendelsohn, C.L., 2005. Pathways of vitamin a delivery to the embryo:Insights from a new tunable model of embryonic vitamin a deficiency. Endocrinology 146, 4479-4490
    Ray, K., 2021. Gut microbiome influences the protective effects of a mediterranean diet. Nat Rev Gastroenterol Hepatol 18, 215
    Rognes, T., Flouri, T., Nichols, B., Quince, C.,Mahe, F., 2016. Vsearch:A versatile open source tool for metagenomics. PeerJ 4, e2584
    Salazar, N., Valdes-Varela, L., Gonzalez, S., Gueimonde, M.,de Los Reyes-Gavilan, C.G., 2017. Nutrition and the gut microbiome in the elderly. Gut Microbes 8, 82-97
    Singh, R.K., Chang, H.W., Yan, D., Lee, K.M., Ucmak, D., Wong, K., Abrouk, M., Farahnik, B., Nakamura, M., Zhu, T.H., et al., 2017. Influence of diet on the gut microbiome and implications for human health. J Transl Med 15, 73
    Snijders, A.M., Langley, S.A., Kim, Y.M., Brislawn, C.J., Noecker, C., Zink, E.M., Fansler, S.J., Casey, C.P., Miller, D.R., Huang, Y., et al., 2016. Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome. Nat Microbiol 2, 16221
    Tran, T.T.T., Corsini, S., Kellingray, L., Hegarty, C., Le Gall, G., Narbad, A., Muller, M., Tejera, N., O'Toole, P.W., Minihane, A.M., et al., 2019. Apoe genotype influences the gut microbiome structure and function in humans and mice:Relevance for alzheimer's disease pathophysiology. FASEB J 33, 8221-8231
    Turnbaugh, P.J., Ridaura, V.K., Faith, J.J., Rey, F.E., Knight, R.,Gordon, J.I., 2009. The effect of diet on the human gut microbiome:A metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1, 6ra14
    Vuong, H.E., Pronovost, G.N., Williams, D.W., Coley, E.J.L., Siegler, E.L., Qiu, A., Kazantsev, M., Wilson, C.J., Rendon, T.,Hsiao, E.Y., 2020. The maternal microbiome modulates fetal neurodevelopment in mice. Nature 586, 281-286
    Wang, Y., Song, F., Zhu, J., Zhang, S., Yang, Y., Chen, T., Tang, B., Dong, L., Ding, N., Zhang, Q., et al., 2017. Gsa:Genome sequence archive<sup/>. Genomics Proteomics Bioinformatics 15, 14-18
    Wickham, H., 2016. Ggplot2:Elegant graphics for data analysis. Springer-Verlag New York
    Wilson, A.S., Koller, K.R., Ramaboli, M.C., Nesengani, L.T., Ocvirk, S., Chen, C., Flanagan, C.A., Sapp, F.R., Merritt, Z.T., Bhatti, F., et al., 2020. Diet and the human gut microbiome:An international review. Dig Dis Sci 65, 723-740
    Yamamoto, E.A.,Jorgensen, T.N., 2019. Relationships between vitamin d, gut microbiome, and systemic autoimmunity. Front Immunol 10, 3141
    Yatsunenko, T., Rey, F.E., Manary, M.J., Trehan, I., Dominguez-Bello, M.G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R.N., Anokhin, A.P., et al., 2012. Human gut microbiome viewed across age and geography. Nature 486, 222-227
    Zhang, J., Zhou, S., Zhang, Q., Feng, S., Chen, Y., Zheng, H., Wang, X., Zhao, W., Zhang, T., Zhou, Y., et al., 2014. Proteomic analysis of rbp4/vitamin a in children with cleft lip and/or palate. J Dent Res 93, 547-552
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