Key bacterial taxa determine longitudinal dynamics of aromatic amino acid catabolism in infants’ gut

References

• Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med. 2016;22(7):713–17. doi:10.1038/nm.4142.
   PubMed Web of Science ®Google Scholar
• Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019;68(6):1108–1114. doi:10.1136/gutjnl-2018-317503.
   PubMed Web of Science ®Google Scholar
• Laue HE, Coker MO, Madan JC. The developing microbiome from birth to 3 years: the gut-brain axis and neurodevelopmental outcomes. Front Pediatr. 2022;10:254. doi:10.3389/fped.2022.815885.
   Web of Science ®Google Scholar
• Jain N, Walker WA. Diet and host–microbial crosstalk in postnatal intestinal immune homeostasis. Nat Rev Gastroenterol Hepatol. 2015;12(1):14–25. doi:10.1038/nrgastro.2014.153.
   PubMed Web of Science ®Google Scholar
• Roager HM, Dragsted LO. Diet‐derived microbial metabolites in health and disease. Nutr Bull. 2019;44(3):216–227. doi:10.1111/nbu.12396.
   Web of Science ®Google Scholar
• Roager HM, Stanton C, Hall LJ. Microbial metabolites as modulators of the infant gut microbiome and host-microbial interactions in early life. Gut Microbes. 2023;15(1):15. doi:10.1080/1949097620232192151.
   Web of Science ®Google Scholar
• Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. Cell2016. doi:10.1016/j.cell.2016.05.041.
   PubMed Web of Science ®Google Scholar
• Laursen MF, Sakanaka M, von Burg N, Mörbe U, Andersen D, Moll JM, Pekmez CT, Rivollier A, Michaelsen KF, Mølgaard C, et al. Bifidobacterium species associated with breastfeeding produce aromatic lactic acids in the infant gut. Nat Microbiol. 2021;6(11):1367–1382. doi:10.1038/s41564-021-00970-4.
   PubMed Web of Science ®Google Scholar
• Roager HM, Licht TR. Microbial tryptophan catabolites in health and disease. Nat Commun. 2018;9(1):3294. doi:10.1038/s41467-018-05470-4.
   PubMedGoogle Scholar
• Natividad JM, Agus A, Planchais J, Lamas B, Jarry AC, Martin R, Michel ML, Chong-Nguyen C, Roussel R, Straube M, et al. Impaired aryl hydrocarbon receptor ligand production by the gut microbiota is a key factor in metabolic syndrome. Cell Metab. 2018;28(5):737–749.e4. doi:10.1016/j.cmet.2018.07.001.
   PubMed Web of Science ®Google Scholar
• Hoyles L, Fernández-Real J-M, Federici M, Serino M, Abbott J, Charpentier J, Heymes C, Luque JL, Anthony E, Barton RH, et al. Molecular phenomics and metagenomics of hepatic steatosis in non-diabetic obese women. Nat Med. 2018;24(7):1070–1080. doi:10.1038/s41591-018-0061-3.
   PubMed Web of Science ®Google Scholar
• Krishnan S, Ding Y, Saedi N, Choi M, Sridharan GV, Sherr DH, Yarmush ML, Alaniz RC, Jayaraman A, Lee K. Gut microbiota-derived tryptophan metabolites modulate inflammatory response in hepatocytes and macrophages. Cell Rep. 2018;23(4):1099–1111. doi:10.1016/j.celrep.2018.03.109.
   PubMed Web of Science ®Google Scholar
• Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ, Higginbottom SK, Le A, Cowan TM, Nolan GP, Fischbach MA, et al. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature. 2017;551(7682):648–652. doi:10.1038/nature24661.
   PubMed Web of Science ®Google Scholar
• Zelante T, Iannitti RG, Cunha C, DeLuca A, Giovannini G, Pieraccini G, Zecchi R, D’Angelo C, Massi-Benedetti C, Fallarino F, et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013;39(2):372–385. doi:10.1016/j.immuni.2013.08.003.
   PubMed Web of Science ®Google Scholar
• Guo X, Liang Y, Zhang Y, Lasorella A, Kee BL, Fu Y-X. Innate lymphoid cells control early colonization resistance against intestinal pathogens through ID2-dependent regulation of the microbiota. Immunity. 2015;42(4):731–743. doi:10.1016/j.immuni.2015.03.012.
   PubMed Web of Science ®Google Scholar
• Hwang IK, Yoo KY, Li H, Park OK, Lee CH, Choi JH, Jeong YG, Lee YL, Kim YM, Kwon YG, et al. Indole-3-propionic acid attenuates neuronal damage and oxidative stress in the ischemic hippocampus. J Neurosci Res. 2009;87(9):2126–2137. doi:10.1002/jnr.22030.
   PubMed Web of Science ®Google Scholar
• Mimori S, Kawada K, Saito R, Takahashi M, Mizoi K, Okuma Y, Hosokawa M, Kanzaki T. Indole-3-propionic acid has chemical chaperone activity and suppresses endoplasmic reticulum stress-induced neuronal cell death. Biochem Biophys Res Commun. 2019;517(4):623–628. doi:10.1016/j.bbrc.2019.07.074.
   PubMed Web of Science ®Google Scholar
• Serger E, Luengo-Gutierrez L, Chadwick JS, Kong G, Zhou L, Crawford G, Danzi MC, Myridakis A, Brandis A, Bello AT, et al. The gut metabolite indole-3 propionate promotes nerve regeneration and repair. Nature. 2022;607(7919):585–592. doi:10.1038/s41586-022-04884-x.
   PubMed Web of Science ®Google Scholar
• Tsukuda N, Yahagi K, Hara T, Watanabe Y, Matsumoto H, Mori H, Higashi K, Tsuji H, Matsumoto S, Kurokawa K, et al. Key bacterial taxa and metabolic pathways affecting gut short-chain fatty acid profiles in early life. Isme J. 2021;15(9):2574–2590. doi:10.1038/s41396-021-00937-7.
   PubMed Web of Science ®Google Scholar
• Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–227. doi:10.1038/nature11053.
   PubMed Web of Science ®Google Scholar
• Appert O, Garcia AR, Frei R, Roduit C, Constancias F, Neuzil-Bunesova V, Ferstl R, Zhang J, Akdis C, Lauener R, et al. Initial butyrate producers during infant gut microbiota development are endospore formers. Environ Microbiol. 2020;22(9):3909–3921. doi:10.1111/1462-2920.15167.
   PubMed Web of Science ®Google Scholar
• Laursen MF, Laursen RP, Larnkjær A, Mølgaard C, Michaelsen KF, Frøkiær H, Bahl MI, Licht TR, Suen G. Faecalibacterium gut colonization is accelerated by presence of older siblings. mSphere. 2017;2(6):e00448–17. doi:10.1128/mSphere.00448-17.
   PubMed Web of Science ®Google Scholar
• Sugiyama Y, Mori Y, Nara M, Kotani Y, Nagai E, Kawada H, Kitamura M, Hirano R, Shimokawa H, Nakagawa A, et al. Gut bacterial aromatic amine production: aromatic amino acid decarboxylase and its effects on peripheral serotonin production. Gut Microbes. 2022;14(1):2128605. doi:10.1080/19490976.2022.2128605.
   PubMed Web of Science ®Google Scholar
• Valerio F, Lavermicocca P, Pascale M, Visconti A. Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett. 2004;233(2):289–295. doi:10.1111/j.1574-6968.2004.tb09494.x.
   PubMed Web of Science ®Google Scholar
• Ohhiral I, Kuwaki S, Morita H, Suzuki T, Tomita S, Hisamatsu S, Sonoki S, Shinoda S. Identification of 3-phenyllactic acid as a possible antibacterial substance produced by enterococcus faecalis TH 10. Biocontrol Sci. 2004;9(3):77–81. doi:10.4265/bio.9.77.
   Google Scholar
• Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, Anderson SE, Flint HJ. Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res. 2013;57(3):523–535. doi:10.1002/mnfr.201200594.
   PubMed Web of Science ®Google Scholar
• Sillner N, Walker A, Lucio M, Maier TV, Bazanella M, Rychlik M, Haller D, Schmitt-Kopplin P. Longitudinal profiles of dietary and microbial metabolites in formula- and breastfed infants. Front Mol Biosci. 2021;8:490. doi:10.3389/fmolb.2021.660456.
   Web of Science ®Google Scholar
• Chow J, Panasevich MR, Alexander D, Vester Boler BM, Rossoni Serao MC, Faber TA, Bauer LL, Fahey GC. Fecal metabolomics of healthy breast-fed versus formula-fed infants before and during in vitro batch culture fermentation. J Proteome Res. 2014;13(5):2534–2542. doi:10.1021/pr500011w.
   PubMed Web of Science ®Google Scholar
• He X, Parenti M, Grip T, Lönnerdal B, Timby N, Domellöf M, Hernell O, Slupsky CM. Fecal microbiome and metabolome of infants fed bovine MFGM supplemented formula or standard formula with breast-fed infants as reference: a randomized controlled trial. Sci Rep. 2019;9(1):1–14. doi:10.1038/s41598-019-48858-y.
   PubMedGoogle Scholar
• Béghin L, Marchandise X, Lien E, Bricout M, Bernet JP, Lienhardt JF, Jeannerot F, Menet V, Requillart JC, Marx J, et al. Growth, stool consistency and bone mineral content in healthy term infants fed sn-2-palmitate-enriched starter infant formula: a randomized, double-blind, multicentre clinical trial. Clin Nutr. 2019;38(3):1023–1030. doi:10.1016/j.clnu.2018.05.015.
   PubMed Web of Science ®Google Scholar
• Ehrlich AM, Pacheco AR, Henrick BM, Taft D, Xu G, Huda MN, Mishchuk D, Goodson ML, Slupsky C, Barile D, et al. Indole-3-lactic acid associated with Bifidobacterium-dominated microbiota significantly decreases inflammation in intestinal epithelial cells. BMC Microbiol. 2020;20(1):357. doi:10.1186/s12866-020-02023-y.
   PubMed Web of Science ®Google Scholar
• Henrick BM, Rodriguez L, Lakshmikanth T, Pou C, Henckel E, Arzoomand A, Olin A, Wang J, Mikes J, Tan Z, et al. Bifidobacteria-mediated immune system imprinting early in life. Cell. 2021;184(15):3884–3898.e11. doi:10.1016/j.cell.2021.05.030.
   PubMed Web of Science ®Google Scholar
• Meng D, Sommella E, Salviati E, Campiglia P, Ganguli K, Djebali K, Zhu W, Walker WA. Indole-3-lactic acid, a metabolite of tryptophan, secreted by Bifidobacterium longum subspecies infantis is anti-inflammatory in the immature intestine. Pediatr Res. 2020;88(2):209–217. doi:10.1038/s41390-019-0740-x.
   PubMed Web of Science ®Google Scholar
• De Mello VD, Paananen J, Lindström J, Lankinen MA, Shi L, Kuusisto J, Pihlajamäki J, Auriola S, Lehtonen M, Rolandsson O, et al. Indolepropionic acid and novel lipid metabolites are associated with a lower risk of type 2 diabetes in the Finnish Diabetes Prevention Study. Sci Reports. 2017;7(1):1–12. 71 2017. doi:10.1038/srep46337.
   PubMedGoogle Scholar
• Tuomainen M, Lindström J, Lehtonen M, Auriola S, Pihlajamäki J, Peltonen M, Tuomilehto J, Uusitupa M, De Mello VD, Hanhineva K. Associations of serum indolepropionic acid, a gut microbiota metabolite, with type 2 diabetes and low-grade inflammation in high-risk individuals. Nutr Diabetes. 2018;8(1):1–5. 81 2018. doi:10.1038/s41387-018-0046-9.
   PubMedGoogle Scholar
• Laursen MF, Dalgaard MD, Bahl MI. Genomic GC-Content affects the accuracy of 16S rRNA gene sequencing based microbial profiling due to PCR bias. Front Microbiol. 2017;8:1934. doi:10.3389/fmicb.2017.01934.
   PubMed Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
   PubMed Web of Science ®Google Scholar
• Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261–5267. doi:10.1128/AEM.00062-07.
   PubMed Web of Science ®Google Scholar
• Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
   PubMed Web of Science ®Google Scholar
• Johnsen LG, Skou PB, Khakimov B, Bro R. Gas chromatography - mass spectrometry data processing made easy. J Chromatogr A. 2017;1503:57–64. doi:10.1016/j.chroma.2017.04.052.
   PubMed Web of Science ®Google Scholar