1932

Abstract

Amino acids are indispensable substrates for protein synthesis in all organisms and incorporated into diverse aspects of metabolic physiology and signaling. However, animals lack the ability to synthesize several of them and must acquire these essential amino acids from their diet or perhaps their associated microbial communities. The essential amino acids therefore occupy a unique position in the health of animals and their relationships with microbes. Here we review recent work connecting microbial production and metabolism of essential amino acids to host biology, and the reciprocal impacts of host metabolism of essential amino acids on their associated microbes. We focus on the roles of the branched-chain amino acids (valine, leucine, and isoleucine) and tryptophan on host-microbe communication in the intestine of humans and other vertebrates. We then conclude by highlighting research questions surrounding the less-understood aspects of microbial essential amino acid synthesis in animal hosts.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032421-111819
2023-09-15
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032421-111819.html?itemId=/content/journals/10.1146/annurev-micro-032421-111819&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Agus A, Planchais J, Sokol H. 2018. Gut microbiota regulation of tryptophan metabolism in health and disease. Cell Host Microbe 23:716–24
    [Google Scholar]
  2. 2.
    Alkhalaf LM, Ryan KS. 2015. Biosynthetic manipulation of tryptophan in bacteria: pathways and mechanisms. Chem. Biol. 22:317–28
    [Google Scholar]
  3. 3.
    Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–402
    [Google Scholar]
  4. 4.
    Atasoglu C, Valdes C, Walker ND, Newbold CJ, Wallace RJ. 1998. De novo synthesis of amino acids by the ruminal bacteria Prevotella bryantii B14, Selenomonas ruminantium HD4, and Streptococcus bovis ES1. Appl. Environ. Microbiol. 64:2836–43
    [Google Scholar]
  5. 5.
    Barrett J. 1991. Amino acid metabolism in helminths. Adv. Parasitol. 30:39–105
    [Google Scholar]
  6. 6.
    Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ et al. 2006. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269–82
    [Google Scholar]
  7. 7.
    Bellono NW, Bayrer JR, Leitch DB, Castro J, Zhang C et al. 2017. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170:185–98.e16
    [Google Scholar]
  8. 8.
    Bhattarai Y, Williams BB, Battaglioli EJ, Whitaker WR, Till L et al. 2018. Gut microbiota-produced tryptamine activates an epithelial G-protein-coupled receptor to increase colonic secretion. Cell Host Microbe 23:775–85.e5
    [Google Scholar]
  9. 9.
    Brawner KM, Yeramilli VA, Duck LW, Van Der Pol W, Smythies LE et al. 2019. Depletion of dietary aryl hydrocarbon receptor ligands alters microbiota composition and function. Sci. Rep. 9:14724
    [Google Scholar]
  10. 10.
    Broer S, Broer A. 2017. Amino acid homeostasis and signalling in mammalian cells and organisms. Biochem. J. 474:1935–63
    [Google Scholar]
  11. 11.
    Cabreiro F, Au C, Leung KY, Vergara-Irigaray N, Cocheme HM et al. 2013. Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153:228–39
    [Google Scholar]
  12. 12.
    Cervantes-Barragan L, Chai JN, Tianero MD, Di Luccia B, Ahern PP et al. 2017. Lactobacillus reuteri induces gut intraepithelial CD4+CD8αβ+ T cells. Science 357:806–10
    [Google Scholar]
  13. 13.
    Cervenka I, Agudelo LZ, Ruas JL. 2017. Kynurenines: tryptophan's metabolites in exercise, inflammation, and mental health. Science 357:6349eaaf9794
    [Google Scholar]
  14. 14.
    Chen L, Tuo B, Dong H. 2016. Regulation of intestinal glucose absorption by ion channels and transporters. Nutrients 8:143
    [Google Scholar]
  15. 15.
    Cheng Y, Jin UH, Allred CD, Jayaraman A, Chapkin RS, Safe S. 2015. Aryl hydrocarbon receptor activity of tryptophan metabolites in young adult mouse colonocytes. Drug Metab. Dispos. 43:1536–43
    [Google Scholar]
  16. 16.
    Chimerel C, Emery E, Summers DK, Keyser U, Gribble FM, Reimann F. 2014. Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells. Cell Rep. 9:1202–8
    [Google Scholar]
  17. 17.
    Choi BS, Daniel N, Houde VP, Ouellette A, Marcotte B et al. 2021. Feeding diversified protein sources exacerbates hepatic insulin resistance via increased gut microbial branched-chain fatty acids and mTORC1 signaling in obese mice. Nat. Commun. 12:3377
    [Google Scholar]
  18. 18.
    Comai S, Bertazzo A, Brughera M, Crotti S. 2020. Tryptophan in health and disease. Adv. Clin. Chem. 95:165–218
    [Google Scholar]
  19. 19.
    Davies PSW. 2020. Stable isotopes: their use and safety in human nutrition studies. Eur. J. Clin. Nutr. 74:362–65
    [Google Scholar]
  20. 20.
    de Oliveira Filho JG, Carvalho A, Alves JDS, Egea MB. 2022. Next-generation probiotics as a therapeutic strategy for the treatment of phenylketonuria: a review. Nutr. Rev. 80:2100–12
    [Google Scholar]
  21. 21.
    De Vadder F, Grasset E, Manneras Holm L, Karsenty G, Macpherson AJ et al. 2018. Gut microbiota regulates maturation of the adult enteric nervous system via enteric serotonin networks. PNAS 115:6458–63
    [Google Scholar]
  22. 22.
    Desbonnet L, Clarke G, Traplin A, O'Sullivan O, Crispie F et al. 2015. Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour. Brain Behav. Immun. 48:165–73
    [Google Scholar]
  23. 23.
    Devlin AS, Marcobal A, Dodd D, Nayfach S, Plummer N et al. 2016. Modulation of a circulating uremic solute via rational genetic manipulation of the gut microbiota. Cell Host Microbe 20:709–15
    [Google Scholar]
  24. 24.
    Diether NE, Willing BP. 2019. Microbial fermentation of dietary protein: an important factor in diet-microbe-host interaction. Microorganisms 7:119
    [Google Scholar]
  25. 25.
    Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ et al. 2017. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature 551:648–52
    [Google Scholar]
  26. 26.
    Dong F, Hao F, Murray IA, Smith PB, Koo I et al. 2020. Intestinal microbiota-derived tryptophan metabolites are predictive of Ah receptor activity. Gut Microbes 12:1788899
    [Google Scholar]
  27. 27.
    El Aidy S, Kunze W, Bienenstock J, Kleerebezem M. 2012. The microbiota and the gut-brain axis: insights from the temporal and spatial mucosal alterations during colonisation of the germfree mouse intestine. Benef. Microbes 3:251–59
    [Google Scholar]
  28. 28.
    Epelbaum S, Chipman DM, Barak Z. 1996. Metabolic effects of inhibitors of two enzymes of the branched-chain amino acid pathway in Salmonella typhimurium. J. Bacteriol. 178:1187–96
    [Google Scholar]
  29. 29.
    Evenepoel P, Claus D, Geypens B, Hiele M, Geboes K et al. 1999. Amount and fate of egg protein escaping assimilation in the small intestine of humans. Am. J. Physiol. 277:G935–43
    [Google Scholar]
  30. 30.
    Favennec M, Hennart B, Caiazzo R, Leloire A, Yengo L et al. 2015. The kynurenine pathway is activated in human obesity and shifted toward kynurenine monooxygenase activation. Obesity 23:2066–74
    [Google Scholar]
  31. 31.
    Felig P, Marliss E, Cahill GF Jr. 1969. Plasma amino acid levels and insulin secretion in obesity. N. Engl. J. Med. 281:811–16
    [Google Scholar]
  32. 32.
    Fung TC, Vuong HE, Luna CDG, Pronovost GN, Aleksandrova AA et al. 2019. Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut. Nat. Microbiol. 4:2064–73
    [Google Scholar]
  33. 33.
    Gainetdinov RR, Hoener MC, Berry MD. 2018. Trace amines and their receptors. Pharmacol. Rev. 70:549–620
    [Google Scholar]
  34. 34.
    Gao J, Xu K, Liu H, Liu G, Bai M et al. 2018. Impact of the gut microbiota on intestinal immunity mediated by tryptophan metabolism. Front. Cell Infect. Microbiol. 8:13
    [Google Scholar]
  35. 35.
    Gazzaniga F, Stebbins R, Chang SZ, McPeek MA, Brenner C. 2009. Microbial NAD metabolism: lessons from comparative genomics. Microbiol. Mol. Biol. Rev. 73:529–41
    [Google Scholar]
  36. 36.
    Geypens B, Claus D, Evenepoel P, Hiele M, Maes B et al. 1997. Influence of dietary protein supplements on the formation of bacterial metabolites in the colon. Gut 41:70–76
    [Google Scholar]
  37. 37.
    Gibson JA, Sladen GE, Dawson AM. 1976. Protein absorption and ammonia production: the effects of dietary protein and removal of the colon. Br. J. Nutr. 35:61–65
    [Google Scholar]
  38. 38.
    Godon JJ, Delorme C, Bardowski J, Chopin MC, Ehrlich SD, Renault P 1993. Gene inactivation in Lactococcus lactis: branched-chain amino acid biosynthesis. J. Bacteriol. 175:4383–90
    [Google Scholar]
  39. 39.
    Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y et al. 2016. The maternal microbiota drives early postnatal innate immune development. Science 351:1296–302
    [Google Scholar]
  40. 40.
    Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD et al. 2009. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6:279–89
    [Google Scholar]
  41. 41.
    Guo CJ, Allen BM, Hiam KJ, Dodd D, Van Treuren W et al. 2019. Depletion of microbiome-derived molecules in the host using Clostridium genetics. Science 366:6471eaav1282
    [Google Scholar]
  42. 42.
    Gupta NK, Thaker AI, Kanuri N, Riehl TE, Rowley CW et al. 2012. Serum analysis of tryptophan catabolism pathway: correlation with Crohn's disease activity. Inflamm. Bowel Dis. 18:1214–20
    [Google Scholar]
  43. 43.
    Gustafsson BE. 1980 (1959). Vitamin K deficiency in germfree rats. Nutr. Rev. 38:344–47
    [Google Scholar]
  44. 44.
    Hansen EB. 2018. Redox reactions in food fermentations. Curr. Opin. Food Sci. 19:98–103
    [Google Scholar]
  45. 45.
    Hubbard TD, Murray IA, Bisson WH, Lahoti TS, Gowda K et al. 2015. Adaptation of the human aryl hydrocarbon receptor to sense microbiota-derived indoles. Sci. Rep. 5:12689
    [Google Scholar]
  46. 46.
    Huovinen JA, Gustafsson BE. 1967. Inorganic sulphate, sulphite and sulphide as sulphur donors in the biosynthesis of sulphur amino acids in germ-free and conventional rats. Biochim. Biophys. Acta Gen. Subj. 136:441–47
    [Google Scholar]
  47. 47.
    Illes P, Krasulova K, Vyhlidalova B, Poulikova K, Marcalikova A et al. 2020. Indole microbial intestinal metabolites expand the repertoire of ligands and agonists of the human pregnane X receptor. Toxicol. Lett. 334:87–93
    [Google Scholar]
  48. 48.
    Isabella VM, Ha BN, Castillo MJ, Lubkowicz DJ, Rowe SE et al. 2018. Development of a synthetic live bacterial therapeutic for the human metabolic disease phenylketonuria. Nat. Biotechnol. 36:857–64
    [Google Scholar]
  49. 49.
    Iyer SS, Gensollen T, Gandhi A, Oh SF, Neves JF et al. 2018. Dietary and microbial oxazoles induce intestinal inflammation by modulating aryl hydrocarbon receptor responses. Cell 173:1123–34.e11
    [Google Scholar]
  50. 50.
    Jenkins TA, Nguyen JC, Polglaze KE, Bertrand PP. 2016. Influence of tryptophan and serotonin on mood and cognition with a possible role of the gut-brain axis. Nutrients 8:156
    [Google Scholar]
  51. 51.
    Jin UH, Lee SO, Sridharan G, Lee K, Davidson LA et al. 2014. Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Mol. Pharmacol. 85:777–88
    [Google Scholar]
  52. 52.
    Joye I 2019. Protein digestibility of cereal products. Foods 8:6199
    [Google Scholar]
  53. 53.
    Kaiser JC, Heinrichs DE. 2018. Branching out: alterations in bacterial physiology and virulence due to branched-chain amino acid deprivation. mBio 9:5e01188–18
    [Google Scholar]
  54. 54.
    Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids. Res. 28:27–30
    [Google Scholar]
  55. 55.
    Koh A, Molinaro A, Stahlman M, Khan MT, Schmidt C et al. 2018. Microbially produced imidazole propionate impairs insulin signaling through mTORC1. Cell 175:947–61.e17
    [Google Scholar]
  56. 56.
    Krautkramer KA, Fan J, Backhed F. 2021. Gut microbial metabolites as multi-kingdom intermediates. Nat. Rev. Microbiol. 19:77–94
    [Google Scholar]
  57. 57.
    Krishnan S, Ding Y, Saeidi N, Choi M, Sridharan GV et al. 2019. Gut microbiota-derived tryptophan metabolites modulate inflammatory response in hepatocytes and macrophages. Cell Rep. 28:3285
    [Google Scholar]
  58. 58.
    Kumar A, Russell RM, Pifer R, Menezes-Garcia Z, Cuesta S et al. 2020. The serotonin neurotransmitter modulates virulence of enteric pathogens. Cell Host Microbe 28:41–53.e8
    [Google Scholar]
  59. 59.
    Kumar P, Lee JH, Lee J. 2021. Diverse roles of microbial indole compounds in eukaryotic systems. Biol. Rev. Camb. Philos. Soc. 96:2522–45
    [Google Scholar]
  60. 60.
    Kwon YH, Wang H, Denou E, Ghia JE, Rossi L et al. 2019. Modulation of gut microbiota composition by serotonin signaling influences intestinal immune response and susceptibility to colitis. Cell Mol. Gastroenterol. Hepatol. 7:709–28
    [Google Scholar]
  61. 61.
    Lamas B, Natividad JM, Sokol H. 2018. Aryl hydrocarbon receptor and intestinal immunity. Mucosal Immunol. 11:1024–38
    [Google Scholar]
  62. 62.
    Lamas B, Richard ML, Leducq V, Pham HP, Michel ML et al. 2016. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat. Med. 22:598–605
    [Google Scholar]
  63. 63.
    Lanis JM, Alexeev EE, Curtis VF, Kitzenberg DA, Kao DJ et al. 2017. Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia. Mucosal Immunol. 10:1133–44
    [Google Scholar]
  64. 64.
    LaRossa RA, Schloss JV. 1984. The sulfonylurea herbicide sulfometuron methyl is an extremely potent and selective inhibitor of acetolactate synthase in Salmonella typhimurium. J. Biol. Chem. 259:8753–57
    [Google Scholar]
  65. 65.
    Lawther RP, Calhoun DH, Adams CW, Hauser CA, Gray J, Hatfield GW. 1981. Molecular basis of valine resistance in Escherichia coli K-12. PNAS 78:922–25
    [Google Scholar]
  66. 66.
    Lee JH, Lee J. 2010. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34:426–44
    [Google Scholar]
  67. 67.
    Lee JH, Wood TK, Lee J. 2015. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. 23:707–18
    [Google Scholar]
  68. 68.
    Liu D, Wei Y, Liu X, Zhou Y, Jiang L et al. 2018. Indoleacetate decarboxylase is a glycyl radical enzyme catalysing the formation of malodorant skatole. Nat. Commun. 9:4224
    [Google Scholar]
  69. 69.
    Liu M, Nieuwdorp M, de Vos WM, Rampanelli E. 2022. Microbial tryptophan metabolism tunes host immunity, metabolism, and extraintestinal disorders. Metabolites 12:9834
    [Google Scholar]
  70. 70.
    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. 31:818–34
    [Google Scholar]
  71. 71.
    Ma Q, Zhang X, Qu Y. 2018. Biodegradation and biotransformation of indole: advances and perspectives. Front. Microbiol. 9:2625
    [Google Scholar]
  72. 72.
    Malhotra M, Srivastava S. 2008. Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM. Environ. Microbiol. 10:1365–73
    [Google Scholar]
  73. 73.
    Marinangeli CPF, House JD. 2017. Potential impact of the digestible indispensable amino acid score as a measure of protein quality on dietary regulations and health. Nutr. Rev. 75:658–67
    [Google Scholar]
  74. 74.
    Mathai JK, Liu Y, Stein HH. 2017. Values for digestible indispensable amino acid scores (DIAAS) for some dairy and plant proteins may better describe protein quality than values calculated using the concept for protein digestibility-corrected amino acid scores (PDCAAS). Br. J. Nutr. 117:490–99
    [Google Scholar]
  75. 75.
    Matthews DE. 2020. Review of lysine metabolism with a focus on humans. J. Nutr. 150:2548S–55S
    [Google Scholar]
  76. 76.
    Mawe GM, Hoffman JM. 2013. Serotonin signalling in the gut—functions, dysfunctions and therapeutic targets. Nat. Rev. Gastroenterol. Hepatol. 10:473–86
    [Google Scholar]
  77. 77.
    Mellor AL, Munn DH. 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4:762–74
    [Google Scholar]
  78. 78.
    Metges CC, El-Khoury AE, Henneman L, Petzke KJ, Grant I et al. 1999. Availability of intestinal microbial lysine for whole body lysine homeostasis in human subjects. Am. J. Physiol. 277:E597–607
    [Google Scholar]
  79. 79.
    Metges CC, Petzke KJ, El-Khoury AE, Henneman L, Grant I et al. 1999. Incorporation of urea and ammonia nitrogen into ileal and fecal microbial proteins and plasma free amino acids in normal men and ileostomates. Am. J. Clin. Nutr. 70:1046–58
    [Google Scholar]
  80. 80.
    Modoux M, Rolhion N, Mani S, Sokol H. 2021. Tryptophan metabolism as a pharmacological target. Trends Pharmacol. Sci. 42:60–73
    [Google Scholar]
  81. 81.
    Monticello DJ, Hadioetomo RS, Costilow RN. 1984. Isoleucine synthesis by Clostridium sporogenes from propionate or alpha-methylbutyrate. J. Gen. Microbiol. 130:309–18
    [Google Scholar]
  82. 82.
    Moran-Ramos S, Macias-Kauffer L, Lopez-Contreras BE, Villamil-Ramirez H, Ocampo-Medina E et al. 2021. A higher bacterial inward BCAA transport driven by Faecalibacterium prausnitzii is associated with lower serum levels of BCAA in early adolescents. Mol. Med. 27:108
    [Google Scholar]
  83. 83.
    Morbach S, Junger C, Sahm H, Eggeling L. 2000. Attenuation control of ilvBNC in Corynebacterium glutamicum: evidence of leader peptide formation without the presence of a ribosome binding site. J. Biosci. Bioeng. 90:501–7
    [Google Scholar]
  84. 84.
    Morffy N, Strader LC. 2020. Old Town Roads: routes of auxin biosynthesis across kingdoms. Curr. Opin. Plant Biol. 55:21–27
    [Google Scholar]
  85. 85.
    Natividad JM, Agus A, Planchais J, Lamas B, Jarry AC et al. 2018. Impaired aryl hydrocarbon receptor ligand production by the gut microbiota is a key factor in metabolic syndrome. Cell Metab. 28:737–49.e4
    [Google Scholar]
  86. 86.
    Neinast M, Murashige D, Arany Z. 2019. Branched chain amino acids. Annu. Rev. Physiol. 81:139–64
    [Google Scholar]
  87. 87.
    Neis EP, Dejong CH, Rensen SS. 2015. The role of microbial amino acid metabolism in host metabolism. Nutrients 7:2930–46
    [Google Scholar]
  88. 88.
    Nemet I, Saha PP, Gupta N, Zhu W, Romano KA et al. 2020. A cardiovascular disease-linked gut microbial metabolite acts via adrenergic receptors. Cell 180:862–77.e22
    [Google Scholar]
  89. 89.
    Nikolaus S, Schulte B, Al-Massad N, Thieme F, Schulte DM et al. 2017. Increased tryptophan metabolism is associated with activity of inflammatory bowel diseases. Gastroenterology 153:1504–16.e2
    [Google Scholar]
  90. 90.
    Nozawa K, Kawabata-Shoda E, Doihara H, Kojima R, Okada H et al. 2009. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. PNAS 106:3408–13
    [Google Scholar]
  91. 91.
    Obata Y, Castano A, Boeing S, Bon-Frauches AC, Fung C et al. 2020. Neuronal programming by microbiota regulates intestinal physiology. Nature 578:284–89
    [Google Scholar]
  92. 92.
    Ottosson F, Brunkwall L, Smith E, Orho-Melander M, Nilsson PM et al. 2020. The gut microbiota-related metabolite phenylacetylglutamine associates with increased risk of incident coronary artery disease. J. Hypertens. 38:2427–34
    [Google Scholar]
  93. 93.
    Park JH, Lee SY. 2010. Fermentative production of branched chain amino acids: a focus on metabolic engineering. Appl. Microbiol. Biotechnol. 85:491–506
    [Google Scholar]
  94. 94.
    Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T et al. 2016. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature 535:376–81
    [Google Scholar]
  95. 95.
    Pfefferkorn ER, Guyre PM. 1984. Inhibition of growth of Toxoplasma gondii in cultured fibroblasts by human recombinant gamma interferon. Infect. Immun. 44:211–16
    [Google Scholar]
  96. 96.
    Powell DN, Swimm A, Sonowal R, Bretin A, Gewirtz AT et al. 2020. Indoles from the commensal microbiota act via the AHR and IL-10 to tune the cellular composition of the colonic epithelium during aging. PNAS 117:21519–26
    [Google Scholar]
  97. 97.
    Venu VKP, Saifeddine M, Mihara K, Tsai YC, Nieves K et al. 2019. The pregnane X receptor and its microbiota-derived ligand indole 3-propionic acid regulate endothelium-dependent vasodilation. Am. J. Physiol. Endocrinol. Metab. 317:E350–61
    [Google Scholar]
  98. 98.
    Reigstad CS, Salmonson CE, Rainey JF 3rd, Szurszewski JH, Linden DR et al. 2015. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J. 29:1395–403
    [Google Scholar]
  99. 99.
    Rhee SJ, Walker WA, Cherayil BJ. 2005. Developmentally regulated intestinal expression of IFN-gamma and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 175:1127–36
    [Google Scholar]
  100. 100.
    Riazi R, Wykes LJ, Ball RO, Pencharz PB. 2003. The total branched-chain amino acid requirement in young healthy adult men determined by indicator amino acid oxidation by use of l-[1-13C]phenylalanine. J. Nutr. 133:1383–89
    [Google Scholar]
  101. 101.
    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE et al. 2013. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214
    [Google Scholar]
  102. 102.
    Roager HM, Hansen LB, Bahl MI, Frandsen HL, Carvalho V et al. 2016. Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut. Nat. Microbiol. 1:16093
    [Google Scholar]
  103. 103.
    Roager HM, Licht TR. 2018. Microbial tryptophan catabolites in health and disease. Nat. Commun. 9:3294
    [Google Scholar]
  104. 104.
    Robinson CD, Sweeney EG, Ngo J, Ma E, Perkins A et al. 2021. Host-emitted amino acid cues regulate bacterial chemokinesis to enhance colonization. Cell Host Microbe 29:1221–34.e8
    [Google Scholar]
  105. 105.
    Rothhammer V, Mascanfroni ID, Bunse L, Takenaka MC, Kenison JE et al. 2016. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 22:586–97
    [Google Scholar]
  106. 106.
    Sachs JL, Skophammer RG, Regus JU. 2011. Evolutionary transitions in bacterial symbiosis. PNAS 108:Suppl. 210800–7
    [Google Scholar]
  107. 107.
    Sadik A, Somarribas Patterson LF, Ozturk S, Mohapatra SR, Panitz V et al. 2020. IL4I1 is a metabolic immune checkpoint that activates the AHR and promotes tumor progression. Cell 182:1252–70.e34
    [Google Scholar]
  108. 108.
    Seif Y, Choudhary KS, Hefner Y, Anand A, Yang L, Palsson BO. 2020. Metabolic and genetic basis for auxotrophies in Gram-negative species. PNAS 117:6264–73
    [Google Scholar]
  109. 109.
    Smith EA, Macfarlane GT. 1996. Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J. Appl. Bacteriol. 81:288–302
    [Google Scholar]
  110. 110.
    Smith T. 1897. A modification of the method for determining the production of indol by bacteria. J. Exp. Med. 2:543–47
    [Google Scholar]
  111. 111.
    Sonowal R, Swimm A, Sahoo A, Luo L, Matsunaga Y et al. 2017. Indoles from commensal bacteria extend healthspan. PNAS 114:E7506–15
    [Google Scholar]
  112. 112.
    Sookoian S, Pirola CJ. 2015. Liver enzymes, metabolomics and genome-wide association studies: from systems biology to the personalized medicine. World J. Gastroenterol. 21:711–25
    [Google Scholar]
  113. 113.
    Tan C, Zheng Z, Wan X, Cao J, Wei R, Duan J. 2021. The role of gut microbiota and amino metabolism in the effects of improvement of islet beta-cell function after modified jejunoileal bypass. Sci. Rep. 11:4809
    [Google Scholar]
  114. 114.
    Torrallardona D, Harris CI, Coates ME, Fuller MF. 1996. Microbial amino acid synthesis and utilization in rats: incorporation of 15N from 15NH4Cl into lysine in the tissues of germ-free and conventional rats. Br. J. Nutr. 76:689–700
    [Google Scholar]
  115. 115.
    Torrallardona D, Harris CI, Fuller MF. 2003. Lysine synthesized by the gastrointestinal microflora of pigs is absorbed, mostly in the small intestine. Am. J. Physiol. Endocrinol. Metab. 284:E1177–80
    [Google Scholar]
  116. 116.
    Torrallardona D, Harris CI, Fuller MF. 2003. Pigs' gastrointestinal microflora provide them with essential amino acids. J. Nutr. 133:1127–31
    [Google Scholar]
  117. 117.
    Townsend GE 2nd, Han W, Schwalm ND 3rd, Hong X, Bencivenga-Barry NA et al. 2020. A master regulator of Bacteroides thetaiotaomicron gut colonization controls carbohydrate utilization and an alternative protein synthesis factor. mBio 11:1e03221–19. Erratum 2020. mBio 112e00301–20
    [Google Scholar]
  118. 118.
    Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y et al. 2012. Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet. Biol. 49:48–57
    [Google Scholar]
  119. 119.
    Umbarger HE. 1978. Amino acid biosynthesis and its regulation. Annu. Rev. Biochem. 47:532–606
    [Google Scholar]
  120. 120.
    Van Oekelen D, Megens A, Meert T, Luyten WH, Leysen JE. 2002. Role of 5-HT2 receptors in the tryptamine-induced 5-HT syndrome in rats. Behav. Pharmacol. 13:313–18
    [Google Scholar]
  121. 121.
    Venkatesh M, Mukherjee S, Wang H, Li H, Sun K et al. 2014. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 41:296–310
    [Google Scholar]
  122. 122.
    Vieira-Silva S, Falony G, Darzi Y, Lima-Mendez G, Garcia Yunta R et al. 2016. Species-function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 1:16088
    [Google Scholar]
  123. 123.
    Vogel CF, Goth SR, Dong B, Pessah IN, Matsumura F. 2008. Aryl hydrocarbon receptor signaling mediates expression of indoleamine 2,3-dioxygenase. Biochem. Biophys. Res. Commun. 375:331–35
    [Google Scholar]
  124. 124.
    Vujkovic-Cvijin I, Dunham RM, Iwai S, Maher MC, Albright RG et al. 2013. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci. Transl. Med. 5:193ra91
    [Google Scholar]
  125. 125.
    Wek RC, Sameshima JH, Hatfield GW. 1987. Rho-dependent transcriptional polarity in the ilvGMEDA operon of wild-type Escherichia coli K12. J. Biol. Chem. 262:15256–61
    [Google Scholar]
  126. 126.
    Wen J, Mercado GP, Volland A, Doden HL, Lickwar CR et al. 2021. Fxr signaling and microbial metabolism of bile salts in the zebrafish intestine. Sci. Adv. 7:30eabg1371
    [Google Scholar]
  127. 127.
    White PJ, Newgard CB. 2019. Branched-chain amino acids in disease. Science 363:582–83
    [Google Scholar]
  128. 128.
    Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA et al. 2009. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. PNAS 106:3698–703
    [Google Scholar]
  129. 129.
    Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M et al. 2014. Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe 16:495–503
    [Google Scholar]
  130. 130.
    Wlodarska M, Luo C, Kolde R, d'Hennezel E, Annand JW et al. 2017. Indoleacrylic acid produced by commensal Peptostreptococcus species suppresses inflammation. Cell Host Microbe 22:25–37.e6
    [Google Scholar]
  131. 131.
    Wu G. 2014. Dietary requirements of synthesizable amino acids by animals: a paradigm shift in protein nutrition. J. Anim. Sci. Biotechnol. 5:34
    [Google Scholar]
  132. 132.
    Wu M, McNulty NP, Rodionov DA, Khoroshkin MS, Griffin NW et al. 2015. Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350:aac5992
    [Google Scholar]
  133. 133.
    Xiao F, Guo F. 2022. Impacts of essential amino acids on energy balance. Mol. Metab. 57:101393
    [Google Scholar]
  134. 134.
    Xie G, Keyhani NO, Bonner CA, Jensen RA. 2003. Ancient origin of the tryptophan operon and the dynamics of evolutionary change. Microbiol. Mol. Biol. Rev. 67:303–42
    [Google Scholar]
  135. 135.
    Yabut JM, Crane JD, Green AE, Keating DJ, Khan WI, Steinberg GR. 2019. Emerging roles for serotonin in regulating metabolism: new implications for an ancient molecule. Endocr. Rev. 40:1092–107
    [Google Scholar]
  136. 136.
    Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P et al. 2015. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–76
    [Google Scholar]
  137. 137.
    Ye L, Bae M, Cassilly CD, Jabba SV, Thorpe DW et al. 2021. Enteroendocrine cells sense bacterial tryptophan catabolites to activate enteric and vagal neuronal pathways. Cell Host Microbe 29:179–96.e9
    [Google Scholar]
  138. 138.
    Yelamanchi SD, Surolia A. 2021. Targeting amino acid metabolism of Mycobacterium tuberculosis for developing inhibitors to curtail its survival. IUBMB Life 73:643–58
    [Google Scholar]
  139. 139.
    Yu J, Luo Y, Zhu Z, Zhou Y, Sun L et al. 2019. A tryptophan metabolite of the skin microbiota attenuates inflammation in patients with atopic dermatitis through the aryl hydrocarbon receptor. J. Allergy Clin. Immunol. 143:2108–19.e12
    [Google Scholar]
  140. 140.
    Zafar H, Saier MH Jr. 2018. Comparative genomics of transport proteins in seven Bacteroides species. PLOS ONE 13:e0208151
    [Google Scholar]
  141. 141.
    Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G et al. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372–85
    [Google Scholar]
  142. 142.
    Zhang X, Gan M, Li J, Li H, Su M et al. 2020. Endogenous indole pyruvate pathway for tryptophan metabolism mediated by IL4I1. J. Agric. Food Chem. 68:10678–84
    [Google Scholar]
  143. 143.
    Zhao J, Zhang X, Liu H, Brown MA, Qiao S. 2019. Dietary protein and gut microbiota composition and function. Curr. Protein Pept. Sci. 20:145–54
    [Google Scholar]
  144. 144.
    Zhu JX, Zhu XY, Owyang C, Li Y. 2001. Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J. Physiol. 530:431–42
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032421-111819
Loading
/content/journals/10.1146/annurev-micro-032421-111819
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error