Clostridium sporogenes utilizes Stickland’s reductive metabolism in the gut to generate ATP and produce circulating metabolites

  • Van Treuren, W. & Dodd, D. Microbial contribution to the human metabolome: implications for health and disease. Ann. Rev. Pathol. 15345–369 (2020).

    PubMed CAS Google Scholar Article

  • Russell, WR et al. The major phenylpropanoid-derived metabolites in the human gut may arise from microbial fermentation of proteins. Mol. Nutr. Food res. 57523–535 (2013).

    CAS PubMed Google Scholar Article

  • Smith, EA & Macfarlane, GT Dissimilatory amino acid metabolism in human colonic bacteria. Anaerobe 3327–337 (1997).

    CAS PubMed Google Scholar Article

  • Liu, Y., Hou, Y., Wang, G., Zheng, X. & Hao, H. Gut microbial metabolites of aromatic amino acids as signals in host-microbe interaction. Endocrinol Trends. Metab. 31818–834 (2020).

    CAS PubMed Google Scholar Article

  • Allison, MJ, Bryant, MP & Doetsch, RN Volatile fatty acid growth factor for bovine rumen cellulolytic cocci. Science 128474–475 (1958).

    CAS PubMed Google Scholar Article

  • Stack, RJ, Hungate, RE & Opsahl, WP Phenylacetic acid stimulation of cellulose digestion by Ruminococcus albus 8. Appl. Approximately. Microbiol. 46539-544 (1983).

    CAS PubMed PubMed Central Google Scholar Article

  • Hungate, RE & Stack, RJ Phenylpropanoic acid: growth factor for Ruminococcus albus. Appl. Approximately. Microbiol. 4479–83 (1982).

    CAS PubMed PubMed Central Google Scholar Article

  • Stickland, LH Metabolism studies of strict anaerobes (genus Clostridium): the chemical reactions by which Cl. sporogenes gets its energy. Biochemistry. J 281746–1759 (1934).

    CAS PubMed PubMed Central Google Scholar Article

  • Nisman, B. The Stickland Reaction. Bacteriol. Round. 1816–42 (1954).

    CAS PubMed PubMed Central Google Scholar Article

  • Lovitt, RW, Kell, DB & Morris, JG Proline reduction of Clostridium sporogens is coupled to proton vector ejection. Microbiol FEMS. Lett. 36269-273 (1986).

    CAS Google Scholar Article

  • Bader, J. & Simon, H. ATP formation is coupled to hydrogenation of 2-enoates in Clostridium sporogens. Microbiol FEMS. Lett. 20171–175 (1983).

    CAS Google Scholar Article

  • Dickert, S., Pierik, AJ & Buckel, W. Molecular characterization of phenyllactate dehydratase and its initiator of Clostridium sporogens. Mol. Microbiol. 4449–60 (2002).

    CAS PubMed Google Scholar Article

  • Buckel, W. & Thauer, RK Flavin-based electron bifurcation, a novel biological energy coupling mechanism. Chem. Round. 1183862–3886 (2018).

    CAS PubMed Google Scholar Article

  • Kimura, R. & Liao, TH A new anaerobic bacterium decomposing thiamine, Clostridium thiaminolyticum Kimura and Liao. proc. Jpn Acad. 29132–133 (1953).

    Google Scholar article

  • Karu, N. et al. A review of human fecal metabolomics: methods, applications, and human fecal metabolome database. Anal. Chem. Deed 10301–24 (2018).

    CAS PubMed Google Scholar Article

  • Wildenauer, FX & Winter, J. Isoleucine and arginine fermentation by pure and syntrophic cultures of Clostridium sporogens. Microbiol FEMS. Lett. 38373–379 (1986).

    CAS Google Scholar Article

  • Lovitt, RW, Morris, JG & Kell, DB The growth and nutrition of Clostridium sporogens NCIB 8053 in defined media. J.Appl. Bacteriol. 6271–80 (1987).

    CAS PubMed Google Scholar Article

  • Levin, BJ et al. A glycyl radical enzyme important in human gut microbiomes metabolizes trans-4-hydroxy-I-proline. Science https://doi.org/10.1126/science.aai8386 (2017).

  • Lovitt, RW, Kell, DB, and Morris, JG The physiology of Clostridium sporogens NCIB 8053 growing in defined media. J.Appl. Bacteriol. 6281–92 (1987).

    CAS PubMed Google Scholar Article

  • Neumann-Schaal, M., Hofmann, JD, Will, SE, and Schomburg, D. Time-resolved amino acid uptake of Clostridium difficile 630(delta)erm and concomitant formation of fermentation products and toxins. BMC Microbiol. 15281 (2015).

    PubMed PubMed Central CAS Article Google Scholar

  • Bouillaut, L., Self, WT & Sonenshein, AL Proline-dependent regulation of Clostridium difficile Metabolism of sticky earths. J. Bacteriol. 195844–854 (2013).

    CAS PubMed PubMed Central Google Scholar Article

  • Jackson, S., Calos, M., Myers, A. & Self, WT Analysis of proline reduction in nosocomial pathogen Clostridium difficile. J. Bacteriol. 1888487–8895 (2006).

    CAS PubMed PubMed Central Google Scholar Article

  • Ragsdale, SW Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem. Round. 1032333–2346 (2003).

    CAS PubMed Google Scholar Article

  • Xu, XL & Grant, GA Identification and characterization of two new types of bacteria I-serine dehydratases and evaluation of ACT domain function. Camber. Biochemistry. Biophys. 54062–69 (2013).

    CAS PubMed Google Scholar Article

  • Leach, S., Harvey, P. & Wali, R. Changes with growth rate in membrane lipid composition and amino acid utilization by continuous cultures of Campylobacter jejuni. J.Appl. Microbiol. 82631–640 (1997).

    CAS PubMed Google Scholar Article

  • Velayudhan, J., Jones, MA, Barrow, PA, and Kelly, DJ I-Serine catabolism via oxygen-labile I-serine dehydratase is essential for the colonization of the avian intestine by Campylobacter jejuni. Infect. Immun. 72260-268 (2004).

    CAS PubMed PubMed Central Google Scholar Article

  • Claus, SP et al. Multicompartmental systemic effects of the gut microbiome on mouse metabolic phenotypes. Mol. System Biol. 4219 (2008).

    PubMed PubMed Central CAS Article Google Scholar

  • Dodd, D. et al. An intestinal bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature 551648–652 (2017).

    CAS PubMed PubMed Central Google Scholar Article

  • Guo, CJ et al. Depletion of microbiome-derived molecules in the host using Clostridium genetic. Science https://doi.org/10.1126/science.aav1282 (2019).

  • Sharon, G et al. Human Autism Spectrum Disorder Gut Microbiota Promotes Behavioral Symptoms in Mice. Cell 1771600–1618.e1617 (2019).

    CAS PubMed PubMed Central Google Scholar Article

  • Aronov, PA et al. Colonic contribution to uremic solutes. Jam. Soc. Nephrol. 221769-1776 (2011).

    CAS PubMed PubMed Central Google Scholar Article

  • Fonknechten, N. et al. Clostridium sticklandiispecialist in amino acid degradation: revisiting its metabolism through the sequence of its genome. BMC Genom. 11555 (2010).

    CAS Google Scholar Article

  • Stadtman, TC & Elliott, P. Studies on the enzymatic reduction of amino acids. II. Purification and properties of D-proline reductase and a proline racemase of Clostridium sticklandii. J. Biol. Chem. 228983–997 (1957).

    CAS PubMed Google Scholar Article

  • Barker, HA Degradation of amino acids by anaerobic bacteria. Ann. Rev. Biochem. 5023–40 (1981).

    CAS PubMed Google Scholar Article

  • Nemet, I. et al. An intestinal microbial metabolite linked to cardiovascular disease acts via adrenergic receptors. Cell 180862–877.e822 (2020).

    CAS PubMed PubMed Central Google Scholar Article

  • Seedorf, H. et al. The genome of Clostridium kluyveria strict anaerobe with unique metabolic characteristics. proc. Natl Acad.Sci. UNITED STATES 1052128-2133 (2008).

    CAS PubMed PubMed Central Google Scholar Article

  • Li, F et al. Coupled reduction of ferredoxin and crotonyl coenzyme A (CoA) with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex of Clostridium kluyveri. J. Bacteriol. 190843–850 (2008).

    CAS PubMed Google Scholar Article

  • Herrmann, G., Jayamani, E., Mai, G. & Buckel, W. Energy conservation via electron transfer flavoprotein in anaerobic bacteria. J. Bacteriol. 190784–791 (2008).

    CAS PubMed Google Scholar Article

  • Kuhns, M. et al. The Rnf complex of the acetogenic bacterium Acetobacterium woodii: purification and characterization of RnfC and RnfB. Biochem. Biophys. Acta Bioenerg. 1861148263 (2020).

    CAS PubMed Google Scholar Article

  • Hreha, TN et al. Complete topology of the RNF complex of Vibrio cholerae. Biochemistry 542443–2455 (2015).

    CAS PubMed Google Scholar Article

  • Nayfach, S., Fischbach, MA & Pollard, KS MetaQuery: A web server for rapid annotation and quantitative analysis of specific genes in the human gut microbiome. Bioinformatics 313368–3370 (2015).

    CAS PubMed PubMed Central Google Scholar Article

  • Steed, AL et al. The microbial metabolite desaminotyrosine protects against influenza through type I interferon. Science 357498–502 (2017).

    CAS PubMed PubMed Central Google Scholar Article

  • Venkatesh, M. et al. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and the Toll-like receptor 4. Immunity 41296-310 (2014).

    CAS PubMed PubMed Central Google Scholar Article

  • Medema, MH, Takano, E. & Breitling, R. Detecting sequence homology at the gene cluster level with MultiGeneBlast. Mol. Biol. Evol. 301218-1223 (2013).

    CAS PubMed PubMed Central Google Scholar Article