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Escherichia coli acid resistance: pH-sensing, activation by chloride and autoinhibition in GadB.

Gut H, Pennacchietti E, John RA, Bossa F, Capitani G, De Biase D, Grütter MG
EMBO J 25 2643-51 (2006)
Related entries: 1pmm, 1pmo, 2dgl, 2dgm

Cited: 59 times
EuropePMC logo PMID: 16675957

Abstract

Escherichia coli and other enterobacteria exploit the H+ -consuming reaction catalysed by glutamate decarboxylase to survive the stomach acidity before reaching the intestine. Here we show that chloride, extremely abundant in gastric secretions, is an allosteric activator producing a 10-fold increase in the decarboxylase activity at pH 5.6. Cooperativity and sensitivity to chloride were lost when the N-terminal 14 residues, involved in the formation of two triple-helix bundles, were deleted by mutagenesis. X-ray structures, obtained in the presence of the substrate analogue acetate, identified halide-binding sites at the base of each N-terminal helix, showed how halide binding is responsible for bundle stability and demonstrated that the interconversion between active and inactive forms of the enzyme is a stepwise process. We also discovered an entirely novel structure of the cofactor pyridoxal 5'-phosphate (aldamine) to be responsible for the reversibly inactivated enzyme. Our results link the entry of chloride ions, via the H+/Cl- exchange activities of ClC-ec1, to the trigger of the acid stress response in the cell when the intracellular proton concentration has not yet reached fatal values.

Articles - 2dgk mentioned but not cited (2)

  1. Escherichia coli acid resistance: pH-sensing, activation by chloride and autoinhibition in GadB. Gut H, Pennacchietti E, John RA, Bossa F, Capitani G, De Biase D, Grütter MG. EMBO J 25 2643-2651 (2006)
  2. Mutation of His465 alters the pH-dependent spectroscopic properties of Escherichia coli glutamate decarboxylase and broadens the range of its activity toward more alkaline pH. Pennacchietti E, Lammens TM, Capitani G, Franssen MC, John RA, Bossa F, De Biase D. J Biol Chem 284 31587-31596 (2009)


Reviews citing this publication (10)

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  28. Structural insights into inhibition of Bacillus anthracis sporulation by a novel class of non-heme globin sensor domains. Stranzl GR, Santelli E, Bankston LA, La Clair C, Bobkov A, Schwarzenbacher R, Godzik A, Perego M, Grynberg M, Liddington RC. J Biol Chem 286 8448-8458 (2011)
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  31. Biochemical and spectroscopic properties of Brucella microti glutamate decarboxylase, a key component of the glutamate-dependent acid resistance system. Grassini G, Pennacchietti E, Cappadocio F, Occhialini A, De Biase D. FEBS Open Bio 5 209-218 (2015)
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  33. Identification of a proton-chloride antiporter (EriC) by Himar1 transposon mutagenesis in Lactobacillus reuteri and its role in histamine production. Hemarajata P, Spinler JK, Balderas MA, Versalovic J. Antonie Van Leeuwenhoek 105 579-592 (2014)
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  35. A Novel Inorganic Sulfur Compound Metabolizing Ferroplasma-Like Population Is Suggested to Mediate Extracellular Electron Transfer. Ni G, Simone D, Palma D, Broman E, Wu X, Turner S, Dopson M. Front Microbiol 9 2945 (2018)
  36. Ferric Uptake Regulator Provides a New Strategy for Acidophile Adaptation to Acidic Ecosystems. Chen XK, Li XY, Ha YF, Lin JQ, Liu XM, Pang X, Lin JQ, Chen LX. Appl Environ Microbiol 86 e00268-20 (2020)
  37. Production of γ-Aminobutyrate (GABA) in Recombinant Corynebacterium glutamicum by Expression of Glutamate Decarboxylase Active at Neutral pH. Son J, Baritugo KA, Sohn YJ, Kang KH, Kim HT, Joo JC, Park SJ. ACS Omega 7 29106-29115 (2022)
  38. ClC transporter activity modulates histidine catabolism in Lactobacillus reuteri by altering intracellular pH and membrane potential. Hall AE, Engevik MA, Oezguen N, Haag A, Versalovic J. Microb Cell Fact 18 212 (2019)
  39. Expression of recombinant glutamic acid decarboxylase in insect larvae and its application in an immunoassay for the diagnosis of autoimmune diabetes mellitus. Trabucchi A, Bombicino SS, Targovnik AM, Marfía JI, Sabljic AV, Faccinetti NI, Guerra LL, Iacono RF, Miranda MV, Valdez SN. Sci Rep 9 824 (2019)
  40. Molecular Analysis of Glutamate Decarboxylases in Enterococcus avium. Gu X, Zhao J, Zhang R, Yu R, Guo T, Kong J. Front Microbiol 12 691968 (2021)
  41. Development of a 2-pyrrolidone biosynthetic pathway in Corynebacterium glutamicum by engineering an acetyl-CoA balance route. Xu M, Gao H, Ma Z, Han J, Zheng K, Shao M, Rao Z. Amino Acids 54 1437-1450 (2022)
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  43. Enzymatic kinetic resolution of desmethylphosphinothricin indicates that phosphinic group is a bioisostere of carboxyl group. De Biase D, Cappadocio F, Pennacchietti E, Giovannercole F, Coluccia A, Vepsäläinen J, Khomutov A. Commun Chem 3 121 (2020)
  44. On the effect of alkaline pH and cofactor availability in the conformational and oligomeric state of Escherichia coli glutamate decarboxylase. Giovannercole F, Mérigoux C, Zamparelli C, Verzili D, Grassini G, Buckle M, Vachette P, De Biase D. Protein Eng Des Sel 30 235-244 (2017)
  45. Site-directed mutagenesis improves the practical application of L-glutamic acid decarboxylase in Escherichia coli. Fengmin L, Heng Z, Xiangjun Z, Xiaobo W, Huiyan L, Haitian F. Eng Life Sci 23 e2200064 (2023)
  46. Structural basis for substrate specificity of l-methionine decarboxylase. Okawa A, Shiba T, Hayashi M, Onoue Y, Murota M, Sato D, Inagaki J, Tamura T, Harada S, Inagaki K. Protein Sci 30 663-677 (2021)
  47. Transcriptomic and Metabolomic Profiling Reveals That KguR Broadly Impacts the Physiology of Uropathogenic Escherichia coli Under in vivo Relevant Conditions. Yang D, Jiang F, Huang X, Li G, Cai W. Front Microbiol 12 793391 (2021)


Related citations provided by authors (1)

  1. Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase.. Capitani G, De Biase D, Aurizi C, Gut H, Bossa F, Grütter MG EMBO J 22 4027-37 (2003)

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