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The role of bacterial cell envelope structures in acid stress resistance in E. coli

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Abstract

Acid resistance (AR) is an indispensable mechanism for the survival of neutralophilic bacteria, such as Escherichia coli (E. coli) strains that survive in the gastrointestinal tract. E. coli acid tolerance has been extensively studied during past decades, with most studies focused on gene regulation and mechanisms. However, the role of cell membrane structure in the context of acid stress resistance has not been discussed in depth. Here, we provide a comprehensive review of the roles and mechanisms of the E. coli cell envelope from different membrane components, such as membrane proteins, fatty acids, chaperones, and proton-consuming systems, and particularly focus on the innovative effects revealed by recent studies. We hope that the information guides us to understand the bacterial survival strategies under acid stress and to further explore the AR regulatory mechanisms to prevent or treat E. coli and other related Gram-negative bacteria infection, or to enhance the AR of engineering E. coli.

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References

  • Barua S, Yamashino T, Hasegawa T, Yokoyama K, Torii K, Ohta M (2002) Involvement of surface polysaccharides in the organic acid resistance of Shiga toxin-producing Escherichia coli O157:H7. Mol Microbiol 43(3):629–640. https://doi.org/10.1046/j.1365-2958.2002.02768.x

    Article  PubMed  CAS  Google Scholar 

  • Baslé A, Rummel G, Storici P, Rosenbusch JP, Schirmer T (2006) Crystal structure of osmoporin OmpC from E. coli at 2.0 Å. J Mol Biol 362(5):933–942

    PubMed  Google Scholar 

  • Bekhit A, Fukamachi T, Saito H, Kobayashi H (2011) The role of OmpC and OmpF in acidic resistance in Escherichia coli. Biol Pharm Bull 34(3):330–334

    PubMed  CAS  Google Scholar 

  • Bhagwat AA, Tan J, Sharma M, Kothary M, Low S, Tall BD, Bhagwat M (2006) Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl Environ Microbiol 72(7):4978–4986

    PubMed  PubMed Central  CAS  Google Scholar 

  • Buchner S, Schlundt A, Lassak J, Sattler M, Jung K (2015) Structural and functional analysis of the signal-transducing linker in the pH-responsive one-component system CadC of Escherichia coli. J Mol Biol 427(15):2548–2561

    PubMed  CAS  Google Scholar 

  • Cao L, Liang D, Hao P, Song Q, Xue E, Caiyin Q, Cheng Z, Qiao J (2018) The increase of O-acetylation and N-deacetylation in cell wall promotes acid resistance and nisin production through improving cell wall integrity in Lactococcus lactis. J Ind Microbiol Biotechnol 45(9):813–825

    PubMed  CAS  Google Scholar 

  • Capitani G, De Biase D, Aurizi C, Gut H, Bossa F, Grütter MG (2003) Crystal structure and functional analysis of Escherichia coli glutamate decarboxylase. EMBO J 22(16):4027–4037

    PubMed  PubMed Central  CAS  Google Scholar 

  • Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF, Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181(11):3525–3535

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chakraborty S, Winardhi RS, Morgan LK, Yan J, Kenney LJ (2017) Non-canonical activation of OmpR drives acid and osmotic stress responses in single bacterial cells. Nat Commun 8(1):1587–1514. https://doi.org/10.1038/s41467-017-02030-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang YY, Cronan JE (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33(2):249–259

    PubMed  CAS  Google Scholar 

  • Chen YY, Gänzle MG (2016) Influence of cyclopropane fatty acids on heat, high pressure, acid and oxidative resistance in Escherichia coli. Int J Food Microbiol 222:16–22

    PubMed  CAS  Google Scholar 

  • Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PD, Suh H, Marto JA, Garner EC, Bernhardt TG (2016) Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously. Nat Microbiol 1(10):16172

    PubMed  PubMed Central  CAS  Google Scholar 

  • Clausen T, Kaiser M, Huber R, Ehrmann M (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12(3):152

    PubMed  CAS  Google Scholar 

  • Conlan S, Zhang Y, Cheley S, Bayley H (2000) Biochemical and biophysical characterization of OmpG: a monomeric porin. Biochemistry-US 39(39):11845–11854

    CAS  Google Scholar 

  • Cronan JE, Reed R, Taylor F, Jackson M (1979) Properties and biosynthesis of cyclopropane fatty acids in Escherichia coli. J Bacteriol 138(1):118–121

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dahl J-U, Koldewey P, Salmon L, Horowitz S, Bardwell JC, Jakob U (2015) HdeB functions as an acid-protective chaperone in bacteria. J Biol Chem 290(1):65–75

    PubMed  CAS  Google Scholar 

  • De Biase D, Lund PA (2015) The Escherichia coli acid stress response and its significance for pathogenesis. Adv Appl Microbiol. Elsevier, 92:49–88

    PubMed  Google Scholar 

  • De Biase D, Pennacchietti E (2012) Glutamate decarboxylase-dependent acid resistance in orally acquired bacteria: function, distribution and biomedical implications of the gadBC operon. Mol Microbiol 86(4):770–786

    PubMed  Google Scholar 

  • De la Cruz MÁ, Calva E (2010) The complexities of porin genetic regulation. J Mol Microbiol Biotechnol 18(1):24–36

    PubMed  Google Scholar 

  • Egan AJ, Biboy J, van't Veer I, Breukink E, Vollmer W (2015) Activities and regulation of peptidoglycan synthases. Philos T R Soc B 370(1679):20150031

    Google Scholar 

  • Eichinger A, Haneburger I, Koller C, Jung K, Skerra A (2011) Crystal structure of the sensory domain of Escherichia coli CadC, a member of the ToxR-like protein family. Protein Sci 20(4):656–669

    PubMed  PubMed Central  CAS  Google Scholar 

  • Espaillat A, Forsmo O, El Biari K, Björk R, Lemaitre B, Trygg J, Cañada FJ, de Pedro MA, Cava F (2016) Chemometric analysis of bacterial peptidoglycan reveals atypical modifications that empower the cell wall against predatory enzymes and fly innate immunity. J Am Chem Soc 138(29):9193–9204

    PubMed  CAS  Google Scholar 

  • Foit L, George JS, Zhang BW, Brooks CL, Bardwell JC (2013) Chaperone activation by unfolding. P Natl Acad Sci USA 110(14):E1254–E1262

    CAS  Google Scholar 

  • Foster JW (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2(11):898–907

    PubMed  CAS  Google Scholar 

  • Fozo EM, Quivey RG (2004) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70(2):929–936

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fritz G, Koller C, Burdack K, Tetsch L, Haneburger I, Jung K, Gerland U (2009) Induction kinetics of a conditional pH stress response system in Escherichia coli. J Mol Biol 393(2):272–286

    PubMed  CAS  Google Scholar 

  • Fu X, Wang Y, Shao H, Ma J, Song X, Zhang M, Chang Z (2018) DegP functions as a critical protease for bacterial acid resistance. FEBS J 285(18):3525–3538

    PubMed  CAS  Google Scholar 

  • Gayen A, Kumar D, Matheshwaran S, Chandra M (2019) Nonlinear spectroscopy reveals how external pH controls permeation and accumulation of small molecules in two cellular compartments of Escherichia coli. Anal Chem

  • Gianotti A, Iucci L, Guerzoni ME, Lanciotti R (2009) Effect of acidic conditions on fatty acid composition and membrane fluidity of Escherichia coli strains isolated from Crescenza cheese. Ann Microbiol 59(3):603

    CAS  Google Scholar 

  • Gorden J, Small PL (1993) Acid resistance in enteric bacteria. Infect Immun 61(1):364–367

    PubMed  PubMed Central  CAS  Google Scholar 

  • Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61(4):429–441

    PubMed  PubMed Central  CAS  Google Scholar 

  • Groisman EA, Hollands K, Kriner MA, Lee E-J, Park S-Y, Pontes MH (2013) Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet 47:625–646

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gut H, Pennacchietti E, John RA, Bossa F, Capitani G, De Biase D, Grütter MG (2006) Escherichia coli acid resistance: pH-sensing, activation by chloride and autoinhibition in GadB. EMBO J 25(11):2643–2651

    PubMed  PubMed Central  CAS  Google Scholar 

  • Haddaji N, Mahdhi AK, Ismaiil MB, Bakhrouf A (2017) Effect of environmental stress on cell surface and membrane fatty acids of Lactobacillus plantarum. Arch Microbiol 199(9):1243–1250

    PubMed  CAS  Google Scholar 

  • Haneburger I, Fritz G, Jurkschat N, Tetsch L, Eichinger A, Skerra A, Gerland U, Jung K (2012) Deactivation of the E. coli pH stress sensor CadC by cadaverine. J Mol Biol 424(1–2):15–27

    PubMed  CAS  Google Scholar 

  • Harder B-J, Bettenbrock K, Klamt S (2016) Model-based metabolic engineering enables high yield itaconic acid production by Escherichia coli. Metab Eng 38:29–37

    PubMed  CAS  Google Scholar 

  • He D, Zhang M, Liu S, Xie X, Chen PR (2019) Protease-mediated protein quality control for bacterial acid resistance. Cell Chem Biol 26(1):144-150. e3

    PubMed  Google Scholar 

  • Herrera CM, Hankins JV, Trent MS (2010) Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol Microbiol 76(6):1444–1460

    PubMed  PubMed Central  CAS  Google Scholar 

  • Heyde M, Portalier R (1987) Regulation of major outer membrane porin proteins of Escherichia coli K 12 by pH. Mol Gen Genet 208(3):511–517

    PubMed  CAS  Google Scholar 

  • Hong W, Jiao W, Hu J, Zhang J, Liu C, Fu X, Shen D, Xia B, Chang Z (2005) Periplasmic protein HdeA exhibits chaperone-like activity exclusively within stomach pH range by transforming into disordered conformation. J Biol Chem 280(29):27029–27034

    PubMed  CAS  Google Scholar 

  • Huang C-C, Smith CV, Glickman MS, Jacobs WR, Sacchettini JC (2002) Crystal structures of mycolic acid cyclopropane synthases from Mycobacterium tuberculosis. J Biol Chem 277(13):11559–11569

    PubMed  CAS  Google Scholar 

  • Ilgü H, Jeckelmann J-M, Gapsys V, Ucurum Z, de Groot BL, Fotiadis D (2016) Insights into the molecular basis for substrate binding and specificity of the wild-type L-arginine/agmatine antiporter AdiC. P Natl Acad Sci USA 113(37):10358–10363

    Google Scholar 

  • Iyer R, Wu Z, Woster PM, Delcour AH (2000) Molecular basis for the polyamine-OmpF porin interactions: inhibitor and mutant studies. J Mol Biol 297(4):933–945

    PubMed  CAS  Google Scholar 

  • Janßen HJ, Steinbüchel A (2014) Fatty acid synthesis in Escherichia coli and its applications towards the production of fatty acid based biofuels. Biotechnol Biofuels 7(1):7

    PubMed  PubMed Central  Google Scholar 

  • Joloba ML, Clemmer KM, Sledjeski DD, Rather PN (2004) Activation of the gab operon in an RpoS-dependent manner by mutations that truncate the inner core of lipopolysaccharide in Escherichia coli. J Bacteriol 186(24):8542–8546

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kanjee U, Houry WA (2013) Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol 67:65–81

    PubMed  CAS  Google Scholar 

  • Kato A, Chen HD, Latifi T, Groisman EA (2012) Reciprocal control between a bacterium’s regulatory system and the modification status of its lipopolysaccharide. Mol Cell 47(6):897–908

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kenney LJ (2019) The role of acid stress in Salmonella pathogenesis. Curr Opin Microbiol 47:45–51

    PubMed  CAS  Google Scholar 

  • Kern R, Malki A, Abdallah J, Tagourti J, Richarme G (2007) Escherichia coli HdeB is an acid stress chaperone. J Bacteriol 189(2):603–610

    PubMed  CAS  Google Scholar 

  • Krammer E-M, Gibbons A, Roos G, Prévost M (2018) Molecular mechanism of substrate selectivity of the arginine-agmatine Antiporter AdiC. Sci Rep-UK 8(1):15607

    Google Scholar 

  • Krulwich TA, Sachs G, Padan E (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9(5):330

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lai GC, Cho H, Bernhardt TG (2017) The mecillinam resistome reveals a role for peptidoglycan endopeptidases in stimulating cell wall synthesis in Escherichia coli. PLoS Genet 13(7):e1006934

    PubMed  PubMed Central  Google Scholar 

  • Lennen RM, Kruziki MA, Kumar K, Zinkel RA, Burnum KE, Lipton MS, Hoover SW, Ranatunga DR, Wittkopp TM, Marner WD (2011) Membrane stresses induced by overproduction of free fatty acids in Escherichia coli. Appl Environ Microbiol 77(22):8114–8128

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li Z, Quan G, Jiang X, Yang Y, Ding X, Zhang D, Wang X, Hardwidge PR, Ren W, Zhu G (2018) Effects of metabolites derived from gut microbiota and hosts on pathogens. Front Cell Infect Microbiol 8

  • Liko I, Degiacomi MT, Lee S, Newport TD, Gault J, Reading E, Hopper JT, Housden NG, White P, Colledge M (2018) Lipid binding attenuates channel closure of the outer membrane protein OmpF. P Natl Acad Sci USA 115(26):6691–6696

    CAS  Google Scholar 

  • Lin J, Smith MP, Chapin KC, Baik HS, Bennett GN, Foster JW (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62(9):3094–3100

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu N, Delcour AH (1998) Inhibitory effect of acidic pH on OmpC porin: wild-type and mutant studies. FEBS Lett 434(1–2):160–164

    PubMed  CAS  Google Scholar 

  • Lu P, Ma D, Chen Y, Guo Y, Chen G-Q, Deng H, Shi Y (2013) L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res 23(5):635

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lund P, Tramonti A, De Biase D (2014) Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev 38(6):1091–1125

    PubMed  CAS  Google Scholar 

  • Ma D, Lu P, Yan C, Fan C, Yin P, Wang J, Shi Y (2012) Structure and mechanism of a glutamate–GABA antiporter. Nature 483(7391):632–636

    PubMed  CAS  Google Scholar 

  • Malki A, Le H-T, Milles S, Kern R, Caldas T, Abdallah J, Richarme G (2008) Solubilization of protein aggregates by the acid stress chaperones HdeA and HdeB. J Biol Chem 283(20):13679–13687

    PubMed  CAS  Google Scholar 

  • Mari SA, Köster S, Bippes CA, Yildiz Ö, Kühlbrandt W, Muller DJ (2010) pH-induced conformational change of the β-barrel-forming protein OmpG reconstituted into native E. coli lipids. J Mol Biol 396(3):610–616

    PubMed  CAS  Google Scholar 

  • Masi M, Winterhalter M, Pagès J-M (2019) Outer Membrane Porins. In: Kuhn A (ed) Bacterial cell walls and membranes. Springer International Publishing, Cham, pp 79–123

    Google Scholar 

  • Merdanovic M, Clausen T, Kaiser M, Huber R, Ehrmann M (2011) Protein quality control in the bacterial periplasm. Annu Rev Microbiol 65:149–168

    PubMed  CAS  Google Scholar 

  • Merroun ML, Selenska-Pobell S (2008) Bacterial interactions with uranium: an environmental perspective. J Contam Hydrol 102(3):285–295. https://doi.org/10.1016/j.jconhyd.2008.09.019

    Article  PubMed  CAS  Google Scholar 

  • Miller SI, Salama NR (2018) The Gram-negative bacterial periplasm: size matters. PLoS Biol 16(1):e2004935

    PubMed  PubMed Central  Google Scholar 

  • Missiakas D, Raina S (1997) Protein folding in the bacterial periplasm. J Bacteriol 179(8):2465

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell AM, Silhavy TJ (2019) Envelope stress responses: balancing damage repair and toxicity. Nat Rev Microbiol 17:417–428

    PubMed  CAS  Google Scholar 

  • Morè N, Martorana AM, Biboy J, Otten C, Winkle M, Serrano CKG, Silva AM, Atkinson L, Yau H, Breukink E (2019) Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect. MBio 10(1):e02729–e02718

    PubMed  PubMed Central  Google Scholar 

  • Mueller EA, Egan AJ, Breukink E, Vollmer W, Levin PA (2019) Plasticity of Escherichia coli cell wall metabolism promotes fitness and antibiotic resistance across environmental conditions. Elife 8:e40754

    PubMed  PubMed Central  Google Scholar 

  • Murata T, Tseng W, Guina T, Miller SI, Nikaido H (2007) PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar typhimurium. J Bacteriol 189(20):7213–7222

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A (2011) Phenotypic landscape of a bacterial cell. Cell 144(1):143–156

    PubMed  CAS  Google Scholar 

  • Nikaido H, Nakae T (1980) The outer membrane of Gram-negative bacteria advances in microbial physiology. Advances in Microbial 20. Elsevier:163–250

    Google Scholar 

  • Parsons JB, Rock CO (2013) Bacterial lipids: metabolism and membrane homeostasis. Prog Lipid Res 52(3):249–276

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pazos M, Peters K, Vollmer W (2017) Robust peptidoglycan growth by dynamic and variable multi-protein complexes. Curr Opin Microbiol 36:55–61

    PubMed  CAS  Google Scholar 

  • Perez-Rathke A, Fahie MA, Chisholm C, Liang J, Chen M (2018) Mechanism of OmpG pH-dependent gating from loop ensemble and single channel studies. J Am Chem Soc 140(3):1105–1115

    PubMed  PubMed Central  CAS  Google Scholar 

  • Perez JC, Groisman EA (2007) Acid pH activation of the PmrA/PmrB two-component regulatory system of Salmonella enterica. Mol Microbiol 63(1):283–293

    PubMed  PubMed Central  CAS  Google Scholar 

  • Perini D, Alcaraz A, Queralt-Martín M (2019a) Lipid headgroup charge and acyl chain composition modulate closure of bacterial β-barrel channels. Int J Mol Sci 20(3):674

    PubMed Central  CAS  Google Scholar 

  • Perini DA, Alcaraz A, Aguilella VM, Queralt-Martin M (2019b) Mechanistic insights into voltage-induced closure of bacterial beta-barrel channels. Biophys J 116(3):401a

    Google Scholar 

  • Peters K, Kannan S, Rao VA, Biboy J, Vollmer D, Erickson SW, Lewis RJ, Young KD, Vollmer W (2016) The redundancy of peptidoglycan carboxypeptidases ensures robust cell shape maintenance in Escherichia coli. MBio 7(3):e00819–e00816

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pumps E, Cost F, RamA B (2011) Efflux pumps of Gram-negative bacteria: genetic responses to stress and the modulation of their activity by pH, inhibitors, and phenothiazines. Adv Enzymol Relat Areas Mol Biol 238:61

    Google Scholar 

  • Qi Y, Liu H, Chen X, Liu L (2018) Engineering microbial membranes to increase stress tolerance of industrial strains. Metab Eng

  • Queralt-Martín M, García-Giménez E, Mafé S, Alcaraz A (2011) Divalent cations reduce the pH sensitivity of OmpF channel inducing the pKa shift of key acidic residues. Phys Chem Chem Phys 13(2):563–569

    PubMed  Google Scholar 

  • Raetz C, Dowhan W (1990) Biosynthesis and function of phospholipids in Escherichia coli. J Biol Chem 265(3):1235–1238

    PubMed  CAS  Google Scholar 

  • Rao NN, GómezGarcía MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78(78):605–647. https://doi.org/10.1146/annurev.biochem.77.083007.093039

    Article  PubMed  CAS  Google Scholar 

  • Rauschmeier M, Schüppel V, Tetsch L, Jung K (2014) New insights into the interplay between the lysine transporter LysP and the pH sensor CadC in Escherichia coli. J Mol Biol 426(1):215–229

    PubMed  CAS  Google Scholar 

  • Rodriguez-Moya M, Gonzalez R (2015) Proteomic analysis of the response of Escherichia coli to short-chain fatty acids. J Proteome 122:86–99

    CAS  Google Scholar 

  • Rojas ER, Billings G, Odermatt PD, Auer GK, Zhu L, Miguel A, Chang F, Weibel DB, Theriot JA, Huang KC (2018) The outer membrane is an essential load-bearing element in Gram-negative bacteria. Nature 559:617–621. https://doi.org/10.1038/s41586-018-0344-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rowbury R, Goodson M, Wallace A (1992) The PhoE porin and transmission of the chemical stimulus for induction of acid resistance (acid habituation) in Escherichia coli. J Appl Bacteriol 72(3):233–243

    PubMed  CAS  Google Scholar 

  • Rowbury RJ (2004) Enterobacterial responses to external protons, including responses that involve early warning against stress and the functioning of extracellular pheromones, alarmones and varisensors. Sci Progress-UK 87(3):193–225

    CAS  Google Scholar 

  • Royce LA, Liu P, Stebbins MJ, Hanson BC, Jarboe LR (2013) The damaging effects of short chain fatty acids on Escherichia coli membranes. Appl Microbiol Biotechnol 97(18):8317–8327

    PubMed  PubMed Central  CAS  Google Scholar 

  • Royce LA, Yoon JM, Chen Y, Rickenbach E, Shanks JV, Jarboe LR (2015) Evolution for exogenous octanoic acid tolerance improves carboxylic acid production and membrane integrity. Metab Eng 29:180–188

    PubMed  CAS  Google Scholar 

  • Sainz T, Pérez J, Villaseca J, Hernández U, Eslava C, Mendoza G, Wacher C (2005) Survival to different acid challenges and outer membrane protein profiles of pathogenic Escherichia coli strains isolated from pozol, a Mexican typical maize fermented food. Int J Food Microbiol 105(3):357–367

    PubMed  CAS  Google Scholar 

  • Samartzidou H, Delcour AH (1999) Distinct sensitivities of OmpF and PhoE porins to charged modulators. FEBS Lett 444(1):65–70

    PubMed  CAS  Google Scholar 

  • Sandoval NR, Papoutsakis ET (2016) Engineering membrane and cell-wall programs for tolerance to toxic chemicals: beyond solo genes. Curr Opin Microbiol 33:56–66

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sato M, Machida K, Arikado E, Saito H, Kakegawa T, Kobayashi H (2000) Expression of outer membrane proteins in Escherichia coli growing at acid pH. Appl Environ Microbiol 66(3):943–947

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32(2):234–258

    PubMed  CAS  Google Scholar 

  • Schlundt A, Buchner S, Janowski R, Heydenreich T, Heermann R, Lassak J, Geerlof A, Stehle R, Niessing D, Jung K (2017) Structure-function analysis of the DNA-binding domain of a transmembrane transcriptional activator. Sci Rep-UK 7(1):1051

    Google Scholar 

  • Seo SW, Kim D, O’Brien EJ, Szubin R, Palsson BO (2015) Decoding genome-wide GadEWX-transcriptional regulatory networks reveals multifaceted cellular responses to acid stress in Escherichia coli. Nat Commun 6:7970

    PubMed  PubMed Central  CAS  Google Scholar 

  • Seufferheld MJ, Alvarez HM, Farias ME (2008) Role of polyphosphates in microbial adaptation to extreme environments. Appl Environ Microbiol 74(19):5867–5874. https://doi.org/10.1128/aem.00501-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shabala L, Ross T (2008) Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+. Res Microbiol 159(6):458–461

    PubMed  CAS  Google Scholar 

  • Shayanfar S, Broumand A, Pillai SD (2018) Acid stress induces differential accumulation of metabolites in Escherichia coli O26: H11. J Appl Microbiol 125(6):1911–1919

    CAS  Google Scholar 

  • Sina J, Hutchings MI, Thorsten M (2010) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32(1):107–146. https://doi.org/10.1111/j.1574-6976.2007.00091.x

    Article  CAS  Google Scholar 

  • Sochacki KA, Shkel IA, Record MT, Weisshaar JC (2011) Protein diffusion in the periplasm of E. coli under osmotic stress. Biophys J 100(1):22–31

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sohlenkamp C (2017) Membrane homeostasis in bacteria upon pH challenge. Biogenesis of fatty acids, lipids and membranes:1–13

  • Song CW, Kim JW, Cho IJ, Lee SY (2016) Metabolic engineering of Escherichia coli for the production of 3-hydroxypropionic acid and malonic acid through β-alanine route. ACS Synth Biol 5(11):1256–1263

    PubMed  CAS  Google Scholar 

  • Sperandeo P, Martorana AM, Polissi A (2019) Lipopolysaccharide biosynthesis and transport to the outer membrane of Gram-negative bacteria bacterial cell walls and membranes. Springer, pp 9–37

  • Stull F, Hipp H, Stockbridge RB, Bardwell JC (2018) In vivo chloride concentrations surge to proteotoxic levels during acid stress. Nat Chem Biol 14(11):1051–1058

    PubMed  PubMed Central  CAS  Google Scholar 

  • Subbarao GV, van den Berg B (2006) Crystal structure of the monomeric porin OmpG. J Mol Biol 360(4):750–759

    PubMed  CAS  Google Scholar 

  • Tan Z, Black W, Yoon JM, Shanks JV, Jarboe LR (2017a) Improving Escherichia coli membrane integrity and fatty acid production by expression tuning of FadL and OmpF. Microb Cell Factories 16(1):38

    Google Scholar 

  • Tan Z, Clomburg JM, Gonzalez R (2018) Synthetic pathway for the production of olivetolic acid in Escherichia coli. ACS Synth Biol 7(8):1886–1896

    PubMed  CAS  Google Scholar 

  • Tan Z, Khakbaz P, Chen Y, Lombardo J, Yoon JM, Shanks JV, Klauda JB, Jarboe LR (2017b) Engineering Escherichia coli membrane phospholipid head distribution improves tolerance and production of biorenewables. Metab Eng 44:1–12

    PubMed  CAS  Google Scholar 

  • Tan Z, Yoon JM, Nielsen DR, Shanks JV, Jarboe LR (2016) Membrane engineering via trans unsaturated fatty acids production improves Escherichia coli robustness and production of biorenewables. Metab Eng 35:105–113

    PubMed  CAS  Google Scholar 

  • Tapley TL, Franzmann TM, Chakraborty S, Jakob U, Bardwell JC (2010) Protein refolding by pH-triggered chaperone binding and release. P Natl Acad Sci USA 107(3):1071–1076

    CAS  Google Scholar 

  • Tetsch L, Koller C, Haneburger I, Jung K (2008) The membrane-integrated transcriptional activator CadC of Escherichia coli senses lysine indirectly via the interaction with the lysine permease LysP. Mol Microbiol 67(3):570–583

    PubMed  CAS  Google Scholar 

  • Thomas AD, Booth IR (1992) The regulation of expression of the porin gene ompC by acid pH. Microbiology+ 138(9):1829–1835

    CAS  Google Scholar 

  • Todt JC, Rocque WJ, McGroarty EJ (1992) Effects of pH on bacterial porin function. Biochemistry-US 31(43):10471–10478

    CAS  Google Scholar 

  • Tramonti A, De Santis F, Pennacchietti E, De Biase D (2017) The yhiM gene codes for an inner membrane protein involved in GABA export in Escherichia coli. AIMS Microbiol 3:71–87

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tsai M-F, McCarthy P, Miller C (2013) Substrate selectivity in glutamate-dependent acid resistance in enteric bacteria. P Natl Acad Sci USA 110(15):5898–5902

    CAS  Google Scholar 

  • Tsai M-F, Miller C (2013) Substrate selectivity in arginine-dependent acid resistance in enteric bacteria. P Natl Acad Sci USA 110(15):5893–5897

    CAS  Google Scholar 

  • Typas A, Banzhaf M, Gross CA, Vollmer W (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10(2):123

    CAS  Google Scholar 

  • van Straaten KE, Dijkstra BW, Vollmer W, Thunnissen A-MW (2005) Crystal structure of MltA from Escherichia coli reveals a unique lytic transglycosylase fold. J Mol Biol 352(5):1068–1080

    PubMed  Google Scholar 

  • Vivijs B, Aertsen A, Michiels CW (2016) Identification of genes required for growth of Escherichia coli MG1655 at moderately low pH. Front Microbiol 7:1672

    PubMed  PubMed Central  Google Scholar 

  • Vollmer W, Blanot D, De Pedro MA (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32(2):149–167

    PubMed  CAS  Google Scholar 

  • Vollmer W, Seligman SJ (2010) Architecture of peptidoglycan: more data and more models. Trends Microbiol 18(2):59–66

    PubMed  CAS  Google Scholar 

  • Wilks JC, Slonczewski JL (2007) pH of the cytoplasm and periplasm of Escherichia coli: rapid measurement by green fluorescent protein fluorimetry. J Bacteriol 189(15):5601–5607

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biotechnol 39(7):1031–1039

    PubMed  CAS  Google Scholar 

  • Xu J, Li T, Gao Y, Deng J, Gu J (2019) MgrB affects the acid stress response of Escherichia coli by modulating the expression of iraM. FEMS Microbiol Lett 366(11):fnz123. https://doi.org/10.1093/femsle/fnz123

    Article  PubMed  CAS  Google Scholar 

  • Yoon Y, Lee H, Lee S, Kim S, Choi K-H (2015) Membrane fluidity-related adaptive response mechanisms of foodborne bacterial pathogens under environmental stresses. Food Res Int 72:25–36

    CAS  Google Scholar 

  • Yu F, Addison O, Baker SJ, Davenport AJ (2015) Lipopolysaccharide inhibits or accelerates biomedical titanium corrosion depending on environmental acidity. Int J Oral Sci 7(3):179

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan J, Jin F, Glatter T, Sourjik V (2017) Osmosensing by the bacterial PhoQ/PhoP two-component system. P Natl Acad Sci USA 114(50):E10792–E10798

    CAS  Google Scholar 

  • Yuk H-G, Marshall DL (2004) Adaptation of Escherichia coli O157: H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid. Appl Environ Microbiol 70(6):3500–3505

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang M, Lin S, Song X, Liu J, Fu Y, Ge X, Fu X, Chang Z, Chen PR (2011) A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat Chem Biol 7(10):671–677

    PubMed  CAS  Google Scholar 

  • Zhang S, He D, Yang Y, Lin S, Zhang M, Dai S, Chen PR (2016) Comparative proteomics reveal distinct chaperone–client interactions in supporting bacterial acid resistance. P Natl Acad Sci USA 113(39):10872–10877

    CAS  Google Scholar 

  • Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6(3):222

    PubMed  Google Scholar 

  • Zhao B, Houry WA (2010) Acid stress response in enteropathogenic gammaproteobacteria: an aptitude for survival. Biochem Cell Biol 88(2):301–314

    PubMed  CAS  Google Scholar 

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Funding

The work described in this paper was partially supported by a grant with the Grant Nos. 2017YFD0500105 and 2016YFD0500905 from the National Key Research and Development Program of China, grants from the Chinese National Science Foundation Grant (Nos. 31672579, 30571374, 30771603, 31072136, 31270171), a project founded by the Priority Academic Program of Development Jiangsu High Education Institution, grants from Jiangsu Science and Technology Bureau Project (BE2017342), and the Yangzhou Science and Technology Bureau International Cooperation Project (YZ2018154).

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Correspondence to Wenkai Ren or Guoqiang Zhu.

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Li, Z., Jiang, B., Zhang, X. et al. The role of bacterial cell envelope structures in acid stress resistance in E. coli. Appl Microbiol Biotechnol 104, 2911–2921 (2020). https://doi.org/10.1007/s00253-020-10453-x

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