Toxicity and inhibition mechanism of gallic acid on physiology and fermentation performance of Escherichia coli

Lina Liu , Xiaolong Ma , Muhammad Bilal , Linlin Wei , Shijie Tang , Hongzhen Luo , Yuping Zhao , Zhaoyu Wang , Xuguo Duan

Bioresources and Bioprocessing ›› 2022, Vol. 9 ›› Issue (1) : 76

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Bioresources and Bioprocessing ›› 2022, Vol. 9 ›› Issue (1) : 76 DOI: 10.1186/s40643-022-00564-w
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Toxicity and inhibition mechanism of gallic acid on physiology and fermentation performance of Escherichia coli

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Abstract

Gallic acid is a natural phenolic acid that has a stress inhibition effect on Escherichia coli. This study by integrates fermentation characteristics and transcriptional analyses to elucidate the physiological mechanism of E. coli 3110 response to gallic acid. Compared with the control (without stress), the cell growth was severely retarded, and irregular cell morphology appeared in the case of high levels of gallic acid stress. The glucose consumption of E. coli was reduced successively with the increase of gallic acid content in the fermentation medium. After 20 h of gallic acid stress, cofactor levels (ATP, NAD+ and NADH) of E. coli 3110 were similarly decreased, indicating a more potent inhibitory effect of gallic acid on E. coli. The transcriptional analysis revealed that gallic acid altered the gene expression profiles related to five notable differentially regulated pathways. The genes related to the two-component system were up-regulated, while the genes associated with ABC-transporter, energy metabolism, carbon metabolism, and fatty acid biosynthesis were down-regulated. This is the first report to comprehensively assess the toxicity of gallic acid on E. coli. This study has implications for the efficient production of phenolic compounds by E. coli and provides new ideas for the study of microbial tolerance to environmental stress and the identification of associated tolerance targets.

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Escherichia coli / Gallic acid / Physiological mechanism / Fermentation characteristics / Transcriptional analysis

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Lina Liu, Xiaolong Ma, Muhammad Bilal, Linlin Wei, Shijie Tang, Hongzhen Luo, Yuping Zhao, Zhaoyu Wang, Xuguo Duan. Toxicity and inhibition mechanism of gallic acid on physiology and fermentation performance of Escherichia coli. Bioresources and Bioprocessing, 2022, 9(1): 76 DOI:10.1186/s40643-022-00564-w

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References

[1]

Ba A, Fa A, Maab C, Man D, Hn A, Aa B, Rb E, Rmaf G, Ui A, Nc H. Genome-wide identification and expression analysis of two component system genes in Cicer arietinum. Genomics, 2020, 112: 1371-1383.

[2]

Bhattacharjee A, Chetri S, Bhowmik D. Transcriptional response of OmpC and OmpF in Escherichia coli against differential gradient of carbapenem stress. BMC Res Notes, 2019, 12: 138.

[3]

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 1976, 72: 248-254.

[4]

Che LR, He ZB, Liu Y, Yan ZT, Han BZ, Chen XJ, He XF, Zhang J, Chen B, Qiao L. Electroporation-mediated nucleic acid delivery during non-embryonic stages for gene-function analysis in Anopheles sinensis-ScienceDirect. Insect Biochem Mol Biol, 2020, 128: 103500.

[5]

Chen Z, Shen X, Wang J, Wang J, Yuan Q, Yan Y. Rational engineering of p-Hydroxybenzoate hydroxylase to enable efficient gallic acid synthesis via a novel artificial biosynthetic pathway. Biotechnol Bioeng, 2017, 114: 2571-2580.

[6]

Cronan JE. The classical, yet controversial, first enzyme of lipid synthesis: escherichia coli acetyl-CoA carboxylase. Microbiol Mol Biol R, 2021

[7]

DíAz E, Ferrández A, Prieto MA, Garcí J. Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev, 2001, 65(4): 523-569.

[8]

Falero A, Serrano Y, Rodríguez S, Brito S, Marrero K. Scanning electron microscopy as a useful tool for monitoring cell disruption of recombinant Escherichia coli SHuffle T7. Microsc Microanal, 2020, 26: 145.

[9]

Fang L, Fan J, Luo S, Chen Y, Song H. Genome-scale target identification in Escherichia coli for high-titer production of free fatty acids. Nat Commun, 2021

[10]

Feng SX, Zhu L, Luo B, Sun YR, Wang HH. Reconstitution of Escherichia coli fatty acid biosynthesis reaction in vitro. Prog Biochem Biophys, 2008, 35: 954-963.

[11]

Green DR, Galluzzi L, Kroemer G. Metabolic control of cell death. Science, 2014, 345: 1250256.

[12]

Gu H, Zhang J, Bao J. High tolerance and physiological mechanism of Zymomonas mobilis to phenolic inhibitors in ethanol fermentation of corncob residue. Biotechnol Bioeng, 2015, 112: 1770-1782.

[13]

Guo L, Diao W, Gao C, Hu G, Ding Q, Ye C, Chen X, Liu J, Liu L. Engineering Escherichia coli lifespan for enhancing chemical production. Nat Catal, 2020, 3: 307-318.

[14]

Hill RB, Mackenzie KR, Flanagan JM, Cronan JE, Prestegard JH. Overexpression, purification, and characterization of Escherichia coli acyl carrier protein and 2 mutant proteins. Protein Expres Purif, 1995, 6: 394-400.

[15]

Hoeser J, Hong S, Gehmann G, Gennis RB, Friedrich T. Subunit CydX of Escherichia coli cytochrome bd ubiquinol oxidase is essential for assembly and stability of the di-heme active site. Febs Lett, 2014, 588: 1537-1541.

[16]

Hollenstein K, Dawson RJ, Locher KP. Structure and mechanism of ABC transporter proteins—ScienceDirect. Curr Opin Struct Biol, 2007, 17: 412-418.

[17]

Hou J, Scalcinati G, Oldiges M, Vemuri GN. Metabolic impact of increased NADH availability in Saccharomyces cerevisiae. Appl Environ Microbiol, 2010, 76: 851-859.

[18]

Igwe JC, Busayo O, Ehnimidu JO, Josiah AO. Impact of outer membrane protein OmpC and OmpF on antibiotics resistance of E. coli Isolated from UTI and diarrhoeic patients in Zaria. Nigeria. Clin Microbiol, 2016, 5: 6.

[19]

Jiang Y, Zheng T, Ye X, Xin F, Jiang M. Metabolic engineering of Escherichia coli for L-malate production anaerobically. Microb Cell Fact, 2020

[20]

Jones MM, Murphy TF, Mccormick BA. Expression of the oligopeptide permease operon of Moraxella catarrhalis is regulated by temperature and nutrient availability. Infect Immun, 2015, 83: 3497-3505.

[21]

Jozefczuk S, Klie S, Catchpole G, Szymanski J, Willmitzer L. Metabolomic and transcriptomic stress response of Escherichia coli. Mol Syst Biol, 2014, 6: 364.

[22]

Kambourakis S, Draths KM, Frost JW. Synthesis of gallic acid and pyrogallol from glucose: replacing natural product isolation with microbial catalysis. J Am Chem Soc, 2000, 122: 8-17.

[23]

Li H, Wang B, Zhu L, Cheng S, Li Y, Zhang L, Ding ZY, Gu ZH, Shi GY. Metabolic engineering of Escherichia coli W3110 for L-homoserine production. Process Biochem, 2016, 51: 1973-1983.

[24]

Li W, Wu H, Li M, San KY. Effect of NADPH availability on free fatty acid production in E. coli. Biotechnol Bioeng, 2018, 115: 444-542.

[25]

Li J, Liu D, Ding T. Transcriptomic analysis reveal differential gene expressions of Escherichia coli O157:H7 under ultrasonic stress. Ultrason Sonochem, 2021, 71.

[26]

Limpisophon K, Schleining G. Use of gallic acid to enhance the antioxidant and mechanical properties of active fish gelatin film. J Food Sci, 2016, 82: 80-89.

[27]

Lin X, Qi Y, Yan D, Hui L, Liu L. CgMED3 Changes membrane sterol composition to help Candida glabrata tolerate low-pH stress. Appl Environ Microbiol, 2017, 83(17): e00972-e1017.

[28]

Liu L, Duan X, Wu J. L-Tryptophan production in Escherichia coli improved by weakening the Pta-AckA pathway. PLoS ONE, 2016, 11.

[29]

Liu L, Duan X, Wu J. Modulating the direction of carbon flow in Escherichia coli to improve L-tryptophan production by inactivating the global regulator FruR. J Biotechnol, 2016, 231: 141-148.

[30]

Liu J, Lin QL, Chai XY, Luo YC, Guo T. Enhanced phenolic compounds tolerance response of Clostridium beijerinckii NCIMB 8052 by inactivation of Cbei_3304. Microb Cell Fact, 2018, 17: 35.

[31]

Liu M, Liu H, Shi M, Jiang M, Zheng Y. Microbial production of ectoine and hydroxyectoine as high-value chemicals. Microb Cell Fact, 2021

[32]

Marzorati F, Wang C, Pavesi G, Mizzi L, Morandini P. Cleaning the medicago microarray database to improve gene function analysis. Plants, 2021, 10: 1240.

[33]

Mills TY, Sandoval NR, Gill RT. Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol Biofuels, 2009, 2: 26-26.

[34]

Mishra P, Jain A, Takabe T, Tanaka Y, Negi M, Singh N, Jain N, Mishra V, Maniraj R, Krishnamurthy SL. Heterologous expression of serine hydroxymethyltransferase-3 from rice confers tolerance to salinity stress in E. coli and arabidopsis. Front Plant Sci, 2019, 10: 217.

[35]

Niu K, Xu YY, Wu WJ, Zhou HY, Liu ZQ, Zheng YG. Effect of dissolved oxygen on L-methionine production from glycerol by Escherichia coli W3110BL using metabolic flux analysis method. J InDl Microb Biot, 2020, 47: 287-297.

[36]

Noronha SB, Yeh H, Spande TF, Shiloach J. Investigation of the TCA cycle and the glyoxylate shunt in Escherichia coli BL21 and JM109 using (13)C-NMR/MS. Biotechnol Bioeng, 2015, 68: 316-327.

[37]

Oliveira C, Stamford T, Neto N, Souza E. Inhibition of Staphylococcus aureus in broth and meat broth using synergies of phenolics and organic acids. Int J Food Microb, 2010, 137: 312-316.

[38]

Osorio H, Carvalho E, Valle MD, Günther Sillero MA, Moradas-Ferreira P, Sillero A. H2O2, but not menadione, provokes a decrease in the ATP and an increase in the inosine levels in Saccharomyces cerevisiae. Eur J Biochem, 2003, 270: 1578-1589.

[39]

Papon N, Stock AM. Two-component systems. Curr Biol, 2019, 29: R724-R725.

[40]

Pontrelli S, Chiu TY, Lan EI, Chen FY, Chang PC, Liao JC. Escherichia coli as a host for metabolic engineering. Metab Eng, 2018, 50: 16-46.

[41]

Qi Y, Liu H, Yu J, Chen X, Liu L. Med15B regulates acid stress response and tolerance in Candida glabrata. Appl Environ Microbiol, 2017, 83(18): e01128-e1217.

[42]

Rewatkar K, Shende DZ, Wasewar KL. Effect of temperature on reactive extraction of gallic acid using trinbutyl phosphate, trinoctylamine and aliquat 336. J Chem Eng Data, 2016, 61: 3217-3224.

[43]

Satoh S, Ozaki M, Matsumoto S, Nabatame T, Chohnan S. Enhancement of fatty acid biosynthesis by exogenous acetyl-CoA carboxylase and pantothenate kinase in Escherichia coli. Biotechnol Lett, 2020, 42: 2595-2605.

[44]

Tassou CC, Nychas GJE. Inhibition of Staphylococcus aureus by olive phenolics in broth and in a model food system. J Food Protect, 1994, 57: 120-124.

[45]

Thomanek N, Arends J, Lindemann C, Barkovits K, Narberhaus F. Intricate crosstalk between lipopolysaccharide, phospholipid and fatty acid metabolism in Escherichia coli modulates proteolysis of LpxC. Front Microbiol, 2019, 9: 3285.

[46]

Voordouw G. Evolution of hydrogenase genes. Adv Inorg Chem, 1992, 38: 397-422.

[47]

Wang XG, Lin B, Kidder JM, Telford S, Hu LT. Effects of environmental changes on expression of the oligopeptide permease (opp) genes of Borrelia burgdorferi. J Bacteriol, 2002, 184: 6198-6198.

[48]

Wang Q, Zhou K, Ning Y, Zhao G. Effect of the structure of gallic acid and its derivatives on their interaction with plant ferritin. Food Chem, 2016, 213: 260-267.

[49]

Wang J, Shen X, Rey J, Yuan Q, Yan Y. Recent advances in microbial production of aromatic natural products and their derivatives. Appl Microbiol Biotechnol, 2017, 102: 47-61.

[50]

Wang S, Fang Y, Wang Z, Zhang S, Wang X. Improving L-threonine production in Escherichia coli by elimination of transporters ProP and ProVWX. Microb Cell Fact, 2021, 20: 58.

[51]

Wenk S, Schann K, He H, Rainaldi V, Kim S, Lindner S, Bar-Even A. An "energy゛uxotroph" E. coli provides an in vivo platform for assessing NADH regeneration systems. Biotechnol Bioeng, 2020, 117: 3422-3434.

[52]

Yan D, Lin X, Qi Y, Hui L, Jian C. Crz1p regulates pH homeostasis in Candida glabrata by altering membrane lipid composition. Appl Environ Microbiol, 2016, 82: 6920-6929.

Funding

Innovative Research Group Project of the National Natural Science Foundation of China(21808075)

Natural Science Foundation of Jiangsu Province(BK20170459)

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