The Soluble Transhydrogenase UdhA Affecting the Glutamate-dependent Acid Resistance System of Under Acetate Stress

Overview

Journal Biol Open

Specialty Biology

Date 2018 Sep 12

PMID 30201831

Citations 4

Authors

Hanjun Zhao

Feng Zhou

Quan Xing

Zhengyu Cao

Jie Liu

Guoping Zhu

Affiliations

Soon will be listed here.

Abstract

The soluble transhydrogenase (UdhA) is one of two transhydrogenases that play a role in maintaining the balance between NAD(H) pools and NADP(H) pools in Although UdhA has been extensively used in metabolic engineering and biocatalysis for cofactor regeneration, its role in acid resistance has not been reported. Here we used DNA microarray to explore the impact of UdhA on transcript levels. We demonstrated that during growth on acetate, the expression of genes involved in the respiratory chain and Gad acid resistance system was inhibited in the -knockout strain. The deletion of significantly repressed the expression of six genes ( and ) which are involved in Gad acid resistance and resulted in low survival of the bacterium at a low pH of 4.9. Moreover, UdhA was essential for NADH production which is important for the adaptive growth of on acetate, while NADH concentration in the -knockout strain was quite low and supplemental NADH significantly increased the expression of acid resistance genes and survival of the -knockout strain. These results demonstrated that UdhA is an important source of NADH of growth on acetate and affects Gad acid resistance system under acetate stress.

Citing Articles

A genetically encoded tool to increase cellular NADH/NAD ratio in living cells.

Pan X, Heacock M, Abdulaziz E, Violante S, Zuckerman A, Shrestha N Nat Chem Biol. 2023; 20(5):594-604.

PMID: 37884806 PMC: 11045668. DOI: 10.1038/s41589-023-01460-w.

Division of labor and collective functionality in Escherichia coli under acid stress.

Brameyer S, Schumacher K, Kuppermann S, Jung K Commun Biol. 2022; 5(1):327.

PMID: 35393532 PMC: 8989999. DOI: 10.1038/s42003-022-03281-4.

Comparative Review of the Responses of and to Low pH Stress.

Arcari T, Feger M, Guerreiro D, Wu J, OByrne C Genes (Basel). 2020; 11(11).

PMID: 33187233 PMC: 7698193. DOI: 10.3390/genes11111330.

SdiA Improves the Acid Tolerance of by Regulating GadW and GadY Expression.

Ma X, Zhang S, Xu Z, Li H, Xiao Q, Qiu F Front Microbiol. 2020; 11:1078.

PMID: 32582066 PMC: 7286202. DOI: 10.3389/fmicb.2020.01078.

References

Voordouw G, Van Der Vies S, Themmen A . Why are two different types of pyridine nucleotide transhydrogenase found in living organisms?. Eur J Biochem. 1983; 131(3):527-33. DOI: 10.1111/j.1432-1033.1983.tb07293.x. View

Canonaco F, Hess T, Heri S, Wang T, Szyperski T, Sauer U . Metabolic flux response to phosphoglucose isomerase knock-out in Escherichia coli and impact of overexpression of the soluble transhydrogenase UdhA. FEMS Microbiol Lett. 2001; 204(2):247-52. DOI: 10.1111/j.1574-6968.2001.tb10892.x. View

Bi H, Sun L, Fukamachi T, Saito H, Kobayashi H . HU participates in expression of a specific set of genes required for growth and survival at acidic pH in Escherichia coli. Curr Microbiol. 2009; 58(5):443-8. DOI: 10.1007/s00284-008-9340-4. View

Price S, Wright J, DeGraves F, Castanie-Cornet M, Foster J . Acid resistance systems required for survival of Escherichia coli O157:H7 in the bovine gastrointestinal tract and in apple cider are different. Appl Environ Microbiol. 2004; 70(8):4792-9. PMC: 492388. DOI: 10.1128/AEM.70.8.4792-4799.2004. View

Kern R, Malki A, Abdallah J, Tagourti J, Richarme G . Escherichia coli HdeB is an acid stress chaperone. J Bacteriol. 2006; 189(2):603-10. PMC: 1797394. DOI: 10.1128/JB.01522-06. View

Heuser F, Marin K, Kaup B, Bringer S, Sahm H . Improving d-mannitol productivity of Escherichia coli: impact of NAD, CO2 and expression of a putative sugar permease from Leuconostoc pseudomesenteroides. Metab Eng. 2009; 11(3):178-83. DOI: 10.1016/j.ymben.2009.01.006. View

Calhoun M, Gennis R . Demonstration of separate genetic loci encoding distinct membrane-bound respiratory NADH dehydrogenases in Escherichia coli. J Bacteriol. 1993; 175(10):3013-9. PMC: 204620. DOI: 10.1128/jb.175.10.3013-3019.1993. View

Tucker D, Tucker N, Conway T . Gene expression profiling of the pH response in Escherichia coli. J Bacteriol. 2002; 184(23):6551-8. PMC: 135413. DOI: 10.1128/JB.184.23.6551-6558.2002. View

Penfound T, Smith D, Elliott J, FOSTER J . Control of acid resistance in Escherichia coli. J Bacteriol. 1999; 181(11):3525-35. PMC: 93821. DOI: 10.1128/JB.181.11.3525-3535.1999. View

10.

Richard H, Foster J . Acid resistance in Escherichia coli. Adv Appl Microbiol. 2003; 52:167-86. DOI: 10.1016/s0065-2164(03)01007-4. View

11.

Lin J, Smith M, Chapin K, Baik H, Bennett G, FOSTER J . Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol. 1996; 62(9):3094-100. PMC: 168100. DOI: 10.1128/aem.62.9.3094-3100.1996. View

12.

Blattner F, Plunkett 3rd G, Bloch C, Perna N, Burland V, Riley M . The complete genome sequence of Escherichia coli K-12. Science. 1997; 277(5331):1453-62. DOI: 10.1126/science.277.5331.1453. View

13.

Hansen A, Qiu Y, Yeh N, Blattner F, Durfee T, Jin D . SspA is required for acid resistance in stationary phase by downregulation of H-NS in Escherichia coli. Mol Microbiol. 2005; 56(3):719-34. DOI: 10.1111/j.1365-2958.2005.04567.x. View

14.

Cusa E, Obradors N, Baldoma L, Badia J, Aguilar J . Genetic analysis of a chromosomal region containing genes required for assimilation of allantoin nitrogen and linked glyoxylate metabolism in Escherichia coli. J Bacteriol. 1999; 181(24):7479-84. PMC: 94204. DOI: 10.1128/JB.181.24.7479-7484.1999. View

15.

Jaworowski A, Campbell H, Poulis M, Young I . Genetic identification and purification of the respiratory NADH dehydrogenase of Escherichia coli. Biochemistry. 1981; 20(7):2041-7. DOI: 10.1021/bi00510a047. View

16.

Stincone A, Daudi N, Rahman A, Antczak P, Henderson I, Cole J . A systems biology approach sheds new light on Escherichia coli acid resistance. Nucleic Acids Res. 2011; 39(17):7512-28. PMC: 3177180. DOI: 10.1093/nar/gkr338. View

17.

Meng S, Bennett G . Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol. 1992; 174(8):2659-69. PMC: 205906. DOI: 10.1128/jb.174.8.2659-2669.1992. View

18.

Lochowska A, Iwanicka-Nowicka R, Zaim J, Witkowska-Zimny M, Bolewska K, Hryniewicz M . Identification of activating region (AR) of Escherichia coli LysR-type transcription factor CysB and CysB contact site on RNA polymerase alpha subunit at the cysP promoter. Mol Microbiol. 2004; 53(3):791-806. DOI: 10.1111/j.1365-2958.2004.04161.x. View

19.

Zhang J, Hellwig P, Osborne J, Gennis R . Arginine 391 in subunit I of the cytochrome bd quinol oxidase from Escherichia coli stabilizes the reduced form of the hemes and is essential for quinol oxidase activity. J Biol Chem. 2004; 279(52):53980-7. DOI: 10.1074/jbc.M408626200. View

20.

Bearson S, Bearson B, FOSTER J . Acid stress responses in enterobacteria. FEMS Microbiol Lett. 1997; 147(2):173-80. DOI: 10.1111/j.1574-6968.1997.tb10238.x. View