Advances in research progress on acid tolerance mechanism of Gram- negative bacteria mediated by molecular chaperone protein

ZHU Hao; LIU Nan

doi:10.11665/j.issn.1000-5048.20210204

Journal of China Pharmaceutical University > 2021 > 52(2): 164-170. > DOI: 10.11665/j.issn.1000-5048.20210204

ZHU Hao, LIU Nan. Advances in research progress on acid tolerance mechanism of Gram- negative bacteria mediated by molecular chaperone protein[J]. Journal of China Pharmaceutical University, 2021, 52(2): 164-170. DOI: 10.11665/j.issn.1000-5048.20210204

Citation:

PDF (851 KB)

Advances in research progress on acid tolerance mechanism of Gram- negative bacteria mediated by molecular chaperone protein

ZHU Hao,
LIU Nan

School of Life Science and Technology, China Pharmaceutical University,Nanjing 210009, China

Funds: This study was supported the National Key Research and Development Program of China (No.2018YFA0902000)

More Information

Received Date: May 03, 2020
Revised Date: March 07, 2021

Graphical Abstract

Abstract

Abstract

The tolerance of microorganism under acid stress is of significant importance to the growth and industrial production of bacterial strain. When the bacterial cells are exposed to the external acid environment, proteins in periplasmic space are under higher acid stress and are thusmore susceptible to severe damage from acid than the intracellular protein, and these are also more susceptible to severe damage from acid than the intracellular protein. During the acid-resisting process of Gram-negative bacteria, in addition to the intracellular decarboxylase system, the molecular chaperone can also participate in the identification and protection of the space structure of protein as an important "correcting" mechanism. This paper, reviews the current researches on the function, structure, acid-resisting mechanism of variousmolecular chaperones, including HdeA, HdeB, DnaK and GroEL. Finally, the research progress of the acid-resisting mechanism among Gram-negative bacteria is summarized. Through in-depth investigation and analysis of the physiological adaptation strategy of molecular chaperone to the acid stress environment, this study can help to conduct physiological property modification of target strain and improve their viability and tolerance in acid stress environment, which has its important theoretical and practical significance.
- Gram-negative bacteria,
- E. coli,
- acid stress,
- periplasmic space,
- molecular chaperone,
- advance

FullText(HTML)

References (54)

References

[1]	. Science， 2014， 346（6205）： 35-36.
[2]	Xu Y， Zhao Z， Tong W， et al. An acid-tolerance response system protecting exponentially growing Escherichia coli ［J］. Nat Commun， 2020， 11（1）： 1496.
[3]	Nguyen TY， Cai CM， Kumar R， et al. Overcoming factors limiting high-solids fermentation of lignocellulosic biomass to ethanol ［J］. Proc Natl Acad Sci U S A， 2017， 114（44）： 11673-11678.
[4]	Li S， Giardina DM， Siegal ML. Control of nongenetic heterogeneity in growth rate and stress tolerance of Saccharomyces cerevisiae by cyclic AMP-regulated transcription factors ［J］. PLoS Genetics， 2018， 14（11）： e1007744.
[5]	Kanjee U， Houry WA. Mechanisms of acid resistance in Escherichia coli ［J］. Annu Rev Microbiol， 2013， 67： 65-81.
[6]	Sun Y， Fukamachi T， Saito H， et al. Respiration and the F?Fo-ATPase enhance survival under acidic conditions in Escherichia coli ［J］. PLoS One， 2012， 7（12）： e52577.
[7]	Pennacchietti E， D''alonzo C， Freddi L， et al. The glutaminase-dependent acid resistance system： qualitative and quantitative assays and analysis of its distribution in enteric bacteria ［J］. Front Microbiol， 2018， 9： 2869.
[8]	Wollmann P， Zeth K. The structure of RseB： a sensor in periplasmic stress response of E. coli ［J］. J Molecul Biol， 2007， 372（4）： 927-941.
[9]	Merdanovic M， Clausen T， Kaiser M， et al. Protein quality control in the bacterial periplasm ［J］. Annu Rev Microbiol， 2011， 65： 149-168.
[10]	Sklar JG， Wu T， Kahne D， et al. Defining the roles of the periplasmic chaperones SurA， Skp， and DegP in Escherichia coli ［J］. Genes Dev， 2007， 21（19）： 2473-2484.
[11]	Hartl FU， Bracher A， HayerHartl M. Molecular chaperones in protein folding and proteostasis ［J］. Nature， 2011， 475（7356）： 324-332.
[12]	Willmund F， Del Alamo M， Pechmann S， et al. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis ［J］. Cell， 2013， 152（1/2）： 196-209.
[13]	B?ttinger L， Oeljeklaus S， Guiard B， et al. Mitochondrial heat shock protein （Hsp） 70 and Hsp10 cooperate in the formation of Hsp60 complexes ［J］. J Biol Chem， 2015， 290（18）： 11611-11622.
[14]	Rani S， Sharma A， Goel M. Insights into archaeal chaperone machinery： a network-based approach ［J］. Cell Stress Chaperones， 2018， 23（6）： 1257-1274.
[15]	Li X， Shao H， Taylor IR， et al. Targeting allosteric control mechanisms in heat shock protein 70 （Hsp70）［J］. Curr Top Med Chem， 2016， 16（25）： 2729-2740.
[16]	Yang J， Zong Y， Su J， et al. Conformation transitions of the polypeptide-binding pocket support an active substrate release from Hsp70s ［J］. Nat Commun， 2017， 8（1）： 1201.
[17]	BudinaKolomets A， Webster MR， Leu JJ， et al. HSP70 inhibition limits FAK-dependent invasion and enhances the response to melanoma treatment with BRAF inhibitors ［J］. Cancer Res， 2016， 76（9）： 2720-2730.
[18]	Ellison MA， Ferrier MD， Carney SL. Salinity stress results in differential Hsp70 expression in the exaiptasia pallida and symbiodinium symbiosis ［J］. Mar Environ Res， 2017， 132： 63-67.
[19]	Kumar S， Stokes J， Singh UP， et al. Targeting Hsp70： a possible therapy for cancer ［J］. Cancer Lett， 2016， 374（1）： 156-166.
[20]	Reeg S， Jung T， Castro JP， et al. The molecular chaperone Hsp70 promotes the proteolytic removal of oxidatively damaged proteins by the proteasome ［J］. Free Radic Biol Med， 2016， 99： 153-166.
[21]	Meng Q， Li BX， Xiao X. Toward developing chemical modulators of Hsp60 as potential therapeutics ［J］. Front Mol Biosci， 2018， 20： 5-35.
[22]	Marino Gammazza A， Macaluso F， Di FeliceV， et al. Hsp60 in skeletal muscle fiber biogenesis and homeostasis： from physical exercise to skeletal muscle pathology ［J］. Cells， 2018， 7（12）： 224.
[23]	Gajiwala KS， Burley SK. HDEA， a periplasmic protein that supports acid resistance in pathogenic enteric bacteria ［J］. J Biol Chem， 2000， 295（3）： 605-612.
[24]	Wang W， Rasmussen T， Harding AJ， et al. Salt bridges regulate both dimer formation and monomeric flexibility in HdeB and may have a role in periplasmic chaperone function ［J］. J Biol Chem， 2012， 415（3）： 538-546.
[25]	Tapley TL， K?rner JL， Barge MT， et al. Structural plasticity of an acid-activated chaperone allows promiscuous substrate binding ［J］. Proc Natl Acad Sci U S A， 2009， 106（14）： 5557-5562.
[26]	Guan N， Liu L. Microbial response to acid stress： mechanisms and applications ［J］. Appl Microbiol Biotechnol， 2020， 104（1）： 51-65.
[27]	Yu XC， Hu Y， Ding J， et al. Structural basis and mechanism of the unfolding-induced activation of HdeA， a bacterial acid response chaperone ［J］. J Biol Chem， 2019， 294（9）： 3192-3206.
[28]	Zhang M， Lin S， Song X， et al. A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance ［J］. Nat Chem Biol， 2011， 7（10）： 671-677.
[29]	Kern R， Malki A， Abdallah J， et al. Escherichia coli HdeB is an acid stress chaperone ［J］. J Bacteriol， 2007， 189（2）： 603-610.
[30]	Zhang S， He D， Yang Y， et al. Comparative proteomics reveal distinct chaperone-client interactions in supporting bacterial acid resistance ［J］. Proc Natl Acad Sci U S A， 2016， 113（39）： 10872-10877.
[31]	Libich DS， Tugarinov V， Clore GM. Intrinsic unfoldase/foldase activity of the chaperonin GroEL directly demonstrated using multinuclear relaxation-based NMR ［J］. Proc Natl Acad Sci U S A， 2015， 112（29）： 8817-8823.
[32]	W?lti MA， Steiner J， Meng F， et al. Probing the mechanism of inhibition of amyloid-β（1-42）-induced neurotoxicity by the chaperonin GroEL ［J］. Proc Natl Acad Sci U S A， 2018， 115（51）： E11924-E11932.
[33]	Feng S， Yang H， Wang W. System-level understanding of the potential acid-tolerance components of Acidithiobacillus thiooxidans ZJJN-3 under extreme acid stress ［J］. Extremophiles， 2015， 19（5）： 1029-1039.
[34]	Kaspar J， Kim JN， Ahn SJ， et al. An essential role for （p）ppGpp in the integration of stress tolerance， peptide signaling， and competence development in Streptococcus mutans ［J］. Front Microbiol， 2016， 7： 1162.
[35]	Dahiya V， Chaudhuri TK. Chaperones GroEL/GroES accelerate the refolding of a multidomain protein through modulating on-pathway intermediates ［J］. J Biol Chem， 2014， 289（1）： 286-298.
[36]	Jewett AI， Shea JE. Reconciling theories of chaperonin accelerated folding with experimental evidence ［J］. Cell Mol Life Sci， 2010， 67（2）： 255-276.
[37]	Zanotti G， Cendron L. Functional and structural aspects of helicobacter pylori acidic stress response factors ［J］. IUBMB Life， 2010， 62（10）： 715-723.
[38]	AlM Abdullah， Sugimoto S， Higashi C， et al. Improvement of multiple-stress tolerance and lactic acid production in Lactococcus lactis NZ9000 under conditions of thermal stress by heterologous expression of Escherichia coli DnaK ［J］. Appl Environ Microbiol， 2010， 76（13）： 4277-4285.
[39]	Vinusha KS， Deepika K， Johnson TS， et al. Proteomic studies on lactic acid bacteria： a review ［J］. Biochem Biophys Rep， 2018， 14： 140-148.
[40]	Arunima A， Swain SK， Ray S， et al. RpoS-regulated gene promotes resistance to stress and influences Salmonella enterica serovar enteritidis virulence ［J］. Virulence， 2020， 11（1）： 295-314.
[41]	Chen C， Choudhury A， Zhang S， et al. Integrating CRISPR-enabled trackable genome engineering and transcriptomic analysis of global regulators for antibiotic resistance selection and identification in Escherichia coli ［J］. mSystems， 2020， 5（2）： e00232-20.
[42]	Basak S， Geng H， Jiang R. Rewiring global regulator cAMP receptor protein （CRP） to improve E. coli tolerance towards low pH ［J］. J Biotechnol， 2014， 173： 68-75.
[43]	Dorman CJ. H-NS-like nucleoid-associated proteins， mobile genetic elements and horizontal gene transfer in bacteria ［J］. Plasmid， 2014， 75： 1-11
[44]	Shin M， Song M， Rhee JH， et al. DNA looping-mediated repression by histone-like protein H-NS： specific requirement of esigma70 as a cofactor for looping ［J］. Genes Dev， 2005， 19（19）： 2388-2398.
[45]	Gao X， Yang X， Li J， et al. Engineered global regulator H-NS improves the acid tolerance of E. coli ［J］. Microb Cell Fact， 2018， 17（1）： 118.
[46]	Shilling RA， Venter H， Velamakanni S， et al. New light on multidrug binding by an ATP-binding-cassette transporter ［J］. Trends Pharmacol Sci， 2006， 27（4）： 195-203.
[47]	Ford RC， Beis K. Learning the ABCs one at a time： structure and mechanism of ABC transporters ［J］. Biochem Soc Trans， 2019， 47（1）： 23-36.
[48]	Zhu Z， Yang J， Yang P， et al. Enhanced acid-stress tolerance in Lactococcus lactis NZ9000 by overexpression of ABC transporters ［J］. Microb Cell Fact， 2019， 18（1）： 136.
[49]	Robinson T， Smith P， Alberts ER， et al. Cooperation and cheating through a secreted aminopeptidase in the pseudomonas aeruginosa RpoS response ［J］. mBio， 2020， 11（2）： e03090-e03119.
[50]	Seo SW， Kim D， O''brien E J， et al. Decoding genome-wide GadEWX-transcriptional regulatory networks reveals multifaceted cellular responses to acid stress in Escherichia coli ［J］. Nat Commun， 2015， 6： 7970.
[51]	Liu CJ， Lin CT， Chiang JD， et al. RcsB regulation of the YfdX-mediated acid stress response in Klebsiella pneumoniae CG43S3 ［J］. PLoS One， 2019， 14（2）： e0212909.
[52]	Sen H， Aggarwal N， Ishionwu C， et al. Structural and functional analysis of the Escherichia coli acid-sensing histidine kinase EvgS ［J］. J Bacteriol， 2017， 199（18）：e00310-e00317.
[53]	Oglesby AG， Murphy ER， Iyer VR， et al. Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP ［J］. Mol Microbiol， 2005， 58（5）： 1354-1367.
[54]	Xu N， Lv H， Wei L， et al. Impaired oxidative stress and sulfur assimilation contribute to acid tolerance of Corynebacterium glutamicum ［J］. Appl Microbiol Biotechnol， 2019， 103（4）： 1877-1891.

Cited By

Cited by

Periodical cited type(3)

1.	胡彤，李爽，钟卫鸿. 基于酸信号转导系统的细菌耐酸机制及其应用. 生物工程学报. 2024(03): 644-664 .
2.	吴晓妍，吴剑梅，傅丹丹，涂健，宋祥军，邵颖，祁克宗. hipA对禽致病性大肠杆菌生物学特性和致病性的影响. 西北农林科技大学学报(自然科学版). 2023(08): 11-18+28 .
3.	郝雪雁，刘梦晓，韩紫依，房立霞，曹英秀. 大肠杆菌的耐酸机制及其改造研究进展. 微生物学通报. 2023(10): 4667-4680 .

Other cited types(1)

Get Citation

PDF

XML

Article views (223) PDF downloads (1041) Cited by(4)

Turn off MathJax

Article Contents

Abstract

References

Advances in research progress on acid tolerance mechanism of Gram- negative bacteria mediated by molecular chaperone protein

Abstract

References

Cited by

Periodical cited type(3)

Other cited types(1)

Catalog

Export File

Citation

Format

Content