Home > Archive>Volume 61, Issue 8, 2021 >2278-2293. DOI:10.13343/j.cnki.wsxb.20200623
PDF HTML XML Export Cite reminder
Advances in protein lipoylation pathways in bacteria
Author:
  • Article
    • | |
  • Metrics
    • |
  • Reference [57]
    • |
  • Related [20]
    • |
  • Cited by
    • | |
  • Comments
    Abstract:

    Lipoic acid is a derivative of octanoic acid with two sulfur atoms at carbon atoms 6 and 8. The strong antioxidant activity of lipoic acid makes it have a good application prospect in the fields of health food, cosmetics and medicine. Lipoic acid as an important cofactor is required for several key enzymes complexes, like α-ketoacid dehydrogenase, and it also involves in energy generation and intermediate metabolisms. The protein lipoylation pathways have been well studied in the model organism Escherichia coli, including the lipoic acid de novo synthetic pathway dependent on LipB-LipA and the lipoic acid salvage pathway dependent on LplA. However, the lipoylation pathways in different bacteria show a highly diversity. The GcvH protein in certain bacteria also participates in protein lipoylation eventhough the related enzymes are different. In this review, we comprehensively discussed the current research progress on lipoic acid dependent multiple enzyme complexes, the lipoyl domain, GcvH proteins, as well as the protein lipoylation pathways in differen bacteria, aiming to provide theoretical support for further understanding the protein lipoylation in bacteria, developing the targeted antibacterial drugs, and efficient lipoic acid production with biological methods.

    Reference
    [1] Reed KE, Cronan JE. Lipoic acid metabolism in Escherichia coli:sequencing and functional characterization of the lipA and lipB genes. Journal of Bacteriology, 1993, 175(5):1325-1336.
    [2] Liao DF, Chen JW, Xie P, Zhu ZQ, Xu R. Studies on the antioxidation effects of alpha-lipoic acid and dihydrolipoic acid. Journal of East China Normal University:Natural Science, 2007(2):87-92, 136. (in Chinese) 廖德丰, 陈季武, 谢萍, 朱振勤, 徐容. α-硫辛酸和二氢硫辛酸的抗氧化作用. 华东师范大学学报:自然科学版, 2007(2):87-92, 136.
    [3] Tajima K, Ikeda K, Chang HY, Chang CH, Yoneshiro T, Oguri Y, Jun H, Wu J, Ishihama Y, Kajimura S. Mitochondrial lipoylation integrates age-associated decline in brown fat thermogenesis. Nature Metabolism, 2019, 1(9):886-898.
    [4] Liu Y, Wang EX, Pan CH, Dong XT, Ding MZ. Biosynthesis of a-lipoic acid in Gluconobacter oxydans increases the production of vitamin C by one-step fermentation. Chinese Journal of Biotechnology, 2019, 35(7):1266-1276. (in Chinese) 刘宇, 王恩旭, 潘才惠, 董秀涛, 丁明珠. 氧化葡萄糖酸杆菌中硫辛酸合成模块对维生素C一步混菌发酵的影响. 生物工程学报, 2019, 35(7):1266-1276.
    [5] Hayakawa S, Kawamura M, Sato T, Hirano T, Kikuchi T, Watanabe A, Fujimura S. An α-Lipoic acid derivative, and anti-ROS agent, prevents the acquisition of multi-drug resistance in clinical isolates of Pseudomonas aeruginosa. Journal of Infection and Chemotherapy, 2019, 25(1):28-33.
    [6] Lanz ND, Lee KH, Horstmann AK, Pandelia ME, Cicchillo RM, Krebs C, Booker SJ. Characterization of lipoyl synthase from Mycobacterium tuberculosis. Biochemistry, 2016, 55(9):1372-1383.
    [7] Cronan JE. Advances in synthesis of biotin and assembly of lipoic acid. Current Opinion in Chemical Biology, 2018, 47:60-66.
    [8] Cronan JE. Assembly of lipoic acid on its cognate enzymes:an extraordinary and essential biosynthetic pathway. Microbiology and Molecular Biology Reviews, 2016, 80(2):429-450.
    [9] Spalding MD, Prigge ST. Lipoic acid metabolism in microbial pathogens. Microbiology and Molecular Biology Reviews, 2010, 74(2):200-228.
    [10] Cronan JE. Progress in the enzymology of the mitochondrial diseases of lipoic acid requiring enzymes. Frontiers in Genetics, 2020, 11:510. DOI:10.3389/fgene.2020.00510.
    [11] Perham RN. Swinging arms and swinging domains in multifunctional enzymes:catalytic machines for multistep reactions. Annual Review of Biochemistry, 2000, 69:961-1004.
    [12] Perham RN. Domains, motifs, and linkers in 2-oxo acid dehydrogenase multienzyme complexes:a paradigm in the design of a multifunctional protein. Biochemistry, 1991, 30(35):8501-8512.
    [13] Cronan JE. Biotin and lipoic acid:synthesis, attachment, and regulation. EcoSal Plus, 2008, 3(1):10.1128. DOI:10.1128/ecosalplus.3.6.3.5.
    [14] Tezuka T, Ohnishi Y. Two Glycine riboswitches activate the Glycine cleavage system essential for Glycine detoxification in Streptomyces griseus. Journal of Bacteriology, 2014, 196(7):1369-1376.
    [15] Reed LJ, Hackert ML. Structure-function relationships in dihydrolipoamide acyltransferases. The Journal of Biological Chemistry, 1990, 265(16):8971-8974.
    [16] Ricaud PM, Howard MJ, Roberts EL, Broadhurst RW, Perham RN. Three-dimensional structure of the lipoyl domain from the dihydrolipoyl succinyltransferase component of the 2-oxoglutarate dehydrogenase multienzyme complex of Escherichia coli. Journal of Molecular Biology, 1996, 264(1):179-190.
    [17] Zhao X, Miller JR, Cronan JE. The reaction of LipB, the octanoyl-[acyl carrier protein]:protein N-octanoyltransferase of lipoic acid synthesis, proceeds through an acyl-enzyme intermediate. Biochemistry, 2005, 44(50):16737-16746.
    [18] Ali ST, Moir AJG, Ashton PR, Engel PC, Guest JR. Octanoylation of the lipoyl domains of the pyruvate dehydrogenase complex in a lipoyl-deficient strain of Escherichia coli. Molecular Microbiology, 1990, 4(6):943-950.
    [19] Cao XY, Zhu L, Song XJ, Hu Z, Cronan JE. Protein moonlighting elucidates the essential human pathway catalyzing lipoic acid assembly on its cognate enzymes. Proceedings of the National Academy of Sciences USA, 2018, 115(30):E7063-E7072.
    [20] Martin N, Christensen QH, Mansilla MC, Cronan JE, de Mendoza D. A novel two-gene requirement for the octanoyltransfer reaction of Bacillus subtilis lipoic acid biosynthesis. Molecular Microbiology, 2011, 80(2):335-349.
    [21] Cao XY, Hong YQ, Zhu L, Hu YY, Cronan JE. Development and retention of a primordial moonlighting pathway of protein modification in the absence of selection presents a puzzle. Proceedings of the National Academy of Sciences USA, 2018, 115(4):647-655.
    [22] Jordan SW, Cronan JE Jr. The Escherichia coli lipB gene encodes lipoyl (octanoyl)-acyl carrier protein:protein transferase. Journal of Bacteriology, 2003, 185(5):1582-1589.
    [23] Cronan JE. The structure of lipoyl synthase, a remarkable enzyme that performs the last step of an extraordinary biosynthetic pathway. Biochemical Journal, 2014, 464(1):e1-e3. DOI:10.1042/bj20141061.
    [24] Morris TW, Reed KE, Cronan JE. Lipoic acid metabolism in Escherichia coli:the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. Journal of Bacteriology, 1995, 177(1):1-10.
    [25] Kim DJ, Lee SJ, Kim HS, Kim KH, Lee HH, Yoon HJ, Suh SW. Structural basis of octanoic acid recognition by lipoate-protein ligase B. Proteins:Structure, Function, and Bioinformatics, 2008, 70(4):1620-1625.
    [26] Harmer JE, Hiscox MJ, Dinis PC, Fox SJ, Iliopoulos A, Hussey JE, Sandy J, van Beek FT, Essex JW, Roach PL. Structures of lipoyl synthase reveal a compact active site for controlling sequential sulfur insertion reactions. The Biochemical Journal, 2014, 464(1):123-133.
    [27] McLaughlin MI, Lanz ND, Goldman PJ, Lee KH, Booker SJ, Drennan CL. Crystallographic snapshots of sulfur insertion by lipoyl synthase. Proceedings of the National Academy of Sciences USA, 2016, 113(34):9446-9450.
    [28] Lanz ND, Rectenwald JM, Wang B, Kakar ES, Laremore TN, Booker SJ, Silakov A. Characterization of a radical intermediate in lipoyl cofactor biosynthesis. Journal of the American Chemical Society, 2015, 137(41):13216-13219.
    [29] McCarthy EL, Booker SJ. Destruction and reformation of an iron-sulfur cluster during catalysis by lipoyl synthase. Science, 2017, 358(6361):373-377.
    [30] Dong G, Cao LL, Ryde U. Insight into the reaction mechanism of lipoyl synthase:a QM/MM study. JBIC Journal of Biological Inorganic Chemistry, 2018, 23(2):221-229.
    [31] McCarthy EL, Booker SJ. Biochemical approaches for understanding iron-sulfur cluster regeneration in Escherichia coli lipoyl synthase during catalysis. Methods in Enzymology, 2018, 606:217-239.
    [32] McCarthy EL, Rankin AN, Dill ZR, Booker SJ. The A-type domain in Escherichia coli NfuA is required for regenerating the auxiliary[4Fe-4S] cluster in Escherichia coli lipoyl synthase. Journal of Biological Chemistry, 2019, 294(5):1609-1617.
    [33] Kim DJ, Kim KH, Lee HH, Lee SJ, Ha JY, Yoon HJ, Suh SW. Crystal structure of lipoate-protein ligase A bound with the activated intermediate:insights into interaction with lipoyl domains. The Journal of Biological Chemistry, 2005, 280(45):38081-38089.
    [34] Fujiwara K, Toma S, Okamura-Ikeda K, Motokawa Y, Nakagawa A, Taniguchi H. Crystal structure of lipoate-protein ligase A from Escherichia coli:Determination of the lipoic acid-binding site. Journal of Biological Chemistry, 2005, 280(39):33645-33651.
    [35] Cronan JE, Zhao X, Jiang YF. Function, attachment and synthesis of lipoic acid in Escherichia coli. Advances in Microbial Physiology, 2005, 50:103-146.
    [36] McManus E, Luisi BF, Perham RN. Structure of a putative lipoate protein ligase from Thermoplasma acidophilum and the mechanism of target selection for post-translational modification. Journal of Molecular Biology, 2006, 356(3):625-637.
    [37] Martin N, Lombardía E, Altabe SG, de Mendoza D, Mansilla MC. A lipA (yutB) mutant, encoding lipoic acid synthase, provides insight into the interplay between branched-chain and unsaturated fatty acid biosynthesis in Bacillus subtilis. Journal of Bacteriology, 2009, 191(24):7447-7455.
    [38] Christensen QH, Cronan JE. Lipoic acid synthesis:a new family of octanoyltransferases generally annotated as lipoate protein ligases. Biochemistry, 2010, 49(46):10024-10036.
    [39] Christensen QH, Martin N, Mansilla MC, de Mendoza D, Cronan JE. A novel amidotransferase required for lipoic acid cofactor assembly in Bacillus subtilis. Molecular Microbiology, 2011, 80(2):350-363.
    [40] Zorzoli A, Grayczyk JP, Alonzo F. Staphylococcus aureus tissue infection during Sepsis is supported by differential use of bacterial or host-derived lipoic acid. PLoS Pathogens, 2016, 12(10):e1005933.
    [41] Laczkovich I, Teoh WP, Flury S, Grayczyk JP, Zorzoli A, Alonzo III F. Increased flexibility in the use of exogenous lipoic acid by Staphylococcus aureus. Molecular Microbiology, 2018, 109(2):150-168.
    [42] Grayczyk JP, Harvey CJ, Laczkovich I, Alonzo F III. A lipoylated metabolic protein released by Staphylococcus aureus suppresses macrophage activation. Cell Host & Microbe, 2017, 22(5):678-687.e9.
    [43] Jin JQ, Hachisuka SI, Sato T, Fujiwara T, Atomi H. A structurally novel lipoyl synthase in the hyperthermophilic archaeon Thermococcus kodakarensis. Applied and Environmental Microbiology, 2020, 86(23):e01359-01320.
    [44] Christensen QH, Hagar JA, O'Riordan MXD, Cronan JE. A complex lipoate utilization pathway in Listeria monocytogenes. Journal of Biological Chemistry, 2011, 286(36):31447-31456.
    [45] Jiang YF, Cronan JE. Expression cloning and demonstration of Enterococcus faecalis lipoamidase (pyruvate dehydrogenase inactivase) as a Ser-Ser-Lys triad amidohydrolase. Journal of Biological Chemistry, 2005, 280(3):2244-2256.
    [46] Rasetto NB, Lavatelli A, Martin N, Mansilla MC. Unravelling the lipoyl-relay of exogenous lipoate utilization in Bacillus subtilis. Molecular Microbiology, 2019, 112(1):302-316.
    [47] Christensen QH, Cronan JE. The Thermoplasma acidophilum LplA-LplB complex defines a new class of bipartite lipoate-protein ligases. The Journal of Biological Chemistry, 2009, 284(32):21317-21326.
    [48] Posner MG, Upadhyay A, Bagby S, Hough DW, Danson MJ. A unique lipoylation system in the Archaea. FEBS Journal, 2009, 276(15):4012-4022.
    [49] Cao XY, Cronan JE. The Streptomyces coelicolor lipoate-protein ligase is a circularly permuted version of the Escherichia coli enzyme composed of discrete interacting domains. The Journal of Biological Chemistry, 2015, 290(11):7280-7290.
    [50] Keeney KM, Stuckey JA, O'Riordan MXD. LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence. Molecular Microbiology, 2007, 66(3):758-770.
    [51] Grayczyk JP, Alonzo F III. Staphylococcus aureus Lipoic acid synthesis limits macrophage reactive oxygen and nitrogen species production to promote survival during
    infection. Infection and Immunity, 2019, 87(10):e00344-19.
    [52] Teoh WP, Resko ZJ, Flury S, Alonzo F III. Dynamic relay of protein-bound lipoic acid in Staphylococcus aureus. Journal of Bacteriology, 2019, 201(22):e00446-19.
    [53] Zhu KM, Chen H, Jin J, Wang N, Ma GX, Huang JD, Feng YJ, Xin JQ, Zhang HM, Liu HG. Functional identification and structural analysis of a new lipoate protein ligase in Mycoplasma hyopneumoniae. Frontiers in Cellular and Infection Microbiology, 2020, 10:156.
    [54] Ma Q, Zhao X, Eddine AN, Geerlof A, Li X, Cronan JE, Kaufmann SHE, Wilmanns M. The Mycobacterium tuberculosis LipB enzyme functions as a cysteine/lysine dyad acyltransferase. Proceedings of the National Academy of Sciences USA, 2006, 103(23):8662-8667.
    [55] Ma JR, Liu AN, Zhang WB, Mao YH, Yu YH. LipB-LipA is the only lipoyl acylation pathway in Xanthomonas campestris. Acta Microbiologica Sinica, 2020, 60(8):1729-1740. (in Chinese) 马建荣, 刘安娜, 张文彬, 毛雅慧, 余永红. 野油菜黄单胞菌中LipB-LipA是唯一的硫辛酰化途径. 微生物学报, 2020, 60(8):1729-1740.
    [56] 陶乃敏. 硫辛酸合成的工艺研究. 天津大学硕士学位论文, 2014.
    [57] Sun YR, Zhang WB, Ma JC, Pang HS, Wang HH. Overproduction of α-lipoic acid by gene manipulated Escherichia coli. PLoS ONE, 2017, 12(1):e0169369.
    Cited by
Get Citation

Jianrong Ma, Yonghong Yu, Yicai Chen, Mingfeng Yan, Wenbin Zhang. Advances in protein lipoylation pathways in bacteria. [J]. Acta Microbiologica Sinica, 2021, 61(8): 2278-2293

Copy
Share
Article Metrics
  • Abstract:
  • PDF:
  • HTML:
  • Cited by:
History
  • Received:September 29,2020
  • Revised:January 16,2021
  • Online: August 04,2021
Article QR Code
  • WeChat ID
  • Mobile Terminal

Acta Microbiologica Sinica ® 2025 All Rights Reserved