Iron-sulfur Flavoenzymes: the Added Value of Making the Most Ancient Redox Cofactors and the Versatile Flavins Work Together

Overview

Journal Open Biol

Specialties Biology
Cell Biology
Molecular Biology

Date 2021 May 5

PMID 33947244

Citations 5

Authors

Maria Antonietta Vanoni

Affiliations

Soon will be listed here.

Abstract

Iron-sulfur (Fe-S) flavoproteins form a broad and growing class of complex, multi-domain and often multi-subunit proteins coupling the most ancient cofactors (the Fe-S clusters) and the most versatile coenzymes (the flavin coenzymes, FMN and FAD). These enzymes catalyse oxidoreduction reactions usually acting as switches between donors of electron pairs and acceptors of single electrons, and vice versa. Through selected examples, the enzymes' structure-function relationships with respect to rate and directionality of the electron transfer steps, the role of the apoprotein and its dynamics in modulating the electron transfer process will be discussed.

Citing Articles

Spin-Coupled Electron Densities of Iron-Sulfur Cluster Imaged by Serial Laue Diffraction.

Ren Z, Zhang F, Kang W, Wang C, Shin H, Zeng X Chem. 2024; 10(7):2103-2130.

PMID: 39170732 PMC: 11335340. DOI: 10.1016/j.chempr.2024.02.019.

The radical impact of oxygen on prokaryotic evolution-enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third.

Mrnjavac N, Nagies F, Wimmer J, Kapust N, Knopp M, Trost K FEBS Lett. 2024; 598(14):1692-1714.

PMID: 38750628 PMC: 7616280. DOI: 10.1002/1873-3468.14906.

Mathematical kinetic modelling followed by in vitro and in vivo assays reveal the bifunctional rice GTPCHII/DHBPS enzymes and demonstrate the key roles of OsRibA proteins in the vitamin B2 pathway.

Faustino M, Lourenco T, Strobbe S, Cao D, Fonseca A, Rocha I BMC Plant Biol. 2024; 24(1):220.

PMID: 38532321 PMC: 10964609. DOI: 10.1186/s12870-024-04878-z.

Potential roles of gut microbes in biotransformation of natural products: An overview.

Zhao Y, Zhong X, Yan J, Sun C, Zhao X, Wang X Front Microbiol. 2022; 13:956378.

PMID: 36246222 PMC: 9560768. DOI: 10.3389/fmicb.2022.956378.

Modulating catalytic activity of a modified flavin analogue judicially positioned metal ion toward aerobic sulphoxidation.

Mouli M, Kumar Mishra A RSC Adv. 2022; 12(7):3990-3995.

PMID: 35425444 PMC: 8981109. DOI: 10.1039/d1ra06558k.

References

Binda C, Bossi R, Wakatsuki S, Arzt S, Coda A, Curti B . Cross-talk and ammonia channeling between active centers in the unexpected domain arrangement of glutamate synthase. Structure. 2001; 8(12):1299-308. DOI: 10.1016/s0969-2126(00)00540-2. View

Yan Z, Ferry J . Electron Bifurcation and Confurcation in Methanogenesis and Reverse Methanogenesis. Front Microbiol. 2018; 9:1322. PMC: 6019823. DOI: 10.3389/fmicb.2018.01322. View

Poudel S, Dunham E, Lindsay M, Amenabar M, Fones E, Colman D . Origin and Evolution of Flavin-Based Electron Bifurcating Enzymes. Front Microbiol. 2018; 9:1762. PMC: 6085437. DOI: 10.3389/fmicb.2018.01762. View

Swuec P, Chaves-Sanjuan A, Camilloni C, Vanoni M, Bolognesi M . Cryo-EM Structures of Azospirillum brasilense Glutamate Synthase in Its Oligomeric Assemblies. J Mol Biol. 2019; 431(22):4523-4526. DOI: 10.1016/j.jmb.2019.08.011. View

Mohsen A, Rigby S, Jensen K, Munro A, Scrutton N . Thermodynamic basis of electron transfer in dihydroorotate dehydrogenase B from Lactococcus lactis: analysis by potentiometry, EPR spectroscopy, and ENDOR spectroscopy. Biochemistry. 2004; 43(21):6498-510. DOI: 10.1021/bi036179i. View

Knaff D, Hirasawa M, Ameyibor E, Fu W, Johnson M . Spectroscopic evidence for a [3Fe-4S] cluster in spinach glutamate synthase. J Biol Chem. 1991; 266(23):15080-4. View

Lubner C, Peters J . Electron Bifurcation Makes the Puzzle Pieces Fall Energetically into Place in Methanogenic Energy Conservation. Chembiochem. 2017; 18(23):2295-2297. DOI: 10.1002/cbic.201700533. View

Maklashina E, Cecchini G, Dikanov S . Defining a direction: electron transfer and catalysis in Escherichia coli complex II enzymes. Biochim Biophys Acta. 2013; 1827(5):668-78. PMC: 3615059. DOI: 10.1016/j.bbabio.2013.01.010. View

Beinert H, Kennedy M, Stout C . Aconitase as Ironminus signSulfur Protein, Enzyme, and Iron-Regulatory Protein. Chem Rev. 1996; 96(7):2335-2374. DOI: 10.1021/cr950040z. View

10.

Zhang F, Ma H, Bowatte K, Kwiatkowski D, Mittmann E, Qasem H . Crystal Structures of Bacterial (6-4) Photolyase Mutants with Impaired DNA Repair Activity. Photochem Photobiol. 2016; 93(1):304-314. DOI: 10.1111/php.12699. View

11.

Leys D, Basran J, Talfournier F, Sutcliffe M, Scrutton N . Extensive conformational sampling in a ternary electron transfer complex. Nat Struct Biol. 2003; 10(3):219-25. DOI: 10.1038/nsb894. View

12.

Haapanen O, Sharma V . A modeling and simulation perspective on the mechanism and function of respiratory complex I. Biochim Biophys Acta Bioenerg. 2018; 1859(7):510-523. DOI: 10.1016/j.bbabio.2018.04.001. View

13.

Hagen W, Vanoni M, Rosenbaum K, Schnackerz K . On the iron-sulfur clusters in the complex redox enzyme dihydropyrimidine dehydrogenase. Eur J Biochem. 2000; 267(12):3640-6. DOI: 10.1046/j.1432-1327.2000.01393.x. View

14.

Zickermann V, Wirth C, Nasiri H, Siegmund K, Schwalbe H, Hunte C . Structural biology. Mechanistic insight from the crystal structure of mitochondrial complex I. Science. 2015; 347(6217):44-9. DOI: 10.1126/science.1259859. View

15.

Carrillo N, Ceccarelli E . Open questions in ferredoxin-NADP+ reductase catalytic mechanism. Eur J Biochem. 2003; 270(9):1900-15. DOI: 10.1046/j.1432-1033.2003.03566.x. View

16.

Ravasio S, Curti B, Vanoni M . Determination of the midpoint potential of the FAD and FMN flavin cofactors and of the 3Fe-4S cluster of glutamate synthase. Biochemistry. 2001; 40(18):5533-41. DOI: 10.1021/bi0100889. View

17.

Berry L, Poudel S, Tokmina-Lukaszewska M, Colman D, Nguyen D, Schut G . H/D exchange mass spectrometry and statistical coupling analysis reveal a role for allostery in a ferredoxin-dependent bifurcating transhydrogenase catalytic cycle. Biochim Biophys Acta Gen Subj. 2017; 1862(1):9-17. DOI: 10.1016/j.bbagen.2017.10.002. View

18.

Saito T, Nishino T . Differences in redox and kinetic properties between NAD-dependent and O2-dependent types of rat liver xanthine dehydrogenase. J Biol Chem. 1989; 264(17):10015-22. View

19.

Vanoni M, Edmondson D, Zanetti G, Curti B . Characterization of the flavins and the iron-sulfur centers of glutamate synthase from Azospirillum brasilense by absorption, circular dichroism, and electron paramagnetic resonance spectroscopies. Biochemistry. 1992; 31(19):4613-23. DOI: 10.1021/bi00134a011. View

20.

Page C, Moser C, Chen X, Dutton P . Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature. 1999; 402(6757):47-52. DOI: 10.1038/46972. View