МИКРОБНЫЕ 2-ЕНОАТРЕДУКТАЗЫ, СОДЕРЖАЩИЕ КОВАЛЕНТНО СВЯЗАННЫЙ ФЛАВИНМОНОНУКЛЕОТИД
- Авторы: Богачев А.В1,2, Байков А.А1,2, Анашкин В.А1,2, Берцова Ю.В1,2
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Учреждения:
- Московский государственный университет им. М.В. Ломоносова
- НИИ физико-химической биологии им. А.Н. Белозерского
- Выпуск: Том 90, № 12 (2025)
- Страницы: 1902–1916
- Раздел: Статьи
- URL: https://ogarev-online.ru/0320-9725/article/view/376116
- DOI: https://doi.org/10.7868/S3034529425120023
- ID: 376116
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Аннотация
Об авторах
А. В Богачев
Московский государственный университет им. М.В. Ломоносова; НИИ физико-химической биологии им. А.Н. Белозерского
Email: bogachev@belozersky.msu.ru
Москва, Россия
А. А Байков
Московский государственный университет им. М.В. Ломоносова; НИИ физико-химической биологии им. А.Н. БелозерскогоМосква, Россия
В. А Анашкин
Московский государственный университет им. М.В. Ломоносова; НИИ физико-химической биологии им. А.Н. БелозерскогоМосква, Россия
Ю. В Берцова
Московский государственный университет им. М.В. Ломоносова; НИИ физико-химической биологии им. А.Н. БелозерскогоМосква, Россия
Список литературы
- Macheroux, P., Kappes, B., and Ealick, S. E. (2011) Flavogenomics – a genomic and structural view of flavin-dependent proteins, FEBS J., 278, 2625-2634, https://doi.org/10.1111/j.1742-4658.2011.08202.x.
- Massey, V. (2000) The chemical and biological versatility of riboflavin, Biochem. Soc. Trans., 28, 283-296, https://doi.org/10.1042/0300-5127:0280283.
- Heuts, D. P., Scrutton, N. S., McIntire, W. S., and Fraaije, M. W. (2009) What’s in a covalent bond? On the role and formation of covalently bound flavin cofactors, FEBS J., 276, 3405-3427, https://doi.org/10.1111/j.1742-4658.2009.07053.x.
- McNeil, M. B., and Fineran, P. C. (2013) Prokaryotic assembly factors for the attachment of flavin to complex II, Biochim. Biophys. Acta, 1827, 637-647, https://doi.org/10.1016/j.bbabio.2012.09.003.
- Maklashina, E., Iverson, T. M., and Cecchini, G. (2022) How an assembly factor enhances covalent FAD attachment to the flavoprotein subunit of complex II, J. Biol. Chem., 298, 102472, https://doi.org/10.1016/j.jbc.2022.102472.
- Hayashi, M., Nakayama, Y., Yasui, M., Maeda, M., Furuishi, K., and Unemoto, T. (2001) FMN is covalently attached to a threonine residue in the NqrB and NqrC subunits of Na+-translocating NADH-quinone reductase from Vibrio alginolyticus, FEBS Lett., 488, 5-8, https://doi.org/10.1016/s0014-5793(00)02404-2.
- Bertsova, Y. V., Fadeeva, M. S., Kostyrko, V. A., Serebryakova, M. V., Baykov, A. A., and Bogachev, A. V. (2013) Alternative pyrimidine biosynthesis protein ApbE is a flavin transferase catalyzing covalent attachment of FMN to a threonine residue in bacterial flavoproteins, J. Biol. Chem., 288, 14276-14286, https://doi.org/10.1074/jbc.M113.455402.
- Bogachev, A. V., Baykov, A. A., and Bertsova, Y. V. (2018) Flavin transferase: the maturation factor of flavin-containing oxidoreductases, Biochem. Soc. Trans., 46, 1161-1169, https://doi.org/10.1042/BST20180524.
- Bertsova, Y. V., Serebryakova, M. V., Anashkin, V. A., Baykov, A. A., and Bogachev, A. V. (2019) Mutational analysis of the flavinylation and binding motifs in two protein targets of the flavin transferase ApbE, FEMS Microbiol. Lett., 366, fnz252, https://doi.org/10.1093/femsle/fnz252.
- Fan, X., and Fraaije, M. W. (2025) Flavin transferase ApbE: from discovery to applications, J. Biol. Chem., 26, 108453, https://doi.org/10.1016/j.jbc.2025.108453.
- Méheust, R., Huang, S., Rivera-Lugo, R., Banfield, J. F., and Light. S. H. (2021) Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life, Elife, 10, e66878, https://doi.org/10.7554/eLife.66878.
- Huang, S., Méheust, R., Barquera, B., and Light, S. H. (2024) Versatile roles of protein flavinylation in bacterial extracyotosolic electron transfer, mSystems, 9, e0037524, https://doi.org/10.1128/msystems.00375-24.
- Lawrence, J. (1999) Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes, Curr. Opin. Genet. Dev., 9, 642-648, https://doi.org/10.1016/s0959-437x(99)00025-8.
- Koonin, E. V. (2011) The Logic of Chance: The Nature and Origin of Biological Evolution, Upper Saddle River, NJ, FT Press.
- Rentzsch, R., and Orengo, C. A. (2009) Protein function prediction – the power of multiplicity, Trends Biotechnol., 27, 210-219, https://doi.org/10.1016/j.tibtech.2009.01.002.
- Yeats, C., Bentley, S., and Bateman, A. (2003) New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor, BMC Microbiol., 3, 3, https://doi.org/10.1186/1471-2180-3-3.
- Borshchevskiy, V., Round, E., Bertsova, Y., Polovinkin, V., Gushchin, I., Ishchenko, A., Kovalev, K., Mishin, A., Kachalova, G., Popov, A., Bogachev, A., and Gordeliy, V. (2015) Structural and functional investigation of flavin binding center of the NqrC subunit of sodium-translocating NADH:quinone oxidoreductase from Vibrio harveyi, PLoS One, 10, e0118548, https://doi.org/10.1371/journal.pone.0118548.
- Leys, D., Tsapin, A. S., Nealson, K. H., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1, Nat. Struct. Biol., 6, 1113-1117, https://doi.org/10.1038/70051.
- Reid, G. A., Miles, C. S., Moysey, R. K., Pankhurst, K. L., and Chapman, S. K. (2000) Catalysis in fumarate reductase, Biochim. Biophys. Acta, 1459, 310-315, https://doi.org/10.1016/s0005-2728(00)00166-3.
- Cecchini, G., Schröder, I., Gunsalus, R.P., and Maklashina, E. (2002) Succinate dehydrogenase and fumarate reductase from Escherichia coli, Biochim. Biophys. Acta, 1553, 140-157, https://doi.org/10.1016/s0005-2728(01)00238-9.
- Arkhipova, O. V., and Akimenko, V. K. (2005) Unsaturated organic acids as terminal electron acceptors for reductase chains of anaerobic bacteria, Microbiology, 74, 629-639, https://doi.org/10.1007/s11021-005-0116-6.
- Light, S. H., Méheust, R., Ferrell, J. L., Cho, J., Deng, D., Agostoni, M., Iavarone, A. T., Banfield, J. F., D’Orazio, S. E. F., and Portnoy, D. A. (2019) Extracellular electron transfer powers flavinylated extracellular reductases in Gram-positive bacteria, Proc. Natl. Acad. Sci. USA, 116, 26892-26899, https://doi.org/10.1073/pnas.1915678116.
- Bogachev, A. V., Bertsova, Y. V., Bloch, D. A., and Verkhovsky, M. I. (2012) Urocanate reductase: identification of a novel anaerobic respiratory pathway in Shewanella oneidensis MR-1, Mol. Microbiol., 86, 1452-1463, https://doi.org/10.1111/mmi.12067.
- Kees, E. D., Pendleton, A. R., Paquete, C. M., Arriola, M. B., Kane, A. L., Kotloski, N. J., Intile, P. J., and Gralnick, J. A. (2019) Secreted flavin cofactors for anaerobic respiration of fumarate and urocanate by Shewanella oneidensis: cost and role, Appl. Environ. Microbiol., 85, e00852-19, https://doi.org/10.1128/AEM.00852-19.
- Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., Back, T., Petersen, S., Reiman, D., Clancy, E., Zielinski, M., Steinegger, M., Pacholska, M., Berghammer, T., Bodenstein, S., Silver, D., Vinyals, O., Senior, A. W., Kavukcuoglu, K., Kohli, P., and Hassabis, D. (2021) Highly accurate protein structure prediction with AlphaFold, Nature, 596, 583-589, https://doi.org/10.1038/s41586-021-03819-2.
- Boitreaud, J., Dent, J., McPartlon, M., Meier, J., Reis, V., Rogozhnikov, A., and Wu, K. (2024) Chai-1: Decoding the molecular interactions of life, bioRxiv, 2024.10.10.615955, https://doi.org/10.1101/2024.10.10.615955.
- Bertsova, Y. V., Kostyrko, V. A., Baykov, A. A., and Bogachev, A. V. (2014) Localization-controlled specificity of FAD:threonine flavin transferases in Klebsiella pneumoniae and its implications for the mechanism of Na+-translocating NADH:quinone oxidoreductase, Biochim. Biophys. Acta, 1837, 1122-1129, https://doi.org/10.1016/j.bbabio.2013.12.006.
- Bertsova, Y. V., Oleynikov, I. P., and Bogachev, A. V. (2020) A new water-soluble bacterial NADH: fumarate oxidoreductase, FEMS Microbiol. Lett., 367, fnaa175, https://doi.org/10.1093/femsle/fnaa175.
- Bertsova, Y. V., Serebryakova, M. V., Baykov, A. A., and Bogachev, A. V. (2022) A novel, NADH-dependent acrylate reductase in Vibrio harveyi, Appl. Environ. Microbiol., 88, e0051922, https://doi.org/10.1128/aem.00519-22.
- Bertsova, Y. V., Serebryakova, M. V., Anashkin, V. A., Baykov, A. A., and Bogachev, A. V. (2024) A redox-regulated, heterodimeric NADH:cinnamate reductase in Vibrio ruber, Biochemistry (Moscow), 89, 241-256, https://doi.org/10.1134/S0006297924020056.
- Koike, H., Sasaki, H., Kobori, T., Zenno, S., Saigo, K., Murphy, M. E., Adman, E. T., and Tanokura, M. (1998) 1.8 Å crystal structure of the major NAD(P)H:FMN oxidoreductase of a bioluminescent bacterium, Vibrio fischeri: overall structure, cofactor and substrate-analog binding, and comparison with related flavoproteins, J. Mol. Biol., 280, 259-273, https://doi.org/10.1006/jmbi.1998.1871.
- Agarwal, R., Bonanno, J. B., Burley, S. K., and Swaminathan, S. (2006) Structure determination of an FMN reductase from Pseudomonas aeruginosa PA01 using sulfur anomalous signal, Acta Crystallogr. D Biol. Crystallogr., 62, 383-391, https://doi.org/10.1107/S0907444906001600.
- Mracek, J., Snyder, S. J., Chavez, U. B., and Turrens, J. F. (1991) A soluble fumarate reductase in Trypanosoma brucei procyclic trypomastigotes, J. Protozool., 38, 554-558, https://doi.org/10.1111/j.1550-7408.1991.tb06079.x.
- Besteiro, S., Biran, M., Biteau, N., Coustou, V., Baltz, T., Canioni, P., and Bringaud, F. (2002) Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme, NADH-dependent fumarate reductase, J. Biol. Chem., 277, 38001-38012, https://doi.org/10.1074/jbc.M201759200.
- Coustou, V., Besteiro, S., Rivière, L., Biran, M., Biteau, N., Franconi, J. M., Boshart, M., Baltz, T., and Bringaud, F. (2005) A mitochondrial NADH-dependent fumarate reductase involved in the production of succinate excreted by procyclic Trypanosoma brucei, J. Biol. Chem., 280, 16559-16570, https://doi.org/10.1074/jbc.M500343200.
- Turrens, J. F., Newton, C. L., Zhong, L., Hernandez, F. R., Whitfield, J., and Docampo, R. (1999) Mercaptopyridine-N-oxide, an NADH-fumarate reductase inhibitor, blocks Trypanosoma cruzi growth in culture and in infected myoblasts, FEMS Microbiol. Lett., 175, 217-221, https://doi.org/10.1111/j.1574-6968.1999.tb13623.x.
- Rodríguez Arce, E., Mosquillo, M. F., Pérez-Díaz, L., Echeverría, G. A., Piro, O. E., Merlino, A., Coitiño, E. L., Maríngolo Ribeiro, C., Leite, C. Q., Pavan, F. R., Otero, L., and Gambino, D. (2015) Aromatic amine N-oxide organometallic compounds: searching for prospective agents against infectious diseases, Dalton Trans., 44, 14453-14464, https://doi.org/10.1039/c5dt00557d.
- Serebryakova, M. V., Bertsova, Y. V., Sokolov, S. S., Kolesnikov, A. A., Baykov, A. A., and Bogachev, A. V. (2018) Catalytically important flavin linked through a phosphoester bond in a eukaryotic fumarate reductase, Biochimie, 149, 34-40, https://doi.org/10.1016/j.biochi.2018.03.013.
- Schenk, R., Bachmaier, S., Bringaud, F., and Boshart, M. (2021) Efficient flavinylation of glycosomal fumarate reductase by its own ApbE domain in Trypanosoma brucei, FEBS J., 288, 5430-5445, https://doi.org/10.1111/febs.15812.
- Sancho, J. (2006) Flavodoxins: sequence, folding, binding, function and beyond, Cell Mol. Life Sci., 63, 855-864, https://doi.org/10.1007/s00018-005-5514-4.
- LaRoche, J., Boyd, P. W., McKay, R. M. L., and Geider, R. J. (1996) Flavodoxin as an in situ marker for iron stress in phytoplankton, Nature, 382, 802-805, https://doi.org/10.1038/382802a0.
- Bertsova, Y. V., Kulik, L. V., Mamedov, M. D., Baykov, A. A., and Bogachev, A. V. (2019) Flavodoxin with an air-stable flavin semiquinone in a green sulfur bacterium, Photosynth. Res., 142, 127-136, https://doi.org/10.1007/s11120-019-00658-1.
- Wood, P. M. (1983) Why do c-type cytochromes exist? FEBS Lett., 164, 223-226, https://doi.org/10.1016/0014-5793(83)80289-0.
- Attwood, P. V. (1995) The structure and the mechanism of action of pyruvate carboxylase, Int. J. Biochem. Cell Biol., 27, 231-249, https://doi.org/10.1016/1357-2725(94)00087-r.
- Douce, R., Bourguignon, J., Neuburger, M., and Rébeillé, F. (2001) The glycine decarboxylase system: a fascinating complex, Trends Plant Sci., 6, 167-176, https://doi.org/10.1016/s1360-1385(01)01892-1.
- Venskutonytė, R., Koh, A., Stenström, O., Khan, M. T., Lundqvist, A., Akke, M., Bäckhed, F., and Lindkvist-Petersson, K. (2021) Structural characterization of the microbial enzyme urocanate reductase mediating imidazole propionate production, Nat. Commun., 12, 1347, https://doi.org/10.1038/s41467-021-21548-y.
- Delavari, N., Zhang, Z., and Stull, F. (2024) Rapid reaction studies on the chemistry of flavin oxidation in urocanate reductase, J. Biol. Chem., 300, 105689, https://doi.org/10.1016/j.jbc.2024.105689.
- Bertsova, Y. V., Serebryakova, M. V., Bogachev, V. A., Baykov, A. A., and Bogachev, A. V. (2024) Acrylate reductase of an anaerobic electron transport chain of the marine bacterium Shewanella woodyi, Biochemistry (Moscow), 89, 701-710, https://doi.org/10.1134/S0006297924040096.
- Little, A. S., Younker, I. T., Schechter, M. S., Bernardino, P. N., Méheust, R., Stemczynski, J., Scorza, K., Mullowney, M. W., Sharan, D., Waligurski, E., Smith, R., Ramaswamy, R., Leiter, W., Moran, D., McMillin, M., Odenwald, M. A., Iavarone, A. T., Sidebottom, A. M., Sundararajan, A., Pamer, E. G., Eren, A. M., and Light, S. H. (2024) Dietaryand host-derived metabolites are used by diverse gut bacteria for anaerobic respiration, Nat. Microbiol., 9, 55-69, https://doi.org/10.1038/s41564-023-01560-2.
- Koh, A., and Bäckhed, F. (2020) From association to causality: the role of the gut microbiota and its functional products on host metabolism, Mol. Cell, 78, 584-596, https://doi.org/10.1016/j.molcel.2020.03.005.
- Molinaro, A., Bel Lassen, P., Henricsson, M., Wu, H., Adriouch, S., Belda, E., Chakaroun, R., Nielsen, T., Bergh, P. O., Rouault, C., André, S., Marquet, F., Andreelli, F., Salem, J. E., Assmann, K., Bastard, J. P., Forslund, S., Le Chatelier, E., Falony, G., et al. (2020) Imidazole propionate is increased in diabetes and associated with dietary patterns and altered microbial ecology, Nat. Commun., 11, 5881, https://doi.org/10.1038/s41467-020-19589-w.
- Koh, A., Molinaro, A., Ståhlman, M., Khan, M. T., Schmidt, C., Mannerås-Holm, L., Wu, H., Carreras, A., Jeong, H., Olofsson, L. E., Bergh, P. O., Gerdes, V., Hartstra, A., de Brauw, M., Perkins, R., Nieuwdorp, M., Bergström, G., and Bäckhed, F. (2018) Microbially produced imidazole propionate impairs insulin signaling through mTORC1, Cell, 175, 947-961.e17, https://doi.org/10.1016/j.cell.2018.09.055.
- Unden, G., Strecker, A., Kleefeld, A., and Kim, O.B. (2016) C4-Dicarboxylate utilization in aerobic and anaerobic growth, EcoSal Plus, 7, 10.1128/ecosalplus.ESP-0021-2015, https://doi.org/10.1128/ecosalplus.ESP-0021-2015.
- Van Hellemond, J. J., Klockiewicz, M., Gaasenbeek, C. P., Roos, M. H., and Tielens, A. G. (1995) Rhodoquinone and complex II of the electron transport chain in anaerobically functioning eukaryotes, J. Biol. Chem., 270, 31065-31070, https://doi.org/10.1074/jbc.270.52.31065.
- Ramotar, K., Conly, J. M., Chubb, H., and Louie, T. J. (1984) Production of menaquinones by intestinal anaerobes, J. Infect. Dis., 150, 213-218, https://doi.org/10.1093/infdis/150.2.213.
- Wargnies, M., Plazolles, N., Schenk, R., Villafraz, O., Dupuy, J. W., Biran, M., Bachmaier, S., Baudouin, H., Clayton, C., Boshart, M., and Bringaud, F. (2021) Metabolic selection of a homologous recombination-mediated gene loss protects Trypanosoma brucei from ROS production by glycosomal fumarate reductase, J. Biol. Chem., 296, 100548, https://doi.org/10.1016/j.jbc.2021.100548.
- Sieburth, J. M. (1961) Antibiotic properties of acrylic acid, a factor in the gastrointestinal antibiosis of polar marine animals, J. Bacteriol., 82, 72-79, https://doi.org/10.1128/jb.82.1.72-79.1961.
- Todd, J. D., Curson, A. R., Sullivan, M. J., Kirkwood, M., and Johnston, A. W. (2012) The Ruegeria pomeroyi acuI gene has a role in DMSP catabolism and resembles yhdH of E. coli and other bacteria in conferring resistance to acrylate, PLoS One, 7, e35947, https://doi.org/10.1371/journal.pone.0035947.
- Curson, A. R., Todd, J. D., Sullivan, M. J., and Johnston, A. W. (2011) Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes, Nat. Rev. Microbiol., 9, 849-859, https://doi.org/10.1038/nrmicro2653.
- Raina, J. B., Tapiolas, D., Willis, B. L., and Bourne, D. G. (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur, Appl. Environ. Microbiol., 75, 3492-3501, https://doi.org/10.1128/AEM.02567-08.
- Sogin, E. M., Michellod, D., Gruber-Vodicka, H. R., Bourceau, P., Geier, B., Meier, D. V., Seidel, M., Ahmerkamp, S., Schorn, S., ’D’Angelo, G., Procaccini, G., Dubilier, N., and Liebeke, M. (2022) Sugars dominate the seagrass rhizosphere, Nat. Ecol. Evol., 6, 866-877, https://doi.org/10.1038/s41559-022-01740-z.
- Rameshkumar, N., and Nair, S. (2009) Isolation and molecular characterization of genetically diverse antagonistic, diazotrophic red-pigmented vibrios from different mangrove rhizospheres, FEMS Microbiol. Ecol., 67, 455-467, https://doi.org/10.1111/j.1574-6941.2008.00638.x.
- Blum, M., Andreeva, A., Florentino, L. C., Chuguransky, S. R., Grego, T., Hobbs, E., Pinto, B. L., Orr, A., Paysan-Lafosse, T., Ponamareva, I., Salazar, G. A., Bordin, N., Bork, P., Bridge, A., Colwell, L., Gough, J., Haft, D. H., Letunic, I., Llinares-López, F., Marchler-Bauer, A., Meng-Papaxanthos, L., Mi, H., Natale, D. A., Orengo, C. A., Pandurangan, A. P., Piovesan, D., Rivoire, C., Sigrist, C. J. A., Thanki, N., Thibaud-Nissen, F., Thomas, P. D., Tosatto, S. C. E., Wu, C. H., and Bateman, A. (2025) InterPro: the protein sequence classification resource in 2025, Nucleic Acids Res., 53, D444-D456, https://doi.org/10.1093/nar/gkae1082.
- Eberhardt, J., Santos-Martins, D., Tillack, A. F., and Forli, S. (2021) AutoDock Vina 1.2.0: New docking methods, expanded force field, and Python bindings, J. Chem. Inf. Model., 61, 3891-3898, https://doi.org/10.1021/acs.jcim.1c00203.
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