Увеличение светонезависимой выработки биоводорода путем стимуляции активности гидрогеназ: критический обзор
https://doi.org/10.15518/isjaee.2025.12.039-106
Аннотация
Биоводород, как перспективное биотопливо, обладает рядом ключевых преимуществ, которые включают нулевые выбросы углерода, экологическую устойчивость и высокую энергоэффективность. [NiFe]- и [FeFe]гидрогеназы играют ключевую роль в светонезависимом производстве биоводорода из биомассы с использованием микроорганизмов. Несмотря на значительный прогресс, по-прежнему существует множество проблем, препятствующих крупномасштабному промышленному внедрению этой технологии. В данном обзоре мы представляем подробный анализ структурных особенностей, распространенности и каталитических механизмов основных микроорганизмов, используемых в биореакторах темной ферментации и биоэлектрохимических системах. Мы также рассматриваем передовые стратегии повышения активности ферментов, такие как методы генной инженерии и инновационные методы оценки производительности. Кроме того, мы исследуем базовые механизмы, ответственные за увеличение производства газообразного водорода, включая перенос электронов, рост биомассы и синтез ферредоксина. В заключении обзора выделяются перспективные направления исследований, в частности, интеграция искусственного интеллекта в высокоэффективные системы производства биоводорода, которая может значительно ускорить прогресс в этой области.
Ключевые слова
Об авторах
А. А. ЛайковаРоссия
Лайкова Александра Алексеевна, младший научный сотрудник лаборатории микробиологии антропогенных мест обитания, аспирант,
119071, г. Москва, Ленинский пр-т, д. 33, строение 2.
ResearcherID: IVU-7977-2023;
Scopus AuthorID: 58044317600.
Е. А. Журавлева
Россия
Журавлева Елена Александровна, к. б. н., научный сотрудник лаборатории микробиологии антропогенных мест обитания,
119071, г. Москва, Ленинский пр-т, д. 33, строение 2.
Researcher ID: JBS-4297-2023;
Scopus Author ID: 57216346570.
А. А. Иваненко
Россия
Иваненко Артем Александрович, младший научный сотрудник лаборатории микробиологии антропогенных мест обитания,
119071, г. Москва, Ленинский пр-т, д. 33, строение 2;
119899, г. Москва, Ленинские Горы, д. 1, строение 12.
Researcher ID: JAX-4154-2023;
Scopus Author ID: 57195447250.
С. В. Шехурдина
Россия
Шехурдина Светлана Витальевна, младший научный сотрудник лаборатории микробиологии антропогенных мест обитания, аспирант,
119071, г. Москва, Ленинский пр-т, д. 33, строение 2.
Scopus Author ID: 57564192200;
Researcher ID: JZW-4863-2024.
А. А. Ковалев
Россия
Ковалев Андрей Александрович, доктор технических наук, главный научный сотрудник лаборатории биоэнергетических технологий,
109428, г. Москва, 1-й Институтский проезд, 5.
Researcher ID: F-7045-2017;
Scopus Author ID: 57205285134.
https://www.researchgate.net/profile/Andrey-Kovalev-8
Phone: +7926347795
Д. А. Ковалев
Россия
Ковалев Дмитрий Александрович, заведующий лабораторией биоэнергетических технологий, кандидат технических наук,
109428, г. Москва, 1-й Институтский проезд, д. 5.
Researcher ID: K-4810-2015.
Сантош Пиллаи
Южно-Африканская Республика
Сантош Пиллаи, кандидат наук, профессор университета,
Дурбан.
Scopus Author ID: 57194010507.
Хулио Сезар де Карвалью
Бразилия
Хулио Сезар де Карвалью, доктор философии в области биотехнологических процессов, профессор инженерии,
Куритиба.
Scopus Author ID: 9244670900.
Карлос Рикардо Соккол
Бразилия
Карлос Рикардо Соккол, руководитель исследовательской группы департамента инженерии биопроцессов и биотехнологий (DEBB), доктор философии в области генетической энзиматики, микробиологии и биоконверсии,
Куритиба.
Scopus Author ID: 7004252959.
Бинхуа Янь
Китай
Бинхуа Янь, профессор, доктор философии,
Чанша.
Scopus Author ID: 56890254300.
Мукеш Кумар Авасти
Китай
Мукеш Кумар Авасти, кандидат биологических наук, профессор, ученый-исследователь в области экологии и микробиологических технологий; пожизненный член Индийского общества биотехнологических исследований, Ассоциации научных конгрессов Индии, Общества фундаментальной и прикладной микологии, Ассоциации микробиологов, Национальной ассоциации по переработке твердых отходов Индии и Европейской федерации биотехнологий,
Янлин.
Scopus Author ID: 13003468000.
Карен Трчунян
Армения
Карен Трчунян, доктор наук в области биофизики и биотехнологий, директор Научно-исследовательского института биологии, профессор кафедры биохимии, микробиологии и биотехнологии,
Ереван.
Scopus Author ID: 23974981000.
Ю. В. Литти
Россия
Юрий Владимирович Литти, кандидат биологических наук, заведующий лабораторией микробиологии антропогенных мест обитания,
119071, г. Москва, Ленинский пр-т, д. 33, строение 2.
Researcher ID: C-4945-2014;
Scopus Author ID: 59312651000
Список литературы
1. . Sahil S., Singh R., Masakapalli S. K., Pareek N., Kovalev A. A., Litti Y. V. et al. Biomass pretreatment, bioprocessing and reactor design for biohydrogen production: a review // Environmental Chemistry Letters. 2024; 22:1665-702. https://doi.org/10.1007/s10311-02401722-6.
2. . Laikova A. A., Kovalev A. A., Kovalev D. A., Zhuravleva E. A., Shekhurdina S. V., Loiko N. G. et al. Feasibility of successive hydrogen and methane production in a single-reactor configuration of batch anaerobic digestion through bioaugmentation and stimulation of hydrogenase activity and direct interspecies electron transfer // International Journal of Hydrogen Energy. 2023; 48:12646-60. https://doi.org/10.1016/j.ijhydene.2022.12.231.
3. . Argun H., Kargi F. Bio-hydrogen production by different operational modes of dark and photo-fermentation: An overview // International Journal of Hydrogen Energy. 2011; 36:7443-59. https://doi.org/10.1016/j.ijhydene.2011.03.116.
4. . Jayachandran V., Basak N., De Philippis R., Adessi A. Novel strategies towards efficient molecular biohydrogen production by dark fermentative mechanism: present progress and future perspective // Bioprocess and Biosystems Engineering. 2022; 45:1595-624. https://doi.org/10.1007/s00449-022-02738-4.
5. . Sarangi P. K., Nanda S. Biohydrogen Production Through Dark Fermentation // Chemical Engineering & Technology. 2020; 43:601-12. https://doi.org/10.1002/ceat.201900452.
6. . Ergal İ., Gräf O., Hasibar B., Steiner M., Vukotić S., Bochmann G. et al. Biohydrogen production beyond the Thauer limit by precision design of artificial microbial consortia // Communications Biology. 2020; 3:443. https://doi.org/10.1038/s42003-020-01159-x.
7. . Gopalakrishnan B., Khanna N., Das D. Dark-Fermentative Biohydrogen Production // Biohydrogen, Elsevier. 2019, pр. 79-122. https://doi.org/10.1016/B978-0-444-64203-5.00004-6.
8. . Mai J., Hu B. -B., Zhu M. -J. Metabolic division of labor between Acetivibrio thermocellus DSM 1313 and Thermoanaerobacterium thermosaccharolyticum MJ1 enhanced hydrogen production from lignocellulose // Bioresource Technology. 2023; 390:129871. https://doi.org/10.1016/j.biortech.2023.129871.
9. . Akaniro I. R., Oladipo A. A., Onwujekwe E. C. Metabolic engineering approaches for scale-up of fermentative biohydrogen production. A review // International Journal of Hydrogen Energy. 2024; 52:240-64. https://doi.org/10.1016/j.ijhydene.2023.04.328.
10. . Lee H. -S., Xin W., Katakojwala R., Venkata Mohan. S., Tabish N. M. D. Microbial electrolysis cells for the production of biohydrogen in dark fermentation – A review // Bioresource Technology. 2022; 363:127934. https://doi.org/10.1016/j.biortech.2022.127934.
11. . Rao R., Basak N. Fermentative molecular biohydrogen production from cheese whey: present prospects and future strategy // Applied Biochemistry and Biotechnology. 2021; 193:2297-330. https://doi.org/10.1007/s12010-021-03528-6.
12. . Ren Y., Tang S., Hong F., Jiang W., Liu Z., Lu H. et al. Effects of milli-magnetite on biohydrogen production from potato peels: Insight of metabolism mechanisms // Fuel. 2023; 348:128576. https://doi.org/10.1016/j.fuel.2023.128576.
13. . Yang G., Wang J. Various additives for improving dark fermentative hydrogen production: A review // Renewable and Sustainable Energy Reviews. 2018; 95:130-46. https://doi.org/10.1016/j.rser.2018.07.029.
14. . Swartz J. Opportunities toward hydrogen production biotechnologies // Current Opinion in Biotechnology. 2020; 62:248-55. https://doi.org/10.1016/j.copbio.2020.03.002.
15. . Peters J. W., Schut G. J., Boyd E. S., Mulder D. W., Shepard E. M., Broderick J. B. et al. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research. 2015; 1853:1350-69. https://doi.org/10.1016/j.bbamcr.2014.11.021.
16. . Petrosyan H., Vanyan L., Trchounian A., Trchounian K. Defining the roles of the hydrogenase 3 and 4 subunits in hydrogen production during glucose fermentation: A new model of a H2-producing hydrogenase complex // International Journal of Hydrogen Energy. 2020; 45:5192-201. https://doi.org/10.1016/j.ijhydene.2019.09.204.
17. . Cheng J., Li H., Ding L., Zhou J., Song W., Li Y. -Y. et al. Improving hydrogen and methane co-generation in cascading dark fermentation and anaerobic digestion: The effect of magnetite nanoparticles on microbial electron transfer and syntrophism // Chemical Engineering Journal. 2020; 397:125394. https://doi.org/10.1016/j.cej.2020.125394.
18. . Moura A. G. L., Rabelo CABS, Okino C. H., Maintinguer S. I., Silva E. L., Varesche M. B. A. Enhancement of Clostridium butyricum hydrogen production by iron and nickel nanoparticles: Effects on hydA expression // International Journal of Hydrogen Energy. 2020; 45:28447-61. https://doi.org/10.1016/j.ijhydene.2020.07.161.
19. . Bu J., Wei H. -L., Wang Y. -T., Cheng J. -R., Zhu M. -J. Biochar boosts dark fermentative H2 production from sugarcane bagasse by selective enrichment/colonization of functional bacteria and enhancing extracellular electron transfer // Water Research. 2021; 202:117440. https://doi.org/10.1016/j.watres.2021.117440.
20. . Wang M. -Y., Tsai Y. -L., Olson B. H., Chang J. -S. Monitoring dark hydrogen fermentation performance of indigenous Clostridium butyricum by hydrogenase gene expression using RT-PCR and qPCR // International Journal of Hydrogen Energy. 2008; 33:4730-8. https://doi.org/10.1016/j.ijhydene.2008.06.048.
21. . Laikova A., Zhuravleva E., Shekhurdina S., Ivanenko A., Biryuchkova P., Loiko N. et al. The intracellular accumulation of iron coincides with enhanced biohydrogen production by Thermoanaerobacterium thermosaccharolyticum // Chemical Engineering Journal. 2024; 497:154961. https://doi.org/10.1016/j.cej.2024.154961.
22. . Ren Y., Si B., Liu Z., Jiang W., Zhang Y. Promoting dark fermentation for biohydrogen production: Potential roles of iron-based additives // International Journal of Hydrogen Energy. 2022; 47:1499-515. https://doi.org/10.1016/j.ijhydene.2021.10.137.
23. . Sharma P., Melkania U. Impact of heavy metals on hydrogen production from organic fraction of municipal solid waste using co-culture of Enterobacter aerogenes and E. Coli // Waste Management. 2018; 75:28996. https://doi.org/10.1016/j.wasman.2018.02.005.
24. . Lu J. -H., Chen C., Huang C., Zhuang H., Leu S. -Y., Lee D. -J. Dark fermentation production of volatile fatty acids from glucose with biochar amended biological consortium // Bioresource Technology. 2020; 303:122921. https://doi.org/10.1016/j.biortech.2020.122921.
25. . Mitov M., Chorbadzhiyska E., Nalbandian L., Hubenova Y. Nickel-based electrodeposits as potential cathode catalysts for hydrogen production by microbial electrolysis // Journal of Power Sources. 2017; 356:467-72. https://doi.org/10.1016/j.jpowsour.2017.02.066.
26. . Cieciura-Włoch W., Borowski S., Domański J. Dark fermentative hydrogen production from hydrolyzed sugar beet pulp improved by iron addition // Bioresource Technology. 2020; 314:123713. https://doi.org/10.1016/j.biortech.2020.123713.
27. . Arisht S. N., Roslan R., Gie G. A., Mahmod S. S., Sajab M. S., Lay C. -H. et al. Effect of nano zero-valent iron (nZVI) on biohydrogen production in anaerobic fermentation of oil palm frond juice using Clostridium butyricum JKT37 // Biomass Bioenergy. 2021; 154:106270. https://doi.org/10.1016/j.biombioe.2021.106270.
28. . Trchounian K., Müller N., Schink B., Trchounian A. Glycerol and mixture of carbon sources conversion to hydrogen by Clostridium beijerinckii DSM791 and effects of various heavy metals on hydrogenase activity // International Journal of Hydrogen Energy. 2017; 42:787582. https://doi.org/10.1016/j.ijhydene.2017.01.011.
29. . Fujinawa K., Nagoya M., Kouzuma A., Watanabe K. Conductive carbon nanoparticles inhibit methanogens and stabilize hydrogen production in microbial electrolysis cells // Applied Microbiology and Biotechnology. 2019; 103:6385-92. https://doi.org/10.1007/s00253-019-09946-1.
30. . Piyush Parkhey, Kush Nayak, Reecha Sahu, Arunima Sur. Confluence of Nanocatalysts and Bioenergy: An Overview of Microbial Electrochemical Systems and Biohydrogen Production // Biohydrogen. 2022, pр. 189-213.
31. . Laikova A. A., Zhuravleva E. A., Kovalev A. A., Shekhurdina S. V., Parshina S. N., Litti Yu. V. Biohydrogen Production by Mono- Versus Co- and Mixed Cultures. In: Soccol CR, Brar SK, Permaul K, Pakshirajan K, De Carvalho JC, editors // Biohydrogen - Advances and Processes, vol. 13, Cham: Springer Nature Switzerland; 2024, pр. 83-123. https://doi.org/10.1007/978-3-03149818-3_5.
32. . Greening C., Biswas A., Carere C. R., Jackson C. J., Taylor M. C., Stott M. B. et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival // The ISME Journal. 2016; 10:761-77. https://doi.org/10.1038/ismej.2015.153.
33. . Benoit S. L., Maier R. J., Sawers R. G., Greening C. Molecular Hydrogen Metabolism: a Widespread Trait of Pathogenic Bacteria and Protists // Microbiology and Molecular Biology Reviews. 2020; 84: e00092-19. https://doi.org/10.1128/MMBR.00092-19.
34. . Trchounian K., Trchounian A. Hydrogenase 2 is most and hydrogenase 1 is less responsible for H2 production by Escherichia coli under glycerol fermentation at neutral and slightly alkaline pH // International Journal of Hydrogen Energy. 2009; 34:8839-45. https://doi.org/10.1016/j.ijhydene.2009.08.056.
35. . Pinske C., Jaroschinsky M., Linek S., Kelly C. L., Sargent F., Sawers R. G. Physiology and Bioenergetics of [NiFe]-Hydrogenase 2-Catalyzed H2 -Consuming and H2 -Producing Reactions in Escherichia coli // Journal of Bacteriology. 2015; 197:296-306. https://doi.org/10.1128/JB.02335-14.
36. . Trchounian K., Gevorgyan H., Sawers G., Trchounian A. Interdependence of Escherichia coli formate dehydrogenase and hydrogen-producing hydrogenases during mixed carbon sources fermentation at different pHs // International Journal of Hydrogen Energy. 2021; 46:5085-99. https://doi.org/10.1016/j.ijhydene.2020.11.082.
37. . Xuan J., He L., Wen W., Feng Y. Hydrogenase and Nitrogenase: Key Catalysts in Biohydrogen Production // Molecules. 2023; 28:1392. https://doi.org/10.3390/molecules28031392.
38. . Ivanenko A. A., Laikova A. A., Zhuravleva E. A., Shekhurdina S. V., Vishnyakova A. V., Kovalev A. A. et al. Biological production of hydrogen: From basic principles to the latest advances in process improvement // International Journal of Hydrogen Energy. 2024; 55:740-55. https://doi.org/10.1016/j.ijhydene.2023.11.179.
39. . Bekbayev K., Mirzoyan S., Toleugazykyzy A., Tlevlessova D., Vassilian A., Poladyan A. et al. Growth and hydrogen production by Escherichia coli during utilization of sole and mixture of sugar beet, alcohol, and beer production waste // Biomass Conv Bioref. 2024; 14:90919. https://doi.org/10.1007/s13399-022-02692-x.
40. . Vanyan L., Aghekyan H., Vassilian A., Poladyan A., Trchounian K. Biotechnological potential of spent coffee grounds for biohydrogen production by Escherichia coli // International Journal of Hydrogen Energy. 2024: S0360319924055939. https://doi.org/10.1016/j.ijhydene.2024.12.380.
41. . Iskandaryan M., Baghdasaryan L., Minasyan E., Trchounian K., Antranikian G., Poladyan A. A novel, cost-effective approach for the production of hydrogenase enzymes and molecular hydrogen from recycled wheybased by-products // International Journal of Hydrogen Energy. 2025; 140:1191-202. https://doi.org/10.1016/j.ijhydene.2024.10.256.
42. . Ghimire A., Frunzo L., Pirozzi F., Trably E., Escudie R., Lens P. N. L. et al. A review on dark fermentative biohydrogen production from organic biomass: Process parameters and use of by-products // Appl Energy. 2015; 144:73-95. https://doi.org/10.1016/j.apenergy.2015.01.045.
43. . Lee D-. J., Show K. -Y., Su A. Dark fermentation on biohydrogen production: Pure culture // Bioresour Technol. 2011; 102:8393-402. https://doi.org/10.1016/j.biortech.2011.03.041.
44. . Summers Z. M., Belahbib H., Pradel N., Bartoli M., Mishra P., Tamburini C. et al. A novel Thermotoga strain TFO isolated from a Californian petroleum reservoir phylogenetically related to Thermotoga petrophila and T. naphthophila, two thermophilic anaerobic isolates from a Japanese reservoir: Taxonomic and genomic considerations // Syst Appl Microbiol. 2020; 43:126132. https://doi.org/10.1016/j.syapm.2020.126132.
45. . Cabrol L., Marone A., Tapia-Venegas E., Steyer J. -P., Ruiz-Filippi G., Trably E. Microbial ecology of fermentative hydrogen producing bioprocesses: useful insights for driving the ecosystem function // FEMS Microbiol Rev. 2017; 41:158-81. https://doi.org/10.1093/femsre/fuw043.
46. . Łukajtis R., Hołowacz I., Kucharska K., Glinka M., Rybarczyk P., Przyjazny A. et al. Hydrogen production from biomass using dark fermentation // Renew Sustain Energy Rev. 2018; 91:665-94. https://doi.org/10.1016/j.rser.2018.04.043.
47. . Dahiya S., Chatterjee S., Sarkar O., Mohan S. V. Renewable hydrogen production by dark-fermentation: Current status, challenges and perspectives // Bioresour Technol. 2021; 321:124354. https://doi.org/10.1016/j.biortech.2020.124354.
48. . Ramprakash B., Incharoensakdi A. Supplementation of magnetic nanoparticles for enhancement of dark fermentative hydrogen production from pretreated garden wastes using Enterobacter aerogenes // Fuel. 2023; 342:127857. https://doi.org/10.1016/j.fuel.2023.127857.
49. . Tondro H., Musivand S., Zilouei H., Bazarganipour M., Zargoosh K. Biological production of hydrogen and acetone- butanol-ethanol from sugarcane bagasse and rice straw using co-culture of Enterobacter aerogenes and Clostridium acetobutylicum // Biomass Bioenergy. 2020; 142:105818. https://doi.org/10.1016/j.biombioe.2020.105818.
50. . Sivaramakrishnan R., Shanmugam S., Sekar M., Mathimani T., Incharoensakdi A., Kim S. -H. et al. Insights on biological hydrogen production routes and potential microorganisms for high hydrogen yield // Fuel. 2021; 291:120136. https://doi.org/10.1016/j.fuel.2021.120136.
51. . Cha M., Chung D., Westpheling J. Deletion of a gene cluster for [Ni-Fe] hydrogenase maturation in the anaerobic hyperthermophilic bacterium Caldicellulosiruptor bescii identifies its role in hydrogen metabolism // Appl Microbiol Biotechnol. 2016; 100:1823-31. https://doi.org/10.1007/s00253-015-7025-z.
52. . Krishnan S., Kamyab H., Nasrullah M., Wahid Z. A., Yadav K. K., Reungsang A. et al. Recent advances in process improvement of dark fermentative hydrogen production through metabolic engineering strategies // Fuel. 2023; 343:127980. https://doi.org/10.1016/j.fuel.2023.127980.
53. . Schoelmerich M. C., Müller V. Energy-converting hydrogenases: the link between H2 metabolism and energy conservation // Cell Mol Life Sci. 2020; 77:1461-81. https://doi.org/10.1007/s00018-019-03329-5.
54. . Kim D. -H., Kim M. -S. Hydrogenases for biological hydrogen production // Bioresource Technology. 2011; 102:8423-31. https://doi.org/10.1016/j.biortech.2011.02.113.
55. . Harirchi S., Wainaina S., Sar T., Nojoumi S. A., Parchami M., Parchami M. et al. Microbiological insights into anaerobic digestion for biogas, hydrogen or volatile fatty acids (VFAs): a review // Bioengineered. 2022; 13:6521-57. https://doi.org/10.1080/21655979.2022.2035986.
56. . Laikova A. A., Zhuravleva E. A., Kovalev A. A., Kovalev D. A., Shekhurdina S. V., Ivanenko A. A. et al. Substrate Composition and Effects on Biohydrogen Production. In: Soccol C. R., Brar S. K., Permaul K., Pakshirajan K., De Carvalho J. C., editors. Biohydrogen - Advances and Processes. – Vol. 13, Cham: Springer Nature Switzerland; 2024, pр. 181-214. https://doi.org/10.1007/978-3-031-49818-3_8.
57. . Eberly J. O., Ely R. L. Thermotolerant Hydrogenases: Biological Diversity, Properties, and Biotechnological Applications // Crit Rev Microbiol. 2008; 34:11730. https://doi.org/10.1080/10408410802240893.
58. . Ivanova G., Rákhely G., Kovács K. L. Thermophilic biohydrogen production from energy plants by Caldicellulosiruptor saccharolyticus and comparison with related studies // International Journal of Hydrogen Energy. 2009; 34:3659-70. https://doi.org/10.1016/j.ijhydene.2009.02.082.
59. . Jiang H., Gadow S. I., Tanaka Y., Cheng J., Li Y. -Y. Improved cellulose conversion to bio-hydrogen with thermophilic bacteria and characterization of microbial community in continuous bioreactor // Biomass Bioenergy. 2015; 75:57-64. https://doi.org/10.1016/j.biombioe.2015.02.010.
60. . Kargi F., Eren N. S., Ozmihci S. Hydrogen gas production from cheese whey powder (CWP) solution by thermophilic dark fermentation // International Journal of Hydrogen Energy. 2012; 37:2260-6. https://doi. org/10.1016/j.ijhydene.2011.11.018.
61. . Khamtib S., Reungsang A. Biohydrogen production from xylose by Thermoanaerobacterium thermosaccharolyticum KKU19 isolated from hot spring sediment // International Journal of Hydrogen Energy. 2012; 37:12219-28. https://doi.org/10.1016/j.ijhydene.2012.06.038.
62. . Luo G., Xie L., Zou Z., Zhou Q., Wang J. -Y. Fermentative hydrogen production from cassava stillage by mixed anaerobic microflora: Effects of temperature and pH // Appl Energy. 2010; 87:3710-7. https://doi.org/10.1016/j.apenergy.2010.07.004.
63. . Ngo T. A., Kim M. -S., Sim S. J. High-yield biohydrogen production from biodiesel manufacturing waste by Thermotoga neapolitana // International Journal of Hydrogen Energy. 2011; 36:5836-42. https://doi.org/10.1016/j.ijhydene.2010.11.057.
64. . Wang Y., He L., Zhang Z., Zhao X., Qi N., Han T. Efficiency enhancement of H2 production by a newly isolated maltose-preferring fermentative bio-hydrogen producer of Clostridium butyricum NH-02 // J Energy Storage. 2020; 30:101426. https://doi.org/10.1016/j.est.2020.101426.
65. . Patel A. K., Debroy A., Sharma S., Saini R., Mathur A., Gupta R. et al. Biohydrogen production from a novel alkalophilic isolate Clostridium sp. IODB-O3 // Bioresour Technol. 2015; 175:291-7. https://doi.org/10.1016/j.biortech.2014.10.110.
66. . Kumar N., Das D. Enhancement of hydrogen production by Enterobacter cloacae IIT-BT 08 // Proc Biochem. 2000; 35:589-93. https://doi.org/10.1016/ S0032-9592(99)00109-0.
67. . Fang H. H. P., Liu H. Effect of pH on hydrogen production from glucose by a mixed culture // Bioresour Technol. 2002; 82:87-93. https://doi.org/10.1016/S09608524(01)00110-9.
68. . Ferreira A. F., Ortigueira J., Alves L., Gouveia L., Moura P., Silva C. M. Energy requirement and CO2 emissions of bioH2 production from microalgal biomass // Biomass Bioenergy. 2013; 49:249-59. https://doi.org/10.1016/j.biombioe.2012.12.033.
69. . Mohanraj S., Pandey A., Venkata Mohan S., Anbalagan K., Kodhaiyolii S., Pugalenthi V. Metabolic Engineering and Molecular Biotechnology of Biohydrogen Production // Biohydrogen, Elsevier. – 2019, p. 413-34. https://doi.org/10.1016/B978-0-444-64203-5.00017-4.
70. . Finney A. J., Sargent F. Formate hydrogenlyase. Advances in Microbial Physiology, vol. 74, Elsevier; 2019, p. 465–86. https://doi.org/10.1016/bs.ampbs.2019.02.004.
71. . Sargent F. The Model [NiFe]-Hydrogenases of Escherichia coli. Advances in Microbial Physiology // Elsevier. 2016; 68:433-507. https://doi.org/10.1016/bs.ampbs.2016.02.008.
72. . Andrews S. C., Berks B. C., McClay J., Ambler A., Quail M. A., Golby P. et al. A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system // Microbiology. 1997; 143:3633-47. https://doi.org/10.1099/00221287-143-113633.
73. . Mirzoyan S., Romero-Pareja P. M., Coello M. D., Trchounian A., Trchounian K. Evidence for hydrogenase-4 catalyzed biohydrogen production in Escherichia coli // International Journal of Hydrogen Energy. 2017; 42:21697-703. https://doi.org/10.1016/j.ijhydene.2017.07.126.
74. . Vanyan L., Trchounian K. HyfF subunit of hydrogenase 4 is crucial for regulating FOF1 dependent proton/potassium fluxes during fermentation of various concentrations of glucose // J Bioenerg Biomembr. 2022; 54:69-79. https://doi.org/10.1007/s10863-022-09930-x.
75. . Fan Q., Neubauer P., Lenz O., Gimpel M. Heterologous Hydrogenase Overproduction Systems for Biotechnology – An Overview // IJMS. 2020; 21:5890. https://doi.org/10.3390/ijms21165890.
76. . Liu Q., Ren Z. J., Huang C., Liu B., Ren N., Xing D. Multiple syntrophic interactions drive biohythane production from waste sludge in microbial electrolysis cells // Biotechnol Biofuels. 2016; 9:162. https://doi.org/10.1186/s13068-016-0579-x.
77. . Pi J., Jawed M., Wang J., Xu L., Yan Y. Mutational analysis of the hyc-operon determining the relationship between hydrogenase-3 and NADH pathway in Enterobacter aerogenes // Enzym Microb Technol. 2016; 82:1-7. https://doi.org/10.1016/j.enzmictec.2015.08.011.
78. . Xiong J., Chan D., Guo X., Chang F., Chen M., Wang Q. et al. Hydrogen production driven by formate oxidation in Shewanella oneidensis MR-1 // Appl Microbiol Biotechnol. 2020; 104:5579-91. https://doi.org/10.1007/s00253-020-10608-w.
79. . Zhao J. -F., Song W. -L., Cheng J., Zhang C. -X. Heterologous expression of a hydrogenase gene in Enterobacter aerogenes to enhance hydrogen gas production // World J Microbiol Biotechnol. 2010; 26:177-81. https://doi.org/10.1007/s11274-009-0139-7.
80. . Soo C. -S., Yap W. -S., Hon W. -M., Ramli N., Md Shah U. K., Phang L. -Y. Improvement of hydrogen yield of ethanol-producing Escherichia coli recombinants in acidic conditions // Electron J Biotechnol. 2017; 26:2732. https://doi.org/10.1016/j.ejbt.2016.12.007.
81. . Vignais P. M., Billoud B. Occurrence, Classification, and Biological Function of Hydrogenases: An Overview // Chem Rev. 2007; 107:4206-72. https://doi.org/10.1021/cr050196r.
82. . Kumar K., Anand A., Moholkar V. S. Molecular Hydrogen (H2) Metabolism in Microbes: A Special Focus on Biohydrogen Production. In: Soccol C. R., Brar S. K., Permaul K., Pakshirajan K., De Carvalho J. C., editors // Biohydrogen – Advances and Processes, vol. 13, Cham: Springer Nature Switzerland; 2024, pр. 25-58. https://doi.org/10.1007/978-3-031-49818-3_2.
83. . Hao X., Wei J., Van Loosdrecht M. C. M., Cao D. Analysing the mechanisms of sludge digestion enhanced by iron // Water Res. 2017; 117:58-67. https://doi.org/10.1016/j.watres.2017.03.048.
84. . Hallenbeck P. C. Fundamentals of Biohydrogen // Biohydrogen, Elsevier; 2013, pр. 25-43. https://doi.org/10.1016/B978-0-444-59555-3.00002-7.
85. . Poudel S., Tokmina-Lukaszewska M., Colman D. R., Refai M., Schut G. J., King P. W. et al. Unification of [FeFe]-hydrogenases into three structural and functional groups. Biochimica et Biophysica Acta (BBA) – Gen Subj. 2016; 1860:1910-21. https://doi.org/10.1016/j.bbagen.2016.05.034.
86. . Goldet G., Brandmayr C., Stripp S. T., Happe T., Cavazza C., Fontecilla-Camps J. C. et al. Electrochemical Kinetic Investigations of the Reactions of [FeFe]-Hydrogenases with Carbon Monoxide and Oxygen: Comparing the Importance of Gas Tunnels and Active-Site Electronic/Redox Effects // J Am Chem Soc. 2009; 131:14979-89. https://doi.org/10.1021/ja905388j.
87. . Corrigan P. S., Majer S. H., Silakov A. Evidence of Atypical Structural Flexibility of the Active Site Surrounding of an [FeFe] Hydrogenase from Clostridium beijerinkii // J Am Chem Soc. 2023; 145:11033-44. https://doi.org/10.1021/jacs.2c13458.
88. . Edenharter K., Jaworek M. W., Engelbrecht V., Winter R., Happe T. H2 production under stress: [FeFe]-hydrogenases reveal strong stability in high pressure environments // Biophysl Chem. 2024; 308:107217. https://doi.org/10.1016/j.bpc.2024.107217.
89. . Lubitz W., Ogata H., Rüdiger O., Reijerse E. Hydrogenases // Chem Rev. 2014; 114:4081-148. https://doi.org/10.1021/cr4005814.
90. . Sidabras J. W., Stripp S. T. A personal account on 25 years of scientific literature on [FeFe]-hydrogenase // J Biol Inorg Chem. 2023; 28:355-78. https://doi.org/10.1007/s00775-023-01992-5.
91. . Birrell J. A., Rodríguez-Maciá P., Reijerse E. J., Martini M. A., Lubitz W. The catalytic cycle of [FeFe] hydrogenase: A tale of two sites // Coord Chem Rev. 2021; 449:214191. https://doi.org/10.1016/j.ccr.2021.214191.
92. . Winkler M., Duan J., Rutz A., Felbek C., Scholtysek L., Lampret O. et al. A safety cap protects hydrogenase from oxygen attack // Nat Commun. 2021; 12:756. https://doi.org/10.1038/s41467-020-20861-2.
93. . Dutta T., Das A. K., Das D. Purification and characterization of [Fe]-hydrogenase from high yielding hydrogen-producing strain, Enterobacter cloacae IITBT08 (MTCC 5373) // International Journal of Hydrogen Energy. 2009; 34:7530-7. https://doi.org/10.1016/j.ijhydene.2009.05.076.
94. . Di Leonardo P. F., Antonicelli G., Agostino V., Re A. Genome-Scale Mining of Acetogens of the Genus Clostridium Unveils Distinctive Traits in [FeFe]- and [NiFe]-Hydrogenase Content and Maturation // Microbiol Spectr. 2022; 10:e01019-22. https://doi.org/10.1128/spectrum.01019-22.
95. . Zhao X., Wang Z., Zhou X., Qi N., Chen F., Li D. et al. Full length obtains of hydA and phylogenetic analysis of bio-hydrogen production new species of Clostridium based on efficient hydA degenerate primers // International Journal of Hydrogen Energy. 2019; 44:294939. https://doi.org/10.1016/j.ijhydene.2019.05.050.
96. . Schut G. J., Adams M. W. W. The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production // J Bacteriol. 2009; 191:4451-7. https://doi.org/10.1128/JB.01582-08.
97. . Wang S., Huang H., Kahnt J., Thauer R. K. A Reversible Electron-Bifurcating Ferredoxin- and NAD-Dependent [FeFe]-Hydrogenase (HydABC) in Moorella thermoacetica // J Bacteriol. 2013; 195:1267-75. https://doi.org/10.1128/JB.02158-12.
98. . Morra S. Fantastic [FeFe]-Hydrogenases and Where to Find Them // Front Microbiol. 2022; 13:853626. https://doi.org/10.3389/fmicb.2022.853626.
99. . Schuchmann K., Chowdhury N. P., Müller V. Complex Multimeric [FeFe] Hydrogenases: Biochemistry, Physiology and New Opportunities for the Hydrogen Economy // Front Microbiol. 2018; 9:2911. https://doi.org/10.3389/fmicb.2018.02911.
100. . Sinha P., Roy S., Das D. Genomic and proteomic approaches for dark fermentative biohydrogen production // Renew Sustain Energy Rev. 2016; 56:130821. https://doi.org/10.1016/j.rser.2015.12.035.
101. . Huang H., Wang S., Moll J., Thauer R. K. Electron Bifurcation Involved in the Energy Metabolism of the Acetogenic Bacterium Moorella thermoacetica Growing on Glucose or H2 plus CO2 // J Bacteriol. 2012; 194:3689-99. https://doi.org/10.1128/JB.00385-12.
102. . Peters J. W., Miller A. -F., Jones A. K., King P. W., Adams M. W. Electron bifurcation // Curr Opini Chem Biol. 2016; 31:146-52. https://doi.org/10.1016/j.cbpa.2016.03.007.
103. . Wang S., Huang H., Kahnt J., Mueller A. P., Köpke M., Thauer R. K. NADP-Specific Electron-Bifurcating [FeFe]-Hydrogenase in a Functional Complex with Formate Dehydrogenase in Clostridium autoethanogenum Grown on CO // J Bacteriol. 2013; 195:4373-86. https://doi.org/10.1128/JB.00678-13.
104. . Shaw A. J., Hogsett D. A., Lynd L. R. Identification of the [FeFe]-Hydrogenase Responsible for Hydrogen Generation in Thermoanaerobacterium saccharolyticum and Demonstration of Increased Ethanol Yield via Hydrogenase Knockout // J Bacteriol. 2009; 191:6457-64. https://doi.org/10.1128/JB.00497-09.
105. . Eminoğlu A., Murphy S. J. -L., Maloney M., Lanahan A., Giannone R. J., Hettich R. L. et al. Deletion of the hfsB gene increases ethanol production in Thermoanaerobacterium saccharolyticum and several other thermophilic anaerobic bacteria // Biotechnol Biofuels. 2017; 10:282. https://doi.org/10.1186/s13068-017-0968-9.
106. . Payne N., Kpebe A., Guendon C., Baffert C., Ros J., Lebrun R. et al. The electron-bifurcating FеFehydrogenase Hnd is involved in ethanol metabolism in Desulfovibrio fructosovorans grown on pyruvate // Mol Microbiol. 2022; 117:907-20. https://doi.org/10.1111/mmi.14881.
107. . Zhang K., Ren N. -Q., Cao G. -L., Wang A. -J. Biohydrogen production behavior of moderately thermophile Thermoanaerobacterium thermosaccharolyticum W16 under different gas-phase conditions // International Journal of Hydrogen Energy. 2011; 36:14041-8. https://doi.org/10.1016/j.ijhydene.2011.04.056.
108. . Sorokin D. Y., Gumerov V. M., Rakitin A. L., Beletsky A. V., Damsté J. S. S., Muyzer G. et al. Genome analysis of Chitinivibrio alkaliphilus gen. nov., sp. nov., a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum Termite Group 3 // Environ Microbiol. 2014; 16:1549-65. https://doi.org/10.1111/1462-2920.12284.
109. . Payne N., Kpebe A., Guendon C., Baffert C., Maillot M., Haurogné T. et al. NMR-based metabolomic analysis of the physiological role of the electron-bifurcating FeFe-hydrogenase Hnd in Solidesulfovibrio fructosivorans under pyruvate fermentation // Microbiol Res. 2023; 268:127279. https://doi.org/10.1016/j.micres.2022.127279.
110. . Dai K., Qu C., Li X., Lan Y., Fu H., Wang J. Cofactor engineering in Thermoanaerobacterium aotearoense SCUT27 for maximizing ethanol yield and revealing an enzyme complex with high ferredoxin-NAD+ reductase activity // Bioresour Technol. 2024; 402:130784. https://doi.org/10.1016/j.biortech.2024.130784.
111. . Cabotaje P. R., Walter K., Zamader A., Huang P., Ho F., Land H. et al. Probing Substrate Transport Effects on Enzymatic Hydrogen Catalysis: An Alternative Proton Transfer Pathway in Putatively Sensory [FeFe]-Hydrogenase // ACS Catal. 2023; 13:10435-46. https://doi.org/10.1021/acscatal.3c02314.
112. . Land H., Sekretareva A., Huang P., Redman H. J., Németh B., Polidori N. et al. Characterization of a putative sensory [FeFe]-hydrogenase provides new insight into the role of the active site architecture // Chem Sci. 2020; 11:12789-801. https://doi.org/10.1039/D0SC03319G.
113. . Vignais P. Classification and phylogeny of hydrogenases // FEMS Microbiology Reviews. 2001; 25:455501. https://doi.org/10.1016/S0168-6445(01)00063-8.
114. . Caserta G., Hartmann S., Van Stappen C., Karafoulidi-Retsou C., Lorent C., Yelin S. et al. Stepwise assembly of the active site of [NiFe]-hydrogenase // Nat Chem Biol. 2023; 19:498-506. https://doi.org/10.1038/s41589-022-01226-w.
115. . Lubitz W., Reijerse E., Van Gastel M. [NiFe] and [FeFe] Hydrogenases Studied by Advanced Magnetic Resonance Techniques // Chem Rev. 2007; 107:4331-65. https://doi.org/10.1021/cr050186q.
116. . Shafaat H. S., Rüdiger O., Ogata H., Lubitz W. [NiFe] hydrogenases: A common active site for hydrogen metabolism under diverse conditions. Biochimica et Biophysica Acta (BBA) – Bioenergetics. 2013; 1827:9861002. https://doi.org/10.1016/j.bbabio.2013.01.015.
117. . Ogata H., Lubitz W., Higuchi Y. Structure and function of [NiFe] hydrogenases // J Biochem. 2016; 160:251-8. https://doi.org/10.1093/jb/mvw048.
118. . Radan A., Milčić N., Sudar M., Findrik Blažević Z., Marić A. -K. Hydrogenases – Types, Sources, Properties, and the Potential for Their Application. Kem Ind (Online). 2025; 74:33-42. https://doi.org/10.15255/KUI.2024.018.
119. . Shomura Y., Taketa M., Nakashima H., Tai H., Nakagawa H., Ikeda Y. et al. Structural basis of the redox switches in the NAD+-reducing soluble [NiFe]-hydrogenase // Science. 2017; 357:928-32. https://doi. org/10.1126/science.aan4497.
120. . Kulkarni G., Mand T. D., Metcalf W. W. Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri. mBio. 2018; 9:e01256-18. https://doi.org/10.1128/mBio.01256-18.
121. . Mand T. D., Metcalf W. W. Energy Conservation and Hydrogenase Function in Methanogenic Archaea, in Particular the Genus Methanosarcina // Microbiol Mol Biol Rev. 2019; 83: e00020-19. https://doi.org/10.1128/MMBR.00020-19.
122. . Gutekunst K., Chen X., Schreiber K., Kaspar U., Makam S., Appel J. The Bidirectional [NiFe]-hydrogenase in Synechocystis sp. PCC 6803 Is Reduced by Flavodoxin and Ferredoxin and Is Essential under Mixotrophic, Nitrate-limiting Conditions // J Biol Chem. 2014; 289:1930-7. https://doi.org/10.1074/jbc.M113.526376.
123. . Trchounian K., Poladyan A., Vassilian A., Trchounian A. Multiple and reversible hydrogenases for hydrogen production by Escherichia coli: dependence on fermentation substrate, pH and the F0 F1 -ATPase // Crit Rev Biochem Mol Biol. 2012; 47:236-49. https://doi.org/10.3109/10409238.2012.655375.
124. . Constant P., Hallenbeck P. C. Hydrogenase // Biohydrogen, Elsevier; 2019, pр. 49-78. https://doi.org/10.1016/B978-0-444-64203-5.00003-4.
125. . Wiechert M., Beitz E. Mechanism of formate– nitrite transporters by dielectric shift of substrate acidity // The EMBO Journal. 2017; 36:949-58. https://doi.org/10.15252/embj.201695776.
126. . Trchounian K., Trchounian A. Escherichia coli hydrogenase 4 (hyf) and hydrogenase 2 (hyb) contribution in H2 production during mixed carbon (glucose and glycerol) fermentation at pH 7,5 and pH 5,5 // International Journal of Hydrogen Energy. 2013; 38:3921-9. https://doi.org/10.1016/j.ijhydene.2013.01.138.
127. . Poladyan A., Margaryan L., Trchounian K., Trchounian A. Biomass and biohydrogen production during dark fermentation of Escherichia coli using office paper waste and cardboard // International Journal of Hydrogen Energy. 2020; 45:286-93. https://doi.org/10.1016/j.ijhydene.2019.10.246.
128. . McDowall J. S., Murphy B. J., Haumann M., Palmer T., Armstrong F. A., Sargent F. Bacterial formate hydrogenlyase complex // Proc Natl Acad Sci USA. 2014; 111. https://doi.org/10.1073/pnas.1407927111.
129. . Skibinski D. A. G., Golby P., Chang Y. -S., Sargent F., Hoffman R., Harper R. et al. Regulation of the Hydrogenase-4 Operon of Escherichia coli by the σ54Dependent Transcriptional Activators FhlA and HyfR // J Bacteriol. 2002; 184:6642-53. https://doi.org/10.1128/JB.184.23.6642-6653.2002.
130. . Matsumura Y., Al-saari H., Mino S., Nakagawa S., Maruyama F., Ogura Y. et al. Identification of a gene cluster responsible for hydrogen evolution in Vibrio tritonius strain AM2 with transcriptional analyses // International Journal of Hydrogen Energy. 2015; 40:9137-46. https://doi.org/10.1016/j.ijhydene.2015.05.137.
131. . Self W. T., Hasona A., Shanmugam K. T. Expression and Regulation of a Silent Operon, hyf, Coding for Hydrogenase 4 Isoenzyme in Escherichia coli // J Bacteriol. 2004; 186:580-7. https://doi.org/10.1128/JB.186.2.580-587.2004.
132. . Metcalfe G. D., Sargent F., Hippler M. Hydrogen production in the presence of oxygen by Escherichia coli K-12 // Microbiology. 2022; 168. https://doi.org/10.1099/mic.0.001167.
133. . Wang M., Zhao Q., Li L., Niu K., Li Y., Wang F. et al. Contributing factors in the improvement of cellulosic H2 production in Clostridium thermocellum/ Thermoanaerobacterium co-cultures // Appl Microbiol Biotechnol. 2016; 100:8607-20. https://doi.org/10.1007/s00253-016-7776-1.
134. . Pereira I. A. C., Ramos A. R., Grein F., Marques M. C., Da Silva S. M., Venceslau S. S. A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea // Front Microbiol. 2011; 2. https://doi.org/10.3389/fmicb.2011.00069.
135. . Fu H., Yang X., Qu C., Li Y., Wang J. Enhanced ethanol production from lignocellulosic hydrolysates by inhibiting the hydrogen synthesis in Thermoanaerobacterium aotearoense SCUT27(Δ ldh) // J Chem Tech Biotech. 2019; 94:3305-14. https://doi.org/10.1002/jctb.6141.
136. . De Souza L. C., Herring C. D., Lynd L. R. Genetic investigation of hydrogenases in Thermoanaerobacterium thermosaccharolyticum suggests that redox balance via hydrogen cycling enables high ethanol yield // Appl Environ Microbiol. 2025; 91: e01109-24. https://doi.org/10.1128/aem.01109-24.
137. . Calusinska M., Happe T., Joris B., Wilmotte A. The surprising diversity of clostridial hydrogenases: a comparative genomic perspective // Microbiology. 2010; 156:1575-88. https://doi.org/10.1099/mic.0.032771-0.
138. . Calusinska M., Hamilton C., Monsieurs P., Mathy G., Leys N., Franck F. et al. Genome-wide transcriptional analysis suggests hydrogenase- and nitrogenase-mediated hydrogen production in Clostridium butyricum CWBI 1009 // Biotechnol Biofuels. 2015; 8:27. https://doi.org/10.1186/s13068-015-0203-5.
139. . Hamilton C., Calusinska M., Baptiste S., Masset J., Beckers L., Thonart P. et al. Effect of the nitrogen source on the hydrogen production metabolism and hydrogenases of Clostridium butyricum CWBI1009 // International Journal of Hydrogen Energy. 2018; 43:5451-62. https://doi.org/10.1016/j.ijhydene.2017.12.162.
140. . Biswas R., Zheng T., Olson D. G., Lynd L. R., Guss A. M. Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum // Biotechnol Biofuels. 2015; 8:20. https://doi.org/10.1186/s13068-015-0204-4.
141. . Sander K., Wilson C. M., Rodriguez M., Klingeman D. M., Rydzak T., Davison B. H. et al. Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation // Biotechnol Biofuels. 2015; 8:211. https://doi.org/10.1186/s13068-015-0394-9.
142. . Holwerda E. K., Olson D. G., Ruppertsberger N. M., Stevenson D. M., Murphy S. J. L., Maloney MI, et al. Metabolic and evolutionary responses of Clostridium thermocellum to genetic interventions aimed at improving ethanol production // Biotechnol Biofuels. 2020; 13:40. https://doi.org/10.1186/s13068-020-01680-5.
143. . Therien J. B., Artz J. H., Poudel S., Hamilton T. L., Liu Z., Noone S. M. et al. The Physiological Functions and Structural Determinants of Catalytic Bias in the [FeFe]-Hydrogenases CpI and CpII of Clostridium pasteurianum Strain W5 // Front Microbiol. 2017; 8:1305. https://doi.org/10.3389/fmicb.2017.01305.
144. . Pradhan N., Dipasquale L., D’Ippolito G., Panico A., Lens P., Esposito G. et al. Hydrogen Production by the Thermophilic Bacterium Thermotoga neapolitana // IJMS. 2015; 16:12578-600. https://doi.org/10.3390/ijms160612578.
145. . Bielen A. A. M., Verhaart M. R. A., VanFossen A. L., Blumer-Schuette S. E., Stams A. J. M., Van Der Oost J. et al. A thermophile under pressure: Transcriptional analysis of the response of Caldicellulosiruptor saccharolyticus to different H2 partial pressures // International Journal of Hydrogen Energy. 2013; 38:1837-49. https://doi.org/10.1016/j.ijhydene.2012.11.082.
146. . Pawar S. S. Caldicellulosiruptor saccharolyticus: an ideal hydrogen producer? Lund: Division of Applied Microbiology, Department of Chemistry, Lund University; 2014.
147. . Shen N., Huo Y. -C., Chen J. -J., Zhang F., Zheng H., Zeng R. J. Decolorization by Caldicellulosiruptor saccharolyticus with dissolved hydrogen under extreme thermophilic conditions // Chem Eng J. 2015; 262:847-53. https://doi.org/10.1016/j.cej.2014.10.053.
148. . Castro J. F., Razmilic V., Gerdtzen Z. P. Genome based metabolic flux analysis of Ethanoligenens harbinense for enhanced hydrogen production // International Journal of Hydrogen Energy. 2013; 38:1297-306. https://doi.org/10.1016/j.ijhydene.2012.11.007.
149. . Li Z., Lou Y., Ding J., Liu B. -F., Xie G. -J., Ren N. -Q. et al. Metabolic regulation of ethanol-type fermentation of anaerobic acidogenesis at different pH based on transcriptome analysis of Ethanoligenens harbinense // Biotechnol Biofuels. 2020; 13:101. https://doi.org/10.1186/s13068-020-01740-w.
150. . Zhao J., Song W., Cheng J., Liu M., Zhang C., Cen K. Improvement of fermentative hydrogen production using genetically modified Enterobacter aerogenes // International Journal of Hydrogen Energy. 2017; 42:3676-81. https://doi.org/10.1016/j.ijhydene.2016.08.161.
151. . Mishra J., Khurana S., Kumar N., Ghosh A. K., Das D. Molecular cloning, characterization, and overexpression of a novel [Fe]-hydrogenase isolated from a high rate of hydrogen producing Enterobacter cloacae IIT-BT 08 // Biochem Biophys Res Commun. 2004; 324:679-85. https://doi.org/10.1016/j.bbrc.2004.09.108.
152. . Song W., Cheng J., Zhao J., Carrieri D., Zhang C., Zhou J. et al. Improvement of hydrogen production by over-expression of a hydrogen-promoting protein gene in Enterobacter cloacae // International Journal of Hydrogen Energy. 2011; 36:6609-15. https://doi.org/10.1016/j.ijhydene.2011.02.086.
153. . Bai L., Wu X., Jiang L., Liu J., Long M. Hydrogen production by over-expression of hydrogenase subunit in oxygen-tolerant Klebsiella oxytoca HP1 // I International Journal of Hydrogen Energy. 2012; 37:13227-33. https://doi.org/10.1016/j.ijhydene.2012.03.048.
154. . Raman B., McKeown C. K., Rodriguez M., Brown S. D., Mielenz J. R. Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation // BMC Microbiol. 2011; 11:134. https://doi.org/10.1186/1471-2180-11-134.
155. . Siegbahn P. E. M., Tye J. W., Hall M. B. Computational Studies of [NiFe] and [FeFe] Hydrogenases // Chem Rev. 2007; 107:4414-35. https://doi.org/10.1021/cr050185y.
156. . Szőri-Dorogházi E., Maróti G., Szőri M., Nyilasi A., Rákhely G., Kovács K. L. Analyses of the Large Subunit Histidine-Rich Motif Expose an Alternative Proton Transfer Pathway in [NiFe]-Hydrogenases // PLoS ONE. 2012; 7: e34666. https://doi.org/10.1371/journal.pone.0034666.
157. . Tai H., Hirota S. Mechanism and Application of the Catalytic Reaction of [NiFe] Hydrogenase: Recent Developments // ChemBioChem. 2020; 21:1573-81. https://doi.org/10.1002/cbic.202000058.
158. . Watanabe S., Matsumi R., Atomi H., Imanaka T., Miki K. Crystal Structures of the HypCD Complex and the HypCDE Ternary Complex: Transient Intermediate Complexes during [NiFe] Hydrogenase Maturation // Structure. 2012; 20:2124-37. https://doi.org/10.1016/j.str.2012.09.018.
159. . McGlynn S. E., Shepard E. M., Winslow M. A., Naumov A. V., Duschene K. S., Posewitz M. C. et al. HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis // FEBS Letters. 2008; 582:21837. https://doi.org/10.1016/j.febslet.2008.04.063.
160. . Kuchenreuther J. M., Myers W. K., Suess D. L. M., Stich T. A., Pelmenschikov V., Shiigi S. A. et al. The HydG Enzyme Generates an Fe(CO)2 (CN) Synthon in Assembly of the [FeFe]-Hydrogenase H-Cluster // Science. 2014; 343:424-7. https://doi.org/10.1126/science.1246572.
161. . Lin R., Cheng J., Ding L., Song W., Liu M., Zhou J. et al. Enhanced dark hydrogen fermentation by addition of ferric oxide nanoparticles using Enterobacter aerogenes // Bioresour Technol. 2016; 207:213-9. https://doi.org/10.1016/j.biortech.2016.02.009.
162. . Arizzi M., Morra S., Gilardi G., Pugliese M., Gullino M. L., Valetti F. Improving sustainable hydrogen production from green waste: [FeFe]-hydrogenases quantitative gene expression RT-qPCR analysis in presence of autochthonous consortia // Biotechnol Biofuels. 2021; 14:182. https://doi.org/10.1186/s13068-021-02028-3.
163. . Calusinska M., Joris B., Wilmotte A. Genetic diversity and amplification of different clostridial [FeFe] hydrogenases by group-specific degenerate primers: Amplification of [FeFe]-hydrogenases // Lett Appl Microbiol. 2011; 53:473-80. https://doi.org/10.1111/j.1472765X.2011.03135.x.
164. . Thanh P. M., Ketheesan B., Yan Z., Stuckey D. Trace metal speciation and bioavailability in anaerobic digestion: A review // Biotechnol Adv. 2016; 34:122-36. https://doi.org/10.1016/j.biotechadv.2015.12.006.
165. . Cheng J., Li H., Zhang J., Ding L., Ye Q., Lin R. Enhanced dark hydrogen fermentation of Enterobacter aerogenes/HoxEFUYH with carbon cloth // International Journal of Hydrogen Energy. 2019; 44:3560-8. https://doi.org/10.1016/j.ijhydene.2018.12.080.
166. . Park J. -H., Kim D. -H., Kim H. -S., Wells G. F., Park H. -D. Granular activated carbon supplementation alters the metabolic flux of Clostridium butyricum for enhanced biohydrogen production // Bioresour Technol. 2019; 281:318-25. https://doi.org/10.1016/j.biortech.2019.02.090.
167. . Yang J., Sim Y. -B., Kim S. M., Joo H. -H., Mašek O., Kim S. -H. Synergetic effects of conductive materials and bacterial population in inoculum on mixed-culture biohydrogen production // International Journal of Hydrogen Energy. 2024; 53:1293-302. https://doi.org/10.1016/j.ijhydene.2023.12.103.
168. . Hajdek M., Ardabili S., Ghaebi H., Mosavi A. Nanoadditives for Enzymatic Biohydrogen Production // ACTA POLYTECH HUNG. 2025; 22:7-25. https://doi.org/10.12700/APH.22.3.2025.3.1.
169. . Zhang Y., Liu G., Shen J. Hydrogen production in batch culture of mixed bacteria with sucrose under different iron concentrations // International Journal of Hydrogen Energy. 2005; 30:855-60. https://doi.org/10.1016/j.ijhydene.2004.05.009.
170. . Taherdanak M., Zilouei H., Karimi K. Investigating the effects of iron and nickel nanoparticles on dark hydrogen fermentation from starch using central composite design // International Journal of Hydrogen Energy. 2015; 40:12956-63. https://doi.org/10.1016/j.ijhydene.2015.08.004.
171. . Konhauser K. O., Kappler A., Roden E. E. IRON IN MICROBIAL METABOLISMS // Elements. 2011; 7:89-93. https://doi.org/10.2113/gselements.7.2.89.
172. . Wang J., Wan W. Influence of Ni2+ concentration on biohydrogen production // Bioresour Technol. 2008; 99:8864-8. https://doi.org/10.1016/j.biortech.2008.04.052.
173. . Bundhoo M. A. Z., Mohee R. Inhibition of dark fermentative bio-hydrogen production: A review // International Journal of Hydrogen Energy. 2016; 41:6713-33. https://doi.org/10.1016/j.ijhydene.2016.03.057.
174. . Tirapanampai C., Intasian P., Uthaipaisanwong P., Kusonmano K., Weeranoppanant N., Chaiyen P. et al. Metal additives for boosting hydrogen production in anaerobic fermentation: Focus on the change of gene expression and cost analysis // Jf Clean Prod 2023; 414:137609. https://doi.org/10.1016/j.jclepro.2023.137609.
175. . Taherdanak M., Zilouei H., Karimi K. The effects of Fe0 and Ni0 nanoparticles versus Fe2+ and Ni2+ ions on dark hydrogen fermentation // International Journal of Hydrogen Energy. 2016; 41:167-73. https://doi.org/10.1016/j.ijhydene.2015.11.110.
176. . Zhang Q., Li Y., Jiang H., Liu Z., Jia Q. Enhanced Biohydrogen Production Influenced by Magnetic Nanoparticles Supplementation Using Enterobacter cloacae // Waste Biomass Valor. 2021; 12:2905-13. https://doi.org/10.1007/s12649-020-01002-8.
177. . Elreedy A., Fujii M., Koyama M., Nakasaki K., Tawfik A. Enhanced fermentative hydrogen production from industrial wastewater using mixed culture bacteria incorporated with iron, nickel, and zinc-based nanoparticles // Water Res. 2019; 151:349-61. https://doi.org/10.1016/j.watres.2018.12.043.
178. . Zhang L., Chung J., Ren N., Sun R. Effects of the ecological factors on hydrogen production and [FeFe]-hydrogenase activity in Ethanoligenens harbinense YUAN-3 // International Journal of Hydrogen Energy. 2015; 40:6792-7. https://doi.org/10.1016/j.ijhydene.2015.02.015.
179. . Cao X., Zhao L., Dong W., Mo H., Ba T., Li T. et al. Revealing the mechanisms of alkali-based magnetic nanosheets enhanced hydrogen production from dark fermentation: Comparison between mesophilic and thermophilic conditions // Bioresour Technol. 2022; 343:126141. https://doi.org/10.1016/j.biortech.2021.126141.
180. . Zhang M., Zhang L., Tian S., Zhu S., Chen Z., Si H. The effect of zero-valent iron/Fe3+ coupling and reuse on the properties of anoxic sludge // J Clean Prod. 2022; 344:131031. https://doi.org/10.1016/j.jclepro.2022.131031.
181. . Chen Y., Yin Y., Wang J. Recent advance in inhibition of dark fermentative hydrogen production // International Journal of Hydrogen Energy. 2021; 46:5053-73. https://doi.org/10.1016/j.ijhydene.2020.11.096.
182. . Hidalgo D., Martín-Marroquín J. M., Corona F. The role of magnetic nanoparticles in dark fermentation // Biomass Conv Bioref. 2023; 13:16299-320. https://doi.org/10.1007/s13399-023-04103-1.
183. . Xu F. F., Imlay J. A. Silver(I), Mercury (II), Cadmium (II), and Zinc (II) Target Exposed Enzymic Iron-Sulfur Clusters when They Toxify Escherichia coli // Appl Environ Microbiol. 2012; 78:3614-21. https://doi.org/10.1128/AEM.07368-11.
184. . Sun Y., Ma Y., Zhang B., Sun H., Wang N., Wang L. et al. Comparison of magnetite/reduced graphene oxide nanocomposites and magnetite nanoparticles on enhancing hydrogen production in dark fermentation // International Journal of Hydrogen Energy. 2022; 47:22359-70. https://doi.org/10.1016/j.ijhydene.2022.05.073.
185. . Bennett B. D., Brutinel E. D., Gralnick J. A. A Ferrous Iron Exporter Mediates Iron Resistance in Shewanella oneidensis MR-1 // Appl Environ Microbiol. 2015; 81:7938-44. https://doi.org/10.1128/AEM.0283515.
186. . Sun H., Shen J., Hu M., Zhang J., Cai Z., Zang L. et al. Manganese ferrite nanoparticles enhanced biohydrogen production from mesophilic and thermophilic dark fermentation // Energy Rep. 2021; 7:6234-45. https://doi.org/10.1016/j.egyr.2021.09.070.
187. . Lee D., Li Y., Oh Y., Kim M., Noike T. Effect of iron concentration on continuous H2 production using membrane bioreactor // International Journal of Hydrogen Energy. 2009; 34:1244-52. https://doi.org/10.1016/j.ijhydene.2008.11.093.
188. . Liu H., Zhang T., Fang H. H. P. Thermophilic H2 production from a cellulose-containing wastewater // Biotechnol Lett. 2003; 25:365-9. https://doi.org/10.1023/A:1022341113774.
189. . Pagnier A., Balci B., Shepard E. M., Broderick WE, Broderick JB. [FeFe]-Hydrogenase In Vitro Maturation // Angew Chem Int Ed. 2022; 61: e202212074. https://doi.org/10.1002/anie.202212074.
190. . Zhang L., Xu D., Kong D., Ji M., Shan L., Zhao Y. Improving dark fermentative hydrogen production through zero-valent iron/copper (Fe/Cu) micro-electrolysis // Biotechnol Lett. 2020; 42:445-51. https://doi.org/10.1007/s10529-020-02793-5.
191. . Ziganshin A. M., Wintsche B., Seifert J., Carstensen M., Born J., Kleinsteuber S. Spatial separation of metabolic stages in a tube anaerobic baffled reactor: reactor performance and microbial community dynamics // Appl Microbiol Biotechnol. 2019; 103:3915-29. https://doi.org/10.1007/s00253-019-09767-2.
192. . Zhao X., Xing D., Liu B., Lu L., Zhao J., Ren N. The effects of metal ions and l-cysteine on hydA gene expression and hydrogen production by Clostridium beijerinckii RZF-1108 // International Journal of Hydrogen Energy. 2012; 37:13711-7. https://doi.org/10.1016/j.ijhydene.2012.02.144.
193. . Reddy K., Nasr M., Kumari S., Kumar S., Gupta S. K., Enitan A. M. et al. Biohydrogen production from sugarcane bagasse hydrolysate: effects of pH, S/X, Fe2+, and magnetite nanoparticles // Environ Sci Pollut Res. 2017; 24:8790-804. https://doi.org/10.1007/s11356017-8560-1.
194. . Mamimin C., Probst M., Gómez-Brandón M., Podmirseg S. M., Insam H., Reungsang A. et al. Trace metals supplementation enhanced microbiota and biohythane production by two-stage thermophilic fermentation. // International Journal of Hydrogen Energy. 2019; 44:3325-38. https://doi.org/10.1016/j.ijhydene.2018.09.065.
195. . Hsieh P. -H., Lai Y. -C., Chen K. -Y., Hung C. -H. Explore the possible effect of TiO2 and magnetic hematite nanoparticle addition on biohydrogen production by Clostridium pasteurianum based on gene expression measurements // International Journal of Hydrogen Energy. 2016; 41:21685-91. https://doi.org/10.1016/j.ijhydene.2016.06.197.
196. . Zhao X., Xing D., Qi N., Zhao Y., Hu X., Ren N. Deeply mechanism analysis of hydrogen production enhancement of Ethanoligenens harbinense by Fe2+ and Mg2+: Monitoring at growth and transcription levels // International Journal of Hydrogen Energy. 2017; 42:19695700. https://doi.org/10.1016/j.ijhydene.2017.06.038.
197. . Bu J., Ju X. -W., Liang L. -X., Zhao Q. -Z., Wei Tiong Y., Wu H. -Z. et al. Molecular mechanism of boosted hydrogen production by Thermoanaerobacterium thermosaccharolyticum with biochar revealed by transcriptome analysis // Chem Eng J. 2024; 500:156903. https://doi.org/10.1016/j.cej.2024.156903.
198. . Jamali N. S., Jahim J. M., Isahak W. N. R. W., Abdul P. M. Particle size variations of activated carbon on biofilm formation in thermophilic biohydrogen production from palm oil mill effluent // Energy Convers Manag. 2017; 141:354-66. https://doi.org/10.1016/j.enconman.2016.09.067.
199. . Cheng D., Ngo H. H., Guo W., Chang S. W., Nguyen D. D., Deng L. et al. Advanced strategies for enhancing dark fermentative biohydrogen production from biowaste towards sustainable environment // Bioresour Technol. 2022; 351:127045. https://doi.org/10.1016/j.biortech.2022.127045.
200. . Goveas L. C., Nayak S., Kumar P. S., Vinayagam R., Selvaraj R., Rangasamy G. Recent advances in fermentative biohydrogen production // International Journal of Hydrogen Energy. 2024; 54:200-17. https://doi.org/10.1016/j.ijhydene.2023.04.208.
201. . Song W., Cheng J., Zhao J., Zhang C., Zhou J., Cen K. Enhancing hydrogen production of Enterobacter aerogenes by heterologous expression of hydrogenase genes originated from Synechocystis sp. // Bioresour Technol. 2016; 216:976-80. https://doi.org/10.1016/j.biortech.2016.06.044.
202. . Khanna N., Dasgupta C. N., Mishra P., Das D. Homologous overexpression of [FeFe] hydrogenase in Enterobacter cloacae IIT-BT 08 to enhance hydrogen gas production from cheese whey // International Journal of Hydrogen Energy. 2011; 36:15573-82. https://doi.org/10.1016/j.ijhydene.2011.09.020.
203. . King P. W., Posewitz M. C., Ghirardi M. L., Seibert M. Functional Studies of [FeFe] Hydrogenase Maturation in an Escherichia coli Biosynthetic System // J Bacteriol. 2006; 188:2163-72. https://doi.org/10.1128/JB.188.6.2163-2172.2006.
204. . Kuchenreuther J. M., Grady-Smith C. S., Bingham A. S., George S. J., Cramer S. P., Swartz J. R. HighYield Expression of Heterologous [FeFe]-Hydrogenases in Escherichia coli // PLoS ONE. 2010; 5: e15491. https://doi.org/10.1371/journal.pone.0015491.
205. . Schumann C., Fernández Méndez J., Berggren G., Lindblad P. Novel concepts and engineering strategies for heterologous expression of efficient hydrogenases in photosynthetic microorganisms // Front Microbiol. 2023; 14:1179607. https://doi.org/10.3389/fmicb.2023.1179607.
206. . Ducat D. C., Sachdeva G., Silver P. A. Rewiring hydrogenase-dependent redox circuits in cyanobacteria // Proc Natl Acad Sci USA. 2011; 108:3941-6. https://doi.org/10.1073/pnas.1016026108.
207. . Berto P., D’Adamo S., Bergantino E., Vallese F., Giacometti G. M., Costantini P. The cyanobacterium Synechocystis sp. PCC 6803 is able to express an active [FeFe]-hydrogenase without additional maturation proteins // Biochem Biophys Res Commun. 2011; 405:678-83. https://doi.org/10.1016/j.bbrc.2011.01.095.
208. . Bai R., Chu W., Qiao Z., Lu P., Jiang K., Xu Y. et al. Metabolic regulation of NADH supply and hydrogen production in Enterobacter aerogenes by multigene engineering // International Journal of Hydrogen Energy. 2023; 48:909-20. https://doi.org/10.1016/j.ijhydene.2022.10.015.
209. . Maeda T., Vardar G., Self W. T., Wood T. K. Inhibition of hydrogen uptake in Escherichia coli by expressing the hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 // BMC Biotechnol. 2007; 7:25. https://doi.org/10.1186/1472-6750-7-25.
210. . Zhou P., Wang Y., Gao R., Tong J., Yang Z. Transferring [NiFe]-hydrogenase gene from Rhodopeseudomonas palustris into E. coli BL21(DE3) for improving hydrogen production // International Journal of Hydrogen Energy. 2015; 40:4329-36. https://doi.org/10.1016/j.ijhydene.2015.01.171.
211. . Son Y. -S., Jeon J. -M., Kim D. -H., Yang Y. -H., Jin Y. -S., Cho B. -K. et al. Improved bio-hydrogen production by overexpression of glucose-6-phosphate dehydrogenase and [FeFe]-hydrogenase in Clostridium acetobutylicum // International Journal of Hydrogen Energy. 2021; 46:36687-95. https://doi.org/10.1016/j.ijhydene.2021.08.222.
212. . Kundu A., Sahu J. N., Redzwan G., Hashim M. A. An overview of cathode material and catalysts suitable for generating hydrogen in microbial electrolysis cell // International Journal of Hydrogen Energy. 2013; 38:174557. https://doi.org/10.1016/j.ijhydene.2012.11.031.
213. . Rosenbaum M., Aulenta F., Villano M., Angenent L. T. Cathodes as electron donors for microbial metabolism: Which extracellular electron transfer mechanisms are involved? // Bioresour Technol. 2011; 102:32433. https://doi.org/10.1016/j.biortech.2010.07.008.
214. . Kadier A., Kalil M. S., Abdeshahian P., Chandrasekhar K., Mohamed A., Azman N. F. et al. Recent advances and emerging challenges in microbial electrolysis cells (MECs) for microbial production of hydrogen and value-added chemicals // Renew Sustain Energy Rev. 2016; 61:501-25. https://doi.org/10.1016/j.rser.2016.04.017.
215. . Batlle-Vilanova P., Puig S., Gonzalez-Olmos R., Vilajeliu-Pons A., Bañeras L., Balaguer M. D. et al. Assessment of biotic and abiotic graphite cathodes for hydrogen production in microbial electrolysis cells // International Journal of Hydrogen Energy. 2014; 39:1297-305. https://doi.org/10.1016/j.ijhydene.2013.11.017.
216. . Yan X., Bu J., Chen X., Zhu M. -J. Comparative genomic analysis reveals electron transfer pathways of Thermoanaerobacterium thermosaccharolyticum: Insights into thermophilic electroactive bacteria // Sci Total Environ. 2023; 905:167294. https://doi.org/10.1016/j.scitotenv.2023.167294.
217. . Singh N. K., Singh R. Co-factors applicability in hydrogen production from rice straw hydrolysate in a bioelectrochemical system // Energy. 2022; 255:124554. https://doi.org/10.1016/j.energy.2022.124554.
218. . Noori M. T., Rossi R., Logan B. E., Min B. Hydrogen production in microbial electrolysis cells with biocathodes // Trends Biotechnol. 2024; 42:815-28. https://doi.org/10.1016/j.tibtech.2023.12.010.
219. . Villano M., De Bonis L., Rossetti S., Aulenta F., Majone M. Bioelectrochemical hydrogen production with hydrogenophilic dechlorinating bacteria as electrocatalytic agents // Bioresour Technol. 2011; 102:3193-9. https://doi.org/10.1016/j.biortech.2010.10.146.
220. . Singh N. K., Singh R. A sequential approach to uncapping of theoretical hydrogen production in a sulfate-reducing bacteria-based bio-electrochemical system // International Journal of Hydrogen Energy. 2021; 46:20397-412. https://doi.org/10.1016/j.ijhydene.2021.03.152.
221. . Valente F. M. A., Oliveira A. S. F., Gnadt N., Pacheco I., Coelho A. V., Xavier A. V. et al. Hydrogenases in Desulfovibrio vulgaris Hildenborough: structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase // J Biol Inorg Chem. 2005; 10:667-82. https://doi.org/10.1007/s00775-005-0022-4.
222. . Parkin A., Cavazza C., Fontecilla-Camps J. C., Armstrong F. A. Electrochemical Investigations of the Interconversions between Catalytic and Inhibited States of the [FeFe]-Hydrogenase from Desulfovibrio desulfuricans // J Am Chem Soc. 2006; 128:16808-15. https://doi.org/10.1021/ja064425i.
223. . Marques M. C., Coelho R., De Lacey A. L., Pereira I. A. C., Matias P. M. The Three-Dimensional Structure of [NiFeSe] Hydrogenase from Desulfovibrio vulgaris Hildenborough: A Hydrogenase without a Bridging Ligand in the Active Site in Its Oxidised, “as-Isolated” State // J Mol Biol. 2010; 396:893-907. https://doi.org/10.1016/j.jmb.2009.12.013.
224. . Lim S. S., Kim B. H., Li D., Feng Y., Daud W. R. W., Scott K. et al. Effects of Applied Potential and Reactants to Hydrogen-Producing Biocathode in a Microbial Electrolysis Cell // Front Chem. 2018; 6:318. https://doi.org/10.3389/fchem.2018.00318.
225. . Singh N. K., Kumari P., Singh R. Intensified hydrogen yield using hydrogenase rich sulfate-reducing bacteria in bio-electrochemical system // Energy. 2021; 219:119583. https://doi.org/10.1016/j.energy.2020.119583.
226. . Andronikou M., Christoforou P., Constantinou D., Charalambous P. G., Samanides C., Karachaliou P. et al. Critical role of bicarbonate in Zero-Valent iron for hydrogen generation and biogas upgrading in anaerobic digestion // Bioresour Technol. 2025; 426:132236. https://doi.org/10.1016/j.biortech.2025.132236.
227. . Bora A., Mohanrasu K., Angelin Swetha T., Ananthi V., Sindhu R., Chi N. T. L. et al. Microbial electrolysis cell (MEC): Reactor configurations, recent advances and strategies in biohydrogen production // Fuel 2022; 328:125269. https://doi.org/10.1016/j.fuel.2022.125269.
228. . Guo X., Liu J., Xiao B. Bioelectrochemical enhancement of hydrogen and methane production from the anaerobic digestion of sewage sludge in single-chamber membrane-free microbial electrolysis cells // International Journal of Hydrogen Energy. 2013; 38:1342-7. https://doi.org/10.1016/j.ijhydene.2012.11.087.
229. . Tartakovsky B., Mehta P., Santoyo G., Guiot S. R. Maximizing hydrogen production in a microbial electrolysis cell by real-time optimization of applied voltage // International Journal of Hydrogen Energy. 2011; 36:10557-64. https://doi.org/10.1016/j.ijhydene.2011.05.162.
230. . Ketep S. F., Bergel A., Calmet A., Erable B. Stainless steel foam increases the current produced by microbial bioanodes in bioelectrochemical systems // Energy Environ Sci. 2014; 7:1633-7. https://doi.org/10.1039/C3EE44114H.
231. . Baudler A., Schmidt I., Langner M., Greiner A., Schröder U. Does it have to be carbon? Metal anodes in microbial fuel cells and related bioelectrochemical systems // Energy Environ Sci. 2015; 8:2048-55. https://doi.org/10.1039/C5EE00866B.
232. . Sonawane J. M., Yadav A., Ghosh P. C., Adeloju S. B. Recent advances in the development and utilization of modern anode materials for high performance microbial fuel cells // Biosens Bioelectron. 2017; 90:558-76. https://doi.org/10.1016/j.bios.2016.10.014.
233. . Rousseau R., Etcheverry L., Roubaud E., Basséguy R., Délia M. -L., Bergel A. Microbial electrolysis cell (MEC): Strengths, weaknesses and research needs from electrochemical engineering standpoint // Appl Energy. 2020; 257:113938. https://doi.org/10.1016/j.apenergy.2019.113938.
234. . Xie X., Criddle C., Cui Y. Design and fabrication of bioelectrodes for microbial bioelectrochemical systems // Energy Environ Sci. 2015;8:3418-41. https://doi.org/10.1039/C5EE01862E.
235. . Wang Y., Guo W. -Q., Xing D. -F., Chang J. -S., Ren N. -Q. Hydrogen production using biocathode single-chamber microbial electrolysis cells fed by molasses wastewater at low temperature // International Journal of Hydrogen Energy. 2014; 39:19369-75. https://doi.org/10.1016/j.ijhydene.2014.07.071.
236. . Sharma A., Hussain Mehdi S. E., Pandit S., Eun-Oh S., Natarajan V. Factors affecting hydrogen production in microbial electrolysis cell (MEC): A review // International Journal of Hydrogen Energy. 2024; 61:1473-84. https://doi.org/10.1016/j.ijhydene.2024.02.193.
237. . Jafary T., Daud W. R. W., Ghasemi M., Kim B. H., Carmona-Martínez A. A., Bakar M. H. A. et al. A comprehensive study on development of a biocathode for cleaner production of hydrogen in a microbial electrolysis cell // J Cleanr Prod. 2017; 164:1135-44. https://doi.org/10.1016/j.jclepro.2017.07.033.
238. . Rozendal R. A., Jeremiasse A. W., Hamelers H. V. M., Buisman C. J. N. Hydrogen Production with a Microbial Biocathode // Environ Sci Technol. 2008; 42:629-34. https://doi.org/10.1021/es071720+.
239. . Aulenta F., Catapano L., Snip L., Villano M., Majone M. Linking Bacterial Metabolism to Graphite Cathodes: Electrochemical Insights into the H2-Producing Capability of Desulfovibrio sp. // ChemSusChem. 2012; 5:1080-5. https://doi.org/10.1002/cssc.201100720.
240. . Srivastava P., García-Quismondo E., Palma J., González-Fernández C. Coupling dark fermentation and microbial electrolysis cells for higher hydrogen yield: Technological competitiveness and challenges // International Journal of Hydrogen Energy. 2024; 52:223-39. https://doi.org/10.1016/j.ijhydene.2023.04.293.
241. . Ndayisenga F., Yu Z., Zheng J., Wang B., Liang H., Phulpoto I. A. et al. Microbial electrohydrogenesis cell and dark fermentation integrated system enhances biohydrogen production from lignocellulosic agricultural wastes: Substrate pretreatment towards optimization // Renew Sustain Energy Rev. 2021; 145:111078. https://doi.org/10.1016/j.rser.2021.111078.
242. . Wang A., Sun D., Cao G., Wang H., Ren N., Wu W. -M. et al. Integrated hydrogen production process from cellulose by combining dark fermentation, microbial fuel cells, and a microbial electrolysis cell // Bioresour Technol. 2011; 102:4137-43. https://doi.org/10.1016/j.biortech.2010.10.137.
243. . Bundhoo Z. M. A. Coupling dark fermentation with biochemical or bioelectrochemical systems for enhanced bio-energy production: A review // International Journal of Hydrogen Energy. 2017; 42:26667-86. https://doi.org/10.1016/j.ijhydene.2017.09.050.
244. . Sivagurunathan P., Kuppam C., Mudhoo A., Saratale G. D., Kadier A., Zhen G. et al. A comprehensive review on two-stage integrative schemes for the valorization of dark fermentative effluents // Crit Rev Biotechnol. 2018; 38:868-82. https://doi.org/10.1080/07388551.2017.1416578.
245. . Nguyen P. K. T., Das G., Kim J., Yoon H. H. Hydrogen production from macroalgae by simultaneous dark fermentation and microbial electrolysis cell // Bioresour Technol. 2020; 315:123795. https://doi.org/10.1016/j.biortech.2020.123795.
246. . Phan T. P., Ta Q. T. H., Nguyen P. K. T. Maximizing performance of microbial electrolysis cell fed with dark fermentation effluent from water hyacinth // International Journal of Hydrogen Energy. 2023; 48:5447-62. https://doi.org/10.1016/j.ijhydene.2022.11.155.
247. . Li H., Cheng J., Xia R., Dong H., Zhou J. Electron syntrophy between mixed hydrogenogens and Geobacter metallireducens boosted dark hydrogen fermentation: Clarifying roles of electroactive extracellular polymeric substances // Bioresour Technol. 2024; 395:130350. https://doi.org/10.1016/j.biortech.2024.130350.
248. . Lacasse M. J., Douglas C. D., Zamble D. B. Mechanism of Selective Nickel Transfer from HypB to HypA, Escherichia coli [NiFe]-Hydrogenase Accessory Proteins // Biochemistry. 2016; 55:6821-31. https://doi.org/10.1021/acs.biochem.6b00706.
249. . Douglas C. D., Ngu T. T., Kaluarachchi H., Zamble D. B. Metal Transfer within the Escherichia coli HypB-HypA Complex of Hydrogenase Accessory Proteins // Biochemistry. 2013; 52:6030-9. https://doi.org/10.1021/bi400812r.
250. . Wang X., Chen Y. -P., Guo J. -S., Fang F., Yan P. Flocculation-enhanced photobiological hydrogen production by microalgae: Flocculant composition, hydrogenase activity and response mechanism // Chem Eng J. 2024; 485:150065. https://doi.org/10.1016/j.cej.2024.150065.
251. . Ren Y., Xing X. H., Zhang C., Gou Z. A simplified method for assay of hydrogenase activities of H2 evolution and uptake in Enterobacter aerogenes // Biotechnol Lett. 2005; 27:1029-33. https://doi.org/10.1007/s10529-005-8106-3.
252. . Huang Z., Yu X., Miao H., Ren H., Zhao M., Ruan W. Enzymatic dynamics of microbial acid tolerance response (ATR) during the enhanced biohydrogen production process via anaerobic digestion // International Journal of Hydrogen Energy. 2012; 37:10655-62. https://doi.org/10.1016/j.ijhydene.2012.04.116.
253. . Armstrong F. A. Dynamic electrochemical experiments on hydrogenases // Photosynth Res. 2009; 102:541-50. https://doi.org/10.1007/s11120-009-9428-0.
254. . Wan L., Gao Y., DeBeer S., Rüdiger O. The unusual formaldehyde-induced activation of [NiFe]-hydrogenase: Implications from protein film electrochemistry and infrared spectroscopy // Bioelectrochemistry. 2025; 165:108974. https://doi.org/10.1016/j.bioelechem.2025.108974.
255. . Armstrong F. A., Belsey N. A., Cracknell J. A., Goldet G., Parkin A., Reisner E. et al. Dynamic electrochemical investigations of hydrogen oxidation and production by enzymes and implications for future technology // Chem Soc Rev. 2009; 38:36-51. https://doi.org/10.1039/B801144N.
256. . Armstrong F. A., Evans R. M., Megarity C. F. Protein Film Electrochemistry of Iron-Sulfur Enzymes. Methods in Enzymology, vol. 599, Elsevier; 2018, pр. 387-407. https://doi.org/10.1016/bs.mie.2017.11.001.
257. . Pandey K., Islam S. T. A., Happe T., Armstrong F. A. Frequency and potential dependence of reversible electrocatalytic hydrogen interconversion by [FeFe]-hydrogenases // Proc Natl Acad Sci USA. 2017; 114:3843-8. https://doi.org/10.1073/pnas.1619961114.
258. . Zhao B., Wang S., Dong Z., Cao S., Yuan A., Sha H. et al. Enhancing dark fermentative hydrogen production from wheat straw through synergistic effects of active electric fields and enzymatic hydrolysis pretreatment // Bioresour Technol. 2024; 406:130993. https://doi.org/10.1016/j.biortech.2024.130993.
259. . Tian W., Tang Y., Ducey T. F., Khan E., Tsang D. C. W. Facilitating Intracellular Electron Bifurcation by Mediating Flavin-Based Extracellular and Transmembrane Electron Transfer: A Novel Role of Pyrogenic Carbon in Dark Fermentation for Hydrogen Production // Environ Sci Technol. 2024; 58:17766-76. https://doi.org/10.1021/acs.est.4c05994.
260. . Blackburn J. L., Svedruzic D., McDonald T. J., Kim Y. -H., King P. W., Heben M. J. Raman spectroscopy of charge transfer interactions between single wall carbon nanotubes and [FeFe] hydrogenase // Dalton Trans. 2008: 5454. https://doi.org/10.1039/b806379f.
261. . Horch M., Schoknecht J., Mroginski M. A., Lenz O., Hildebrandt P., Zebger I. Resonance Raman Spectroscopy on [NiFe] Hydrogenase Provides Structural Insights into Catalytic Intermediates and Reactions // J Am Chem Soc. 2014; 136:9870-3. https://doi.org/10.1021/ja505119q.
262. . Siebert E., Rippers Y., Frielingsdorf S., Fritsch J., Schmidt A., Kalms J. et al. Resonance Raman Spectroscopic Analysis of the [NiFe] Active Site and the Proximal [4Fe-3S] Cluster of an O2 – Tolerant Membrane-Bound Hydrogenase in the Crystalline State // J Phys Chem B. 2015; 119:13785-96. https://doi.org/10.1021/acs.jpcb.5b04119.
263. . Stromberg C. J., Kohnhorst C. L., Van Meter G. A., Rakowski E. A., Caplins B. C., Gutowski T. A. et al. Terahertz, infrared and Raman vibrational assignments of [FeFe]-hydrogenase model compounds // Vibr Spectrosc. 2011; 56:219-27. https://doi.org/10.1016/j.vibspec.2011.02.012.
264. . Fan Q., Waldburger S., Neubauer P., Riedel S. L., Gimpel M. Implementation of a high cell density fedbatch for heterologous production of active [NiFe]-hydrogenase in Escherichia coli bioreactor cultivations // Microb Cell Fact. 2022; 21:193. https://doi.org/10.1186/s12934-022-01919-w.
265. . Zhang Z., Ni J., Sheng K., Yang K., Gu P., Ren X. et al. Elucidating the effect of H2S on the syngas autotrophic fermentation: Focusing on functional microorganisms and metabolic pathway // Chem Eng J. 2024; 496:153768. https://doi.org/10.1016/j.cej.2024.153768.
266. . Zhao Z. -T., Yang S. -S., Luo G., Sun H. -J., Liu B. -F., Cao G. -L. et al. Biohydrogen fermentation from pretreated biomass in lignocellulose biorefinery: Effects of inhibitory byproducts and recent progress in mitigation strategies // Biotechnol Adv. 2025; 79:108508. https://doi.org/10.1016/j.biotechadv.2024.108508.
267. . Alavi-Borazjani S. A., Capela I., Tarelho L. A. C. Dark fermentative hydrogen production from food waste: Effect of biomass ash supplementation // International Journal of Hydrogen Energy. 2019; 44:26213-25. https://doi.org/10.1016/j.ijhydene.2019.08.091.
268. . Wang Y., Wei W., Dai X., Ni B. -J. Corncob ash boosts fermentative hydrogen production from waste activated sludge // Science of The Total Environment. 2022; 807:151064. https://doi.org/10.1016/j.scitotenv.2021.151064.
269. . Ramprakash B., Incharoensakdi A. Peanut shell activated carbon doped with nickel-iron nanoparticles as material for improving dark fermentative hydrogen production by Enterobacter aerogenes // International Journal of Hydrogen Energy. 2025; 99:579-88. https://doi.org/10.1016/j.ijhydene.2024.12.175.
270. . Zhang Y., Shen J. Effect of temperature and iron concentration on the growth and hydrogen production of mixed bacteria // International Journal of Hydrogen Energy. 2006; 31:441-6. https://doi.org/10.1016/j.ijhydene.2005.05.006.
271. . Saxena S. Strategies of Strain Improvement of Industrial Microbes: Classical and Recombinant DNA Technology in Improving the Characteristics of Industrially Relevant Microbes. Applied Microbiology, New Delhi: Springer India; 2015, pр. 155-71. https://doi.org/10.1007/978-81-322-2259-0_10.
272. . Gadhamshetty V., Arudchelvam Y., Nirmalakhandan N., Johnson D. C. Modeling dark fermentation for biohydrogen production: ADM1-based model vs. Gompertz model // International Journal of Hydrogen Energy. 2010; 35:479-90. https://doi.org/10.1016/j.ijhydene.2009.11.007.
Рецензия
Для цитирования:
Лайкова А.А., Журавлева Е.А., Иваненко А.А., Шехурдина С.В., Ковалев А.А., Ковалев Д.А., Пиллаи С., де Карвалью Х.С., Соккол К.Р., Янь Б., Авасти М.К., Трчунян К., Литти Ю.В. Увеличение светонезависимой выработки биоводорода путем стимуляции активности гидрогеназ: критический обзор. Альтернативная энергетика и экология (ISJAEE). 2025;(11):39-106. https://doi.org/10.15518/isjaee.2025.12.039-106
For citation:
Laikova A.A., Zhuravleva E.A., Ivanenko A.A., Shekhurdina S.V., Kovalev A.A., Kovalev D.A., Pillai S., de Carvalho J.C., Soccol C.R., Yan B., Awasthi M.K., Trchounian K., Litti Yu.V. Enhancement of light-independent biohydrogen production through stimulation of hydrogenase activity: a critical review. Alternative Energy and Ecology (ISJAEE). 2025;(11):39-106. (In Russ.) https://doi.org/10.15518/isjaee.2025.12.039-106
JATS XML































