OUTLOOKS AND CHALLENGES OF HYDROGEN PRODUCTION BY CYANOBACTERIAL ANABAENA SPECIES
DOI:
https://doi.org/10.26577/eb.2022.v92.i3.05Keywords:
Cyanobacteria, Anabaena sp., H2 production, BioenergyAbstract
Uncontrolled use of conventional energy sources in the 21st century has increased the temperature of the Earth's surface by 2ºС in the last 1 century. Due to the increasing negative aspects of traditional energy sources, the production of hydrogen from microorganisms has quickly become an object of intense research. However, due to their low concentration of biomass, commercial production of hydrogen (H2) from microorganisms has not yet been realized. In this context, it is important to identify strains of hydrogen producers – cyanobacteria, which are actively used in biotechnology, and to carry out work on increasing the possibilities of hydrogen separation. This review examines the importance of the cyanobacterium Anabaena in hydrogen production and their hydrogen release mechanisms, and shows the main factors affecting H2 release. Also, recent technologies of hydrogen separation are included, as well as works on increasing the amount of hydrogen under the influence of chemical and physical factors. Due to the low ability of Anabaena strains to catalyze hydrogen molecules at present, future research will be limited to genetic engineering technologies. It is only possible to solve the problems arising in the current biohydrogen industry by conducting genetic, technical and metabolic research in parallel.
References
Spiller H., Ernst A., Kerfin W., Böger P. Increase and stabilization of photoproduction of hydrogen in Nostoc muscorum by photosynthetic electron transport inhibitors // Zeitschrift für Naturforschung. – 1978. – Vol. 33. – P. 541–47.
Burrows E., Chaplen F., Ely R. Effects of selected electron transport chain inhibitors on 24-h hydrogen production by Synechocystis sp. PCC 6803 // Bioresource technology. – 2010. – Vol. 102. – P. 3062–70.
Abdelwahab H.E.M. Hydrogen production in the cyanobacterium Synechocystis sp. PCC 6803 with engineered subunit of the bidirectional H2-ase // Advances in Life Science and Technology. – 2014. – Vol. 18. – P. 7–19.
Sadvakasova A.K., Kossalbayev B.D., Zayadan B.K., Bolatkhan K., Alwasel S., Najafpour M.M., Tatsuya T., Allakhverdiev S.I. Bioprocesses of hydrogen production by cyanobacteria cells and possible ways to increase their productivity // Renewable and Sustainable Energy Reviews. – 2020. – Vol. 133. – P. 110054. https://doi.org/10.1016/j.rser.2020.110054
Tiwari A., Pandey A. Cyanobacterial hydrogen production – a step towards clean environment // Int J Hydrogen Energy. – 2012. – Vol. 37. – P. 139–50.
Kaushik A., Anjana K. Biohydrogen production by Lyngbya perelegans: influence of physic-chemical environment // Biomass Bioenergy. – 2011. – Vol. 35. – P. 1041–5.
Razeghifard R. Algal biofuels // Photosynth Res. – 2013. – Vol. 117. – P. 207–19.
Tamburic B., Zemichael F.W., Maitland G.C., Hellgardt K. Parameters affecting the growth and hydrogen production of the green alga Chlamydomonas reinhardtii // Int J Hydrogen Energy. – 2011. – Vol. 36. – P. 7872–6.
Antal T.K., Krendeleva T.E., Tyystjärvi E. Multiple regulatory mechanisms in the chloroplast of green algae: relation to hydrogen production // Photosynth Res. – 2015. – Vol. 125, No 3. – P. 357–81.
Kosourov S., Tsygankov A., Seibert M., Ghirardi M.L. Sustained hydrogen photoproduction by Chlamydomonas reinhardtii: effects of culture parameters // Biotechnol Bioeng. – 2002. – Vol. 78, No 3. – P. 731–40.
Stebegg R. Heterotrophic Growth of the Cyanobacterium Anabaena (Nostoc) sp. strain PCC7120 and its Dependence on a Functional Cox1 Locus Encoding Cytochrome C Oxidase, Dissertation (Master in Genetics - Microbiology) Universität Wien, Wien, 2011, p. 130.
Yeager C.M., Milliken C.E., Bagwell C.E., Staples L., Berseth P.A., Sessions H.T. Evaluation of experimental conditions that influence hydrogen production among heterocystous cyanobacteria // Int J Hydrogen Energy. – 2011. – Vol. 36. – P. 7487–99.
Masukawa H., Nakamura K., Mochimaru M., Sakurai H. Photobiological hydrogen production and nitrogenase activity in some heterocystous cyanobacteria. In: Miyake J., Matsunaga T., San Pietro A., BioHydrogen II. – United Kingdom: Elsevier 2001. – P. 63–6.
Allahverdiyeva Y., Leino H., Saari L., Fewer D.P., Shunmugam S., Sivonen K., et al. Screening for biohydrogen production by cyanobacteria isolated from the Baltic Sea and Finnish lakes // Int J Hydrogen Energy. – 2010. – Vol. 35. – P. 1117–27.
Berberoglu H., Jay .J, Pilon L. Effect of nutrient media on photobiological hydrogen production by Anabaena variabilis ATCC 29413 // Int J Hydrogen Energy. – 2008. – Vol. 33. – P. 1172–84.
Sveshnikov D.A., Sveshnikova N.V., Rao K.K., Hall D.O. Hydrogen metabolism of mutant forms of Anabaena variabilis in continuous cultures and under nutritional stress // FEBS Microbiol Lett. – 1997. – Vol. 147. – P. 297–301.
Vyas D., Kumar H.D. Nitrogen fixation and hydrogen uptake in four cyanobacteria // Int J Hydrogen Energy. – 1995. – Vol. 20, No 2. – P. 163–8.
Tsygankov A., Serebryakova L., Rao K., Hall D. Acetylene reduction and hydrogen photoproduction by wild-type and mutant strains of Anabaena at different CO2 and O2 concentrations // FEMS Microbiol Lett. – 1998. – Vol. 167. – P. 13–7.
Markov S.A., Protasov E.S., Bybin V.A., Eivazova E.R., Stom D.I. Using immobilized cyanobacteria and culture medium contaminated with ammonium for H2 production in a hollow-fiber photobioreactor // Int J Hydrogen Energy. – 2015. – Vol. 40. – P. 4752–7.
Benemann J.R. Hydrogen production by microalgae // J Appl Phycol. – 2000. – Vol. 12. – P. 291–300.
Tamagnini P., Troshina O., Oxelfelt F., Salema R., Lindblad P. Hydrogenases in Nostoc sp. strain PCC 73102, a strain lacking a bidirectional enzyme // Appl Environ Microbiol. – 1997;63. – P. 1801–7.
Bergman B., Gallon J.R., Rai A.N., Stal L.J. N2 fixation by non-heterocystous cyanobacteria // FEMS Microbiol Rev. – 1997. – Vol. 19. – P. 139–85.
Herrero A., Muro-Pastor A.M., Flores E. Nitrogen control in cyanobacteria // J. Bacteriol – 2001. – Vol. 183. – P. 411–25.
Borodin V.B., Tsygankov A., Rao K.K., Hall D.O. Hydrogen production by Anabaena variabilis PK84 under simulated outdoor conditions // Biotechnol. Bioeng. – 2000. – Vol. 69:479–85.
Benemann J.R., Weare N.M. Hydrogen evolution by nitrogen fixing Anabaena cylindrica cultures // Science. – 1974. – Vol. 184. – P. 174.
Kufryk G. Advances in utilizing cyanobacteria for hydrogen production // Advances in Microbiology – 2013. – Vol. 3. – P. 60–8.
Manis S., Banerjee R. Comparison of biohydrogen production processes // Int. J. Hydrogen Energy. – 2008. – Vol. 33. – P. 279–86.
Hankamer B., Lehr F., Rupprecht J., Mussgnug J., Posten C., Kruse O. Photosynthetic biomass and H2 production by bioengineering to green algae: from bioreactor scale-up // Physiol Plantarum. – 2007. – Vol. 131. – P. 10–21.
Zhang X.K., Haskell J.B., Tabita F.R., Van B.C. Aerobic hydrogen production by the heterocystous cyanobacteria Anabaena spp. strains CA and 1F // J Bacteriol. – 1983. – Vol. 156. – P. 1118–22.
Horiuchi J., Kikuchi S., Kobayashi M., Kanno T, Shimizu T. Modeling of pH response in continuous anaerobic acidogenesis by an artificial neural network // Biochem Eng J. – 2001. – Vol. 9. – P. 199–204.
Show K.-Y., Lee D.-J., Chang J.-S. Bioreactor and process design for biohydrogen production // Bioresour Technol. – 2011. – Vol. 102. – P. 8524–33. https://doi.org/10.1016/j.biortech.2011.04.055
Yu J., Takahashi H. Biophotolysis-Based Hydrogen Productionby Cyanobacteria and Green Microalgae. In: A. Méndez-Vilas, Ed., Communicating Current Research and Educational Topics and Trends in Applied Microbiology // Formatex. – 2007. – Vol. 1. – P. 79–89.
Kossalbayev B.D., Tomo T., Zayadan B.K., Sadvakasova A.K., Bolatkhan K., Alwasel S., Allakhverdiev S.I. Determination of the potential of cyanobacterial strains for hydrogen production // International Journal of Hydrogen Energy. – 2020. – Vol. 45, No 4. – P. 2627–39. https://doi.org/10.1016/j.ijhydene.2019.11.164
Masirbaeva A.D., Baidyldaeva Z.A., Sadanov A.K., Baigonusova Z.A., Ultanbekova G.D. Study of nitrogen-fixing activity and competitive ability of nodule bacteria of the genus Rhizobium // Biological and medical series. – 2014. – Vol. 2. – P. 3252–62.
Uma L., Subramanian G. Effective use of cyanobacteria in effluent treatment.In proceedings of the national symposium on cyanobacterial N2 fixation. New Delhi: IARI, 1990. 437–44.
Zhakeeva M.B., Bekenova U.S., Zhumadilova Z.S., Shorabaev E.Z., Sadanov A.K. Study of ecological and trophic groups of soil microorganisms under alfalfa and soybeans using biological products of the Rizovit-AKS series // Success of modern natural science. – 2015. – Vol. 2. – P. 144–7.
Weissman J.C., Benemann J.R. Hydrogen production by nitrogen-starved cultures of Anabaena cylindrica // Appl Environ Microbiol. – 1977. – Vol. 33. – P. 123–31.
Benemann J.R., Miyamoto K., Hallenbeck P.C. Bioengineering aspects of biophotolysis // Enzyme Microbiol Technol. – 1980. – Vol. 2. – P. 103.
Bolatkhan K., Kossalbayev B.D., Zayadan B.K., Tomo T., Veziroglu V.T., Allakhverdiev S.I. Hydrogen production from phototrophic microorganisms: Reality and perspectives // International Journal of Hydrogen Energy. – 2019. – Vol. 44, No 12. – P. 5799–811. https://doi.org/10.1016/j.ijhydene.2019.01.092
Sundararaman M., Subramanian G., Averal H.I., Akbharsha M.A. Evaluation of the bioactivity of marine cyanobacteria on some biochemical parameters of rat serum // Phytotherapy Res. – 1996. – Vol. 10. – P. 9–12.
Kaushik B.D., Venkataraman G.S. Effect of algal inoculation on the yield and vitamin C content of two varieties of tomato // Plant Soil. – 1979. – Vol. 52. – P. 135–7.
Choudhary K.K. Occurrence of nitrogen fixing cyanobacteria during different stages of paddy cultivation // Bangladesh J Plant Taxon. – 2011. – Vol. 18. – P. 73–6.
Choudhury A.T.M.A., Kennedy I.R. Prospects and potentials for systems of biological nitrogen fixation in sustainable rice production // Biol Fertil Soils. – 2004. – Vol. 39. – P. 219–27.
Dey H.S., Bastia A.K. Cyanobacterial flora from rice growing areas of Mayurbhanj // Plant Sc Res. – 2008. – Vol. 30. – P. 22–6.
Khetkorn W., Rastogi R.P., Incharoensakdi A., Lindblad P., Datta M., Pandey A., Larroche C. Microalgal hydrogen production – A review // Bioresource Technology. – 2017. – Vol. 243. – P. 1194–206.
Gaffron H., Rubin J. Fermentative and photochemical production of hydrogen in algae // J Gen Physiol. – 1942. – Vol. 26, No 2. – P. 219–40.
Dutta D., Debojyoti D., Chaudhuri S, Bhattacharya S. Hydrogen production by cyanobacteria // Microbial cell factories. – 2005. – Vol. 4. – P. 36.
Melis A., Melnicki M.R. Integrated biological hydrogen production // Int J Hydrogen Energy. – 2006. – Vol. 31. – P. 1563–73.
Momirlan M., Veziroglu T.N. The properties of hydrogen as fuel tomorrow in sustainable energy system for a cleaner // Int J Hydrogen Energy. – 2005. – Vol. 30. – P. 681–8.
Mathews J, Wang G. Metabolic pathway engineering for enhanced biohydrogen production // Int J Hydrogen Energy. – 2009. – Vol. 34. – P. 7404–16.
Das D., Veziroglu T.N. Advances in biological hydrogen production processes // Int J Hydrogen Energy. – 2008. – Vol. 33. – P. 6046–57.
Fani R., Gallo R., Liò P. Molecular evolution of nitrogen fixation: The evolutionary history of the nifD, nifK, nifE, and nifN genes // J Mol Evol. – 2000. – Vol. 51. – P. 1–11.
Miller R.W., Eady R.R. Molybdenum and vanadium nitrogenases of Azotobacter chroococcum. Low temperature favours N2 reduction by vanadium nitrogenase // Biochem J. – 1988. – Vol. 256. – P. 429–32.
Valladares A., Muro-Pastor A.M., Fillat M.F., Herrero A., Flores E. Constitutive and nitrogen-regulated promoters of the petH gene encoding ferredoxin: NADP+ reductase in the heterocyst-forming cyanobacterium Anabaena sp. // FEBS Lett. – 1999. – Vol. 449. – P. 159–64.
Hallenbeck P.C. Hydrogen Production by Cyanobacteria. In book: Microbial Technologies in Advanced Biofuels Production Publisher: Springer US, 2011.P.15–28.
Alberto A.E.F., Henrique C.J., Marcelo V., Alvarenga V., Nunes-Adriano N., Wagner A. Cyanobacterial nitrogenases: Phylogenetic diversity, regulation and functional predictions // Genetics and Molecular Biology. – 2017. – Vol. 40. – P. 261–75.
Suzuki I., Horie N., Sugiyama T., Omata T. Identification and characterization of two nitrogen-regulated genes of the cyanobacterium Synechococcus sp. strain PCC7942 required for maximum efficiency of nitrogen assimilation // J Bacteriol. – 1995. – Vol. 177. – P. 290–6.
Bergman M., Perewoska I., Kirilovsky D. Redox control of ntcA gene expression in Synechocystis sp. PCC 6803 // Plant Physiol. – 2001. – Vol. 125. – P. 969–81.
Thiel T., Lyons E.M., Erker J.C. Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis // J. Bacteriol. – 1997. – Vol. 179. – P. 5222–5.
Kentemich T., Danneberg G., Hundeshagen B., Bothe H. Evidence for the occurrence of the alternative, vanadium-containing nitrogenase in the cyanobacterium Anabaena variabilis // FEMS Microbiol Lett. – 1988. – Vol. 51. – P. 19–24.
Gudrun B., Caroline S., Lucas S., Hermann B. The rice field cyanobacteria Anabaena azotica and Anabaena sp. CH1 express vanadium-dependent nitrogenase // Archives of microbiology. – 2006. – Vol. 186. – P. 367–76.
Thiel T. Isolation and characterization of the vnfEN genes of the cyanobacterium Anabaena variabilis // J Bacteriol. – 1996. – Vol. 178. – P. 4493–9.
Paulette V. Hydrogenases and H+– reduction in primary energy conservation // Results and problems in cell differentiation. – 2008. – Vol. 45. – P. 223–52.
Tamagnini P., Leitao E., Oliveira P., Ferreira D., Pinto F., Harris D.J., Heidorn T., Lindblad P. Cyanobacterial hydrogenases: diversity, regulation and applications // FEMS Microbiology Reviews. – 2007. – Vol. 31. – P. 692–720.
Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P. Hydrogenases and hydrogen metabolism of cyanobacteria // Microbiology and molecular biology reviews: MMBR. – 2002. – Vol. 66. – P. 1–20.
Smith G.D., Ewart G.D., Tucker W. Hydrogen production by cyanobacteria // Int J Hydrogen Energy. – 1992. – Vol. 17. – P. 695–8.
Boison G., Schmitz O., Mikheeva L., Shestakov S., Bothe H. Cloning, molecular analysis and insertional mutagenesis of the bidirectional hydrogenase genes from the cyanobacterium Anacystis nidulans // FEBS Lett. – 1996. – Vol. 394. – P. 153–8.
Boison G., Bothe H., Schmitz O. Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulan sand Anabaena variabilis monitored by RT-PCR // Curr Microbiol. – 2000. – Vol. 40. – P. 315–21.
Sheremetieva M.E., Troshina O.Y., Serebryakova L.T., Lindblad P. Identification of hox genes and analysis of their transcription in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 growing under nitrate-limiting conditions // FEMS Microbiol Lett. – 2002. – Vol. 214. – P. 229–33.
Houchins J.P. The physiology and biochemistry of hydrogen metabolism in cyanobacteria // Biochim Biophys Acta. – 1984. – Vol. 768. – P. 227–55.
Schmitz O., Boison G., Salzmann H., Bothe H., Schutz K., Wang S.H., Happe T. HoxE – a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria // Biochim Biophys Acta. – 2002. – Vol. 1554. – P. 66–74.
Oxelfelt F., Tamagnini P., Lindblad P. Hydrogen uptake in Nostoc sp. strain PCC 73102 cloning and characterization of a hupSL homologue // Arch Microbiol. – 1998. – Vol. 169. – P. 267–74.
Weyman P., Brenda P., Thiel T. Transcription of hupSL in Anabaena variabilis ATCC 29413 is regulated by NtcA and not by hydrogen // Applied and environmental microbiology. – 2008. – Vol. 74. – P. 2103–10.
Carrasco C.D., Buettner J.A., Golden J.W. Programed DNA rearrangment of a cyanobacterial hupL gene in heterocysts // Proc Natl Acad Sci. – 1995. – Vol. 92. – P. 791–5.
Tsygankov A.A. Nitrogen-fixing cyanobacteria: producents of hydrogen // Prikladnaia Biokhimiia I Mikrobiologiia. – 2007. – Vol. 43, No 3. – P. 279–88.
Carrasco C.D., Garcia J.S., Golden J.W. Programmed DNA rearrangement of a hydrogenase gene during Anabaena heterocyst development // BioHydrogen. – 1998. – Vol. – P. 203–7.
Gutthann F., Egert M., Marques A., Appel J. Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803 // Biochim. Biophys. Acta-Bioenergetics. – 2007. – Vol. 1767. – P. 161–9.
Batyrova K., Hallenbeck P. Hydrogen production by a Chlamydomonas reinhardtii strain with inducible expression of photosystem II // International Journal of Molecular Sciences. – 2017. – Vol. 18. – P. 647.
Komenda J. Photosystem 2 photoinactivation and repair in the Scenedesmus cells treated with herbicides DCMU and BNT and exposed to high irradiance // Photosynthetica. – 1998. – Vol. 35. – P. 477–80.
Cournac L., Guedeney G., Peltier G., Vignais P.M. Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex // J. Bacteriol. – 2004. – Vol. 186. – P. 1737–46.
Torimura M., Miki A., Wadano A., Kano K., Ikeda T. Electrochemical investigation of cyanobacteria Synechococcus sp. PCC7942-catalyzed photoreduction of exogenous quinones and photoelectrochemical oxidation of water // Journal of Electroanalytical Chemistry. – 2001. – Vol. 496. – P. 21–8.
Pisciotta J.M., Zou Y., Baskakov I.V. Light-dependent electrogenic activity of cyanobacteria // PLoS ONE. – 2010. – Vol. 5. – P. e10821.
Imafuku H., Katoh T. Intracellular ATP level and light-induced inhibition of respiration in a blue-green alga, Anabaena variabilis // Plant & Cell Physiology. – 1976. – Vol. 17. – P. 515–24.
Berg S.P., Krogmann D.W. Mechanism of KCN inhibition of photosystem I // J. Biol. Chem. – 1975. – Vol. 250. – P. 8957–62.
Hihara Y., Sonoike K., Kanehisa M., Ikeuchi M. DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803 // Journal of bacteriology. – 2003. – Vol. 185. – P. 1719–25.
Boris V., Trubitsin V.V., Ptushenko O.A., Koksharova M.D., Mamedov L.A., Vitukhnovskaya I.A., Grigorev A.Y., Semenov A.N., Tikhonov E.P.R. Study of electron transport in the cyanobacterium Synechocystis sp. PCC 6803: Oxygen-dependent interrelations between photosynthetic and respiratory electron transport chains // Biochimica et Biophysica Acta – Bioenergetics. – 2005. – Vol. 1708. – P. 238–49.
Carrieri D., Wawrousek K., Eckert C., Yu I., Maness P.-J. The role of bidirectional hydrogenases in cyanobacteria // Bioresour. Technol. – 2011. – Vol. 102. – P. 8368–77.
Alalayah W.M., Alhamed Y.A., Al-zahrani A., Edris G. Influence of culture parameters on biological hydrogen production using green algae Chlorella vulgaris // Rev Chim. – 2015. – Vol. 66. – P. 788–91.
Song W., Rashid N., Choi W., Lee K. Biohydrogen production by immobilized Chlorella sp. using cycles of oxygenic photosynthesis and anaerobiosis // Bioresour Technol. – 2011. – Vol. 102. – P. 8676–81. https://doi.org/10.1016/j.biortech.2011.02.082.
Melis A. Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production // Energy Environ Sci. – 2012. – Vol. 5. – P. 5531–9. https://doi.org/10.1039/C1EE02514G.
Mizuno Y., Sato A., Watanabe K., Hirata A., Takeshita T., Ota S. Sequential accumulation of starch and lipid induced by sulfur deficiency in Chlorella and Parachlorella species // Bioresour Technol. – 2013. – Vol. 129. – P. 150–5. https://doi.org/10.1016/j.biortech.2012.11.030.
Axelsson R, Lindblad P. Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel // Appl. Environ. Microbiol. – 2002. – Vol. 68. – P. 444–7.
Rashid N., Lee K., Han J.I., Gross M. Hydrogen production by immobilized Chlorella vulgaris: optimizing pH, carbon source and light // Bioproc Biosyst Eng. – 2013. – Vol. 36. – P. 867–72. https://doi.org/10.1007/s00449-012-0819-9.
Liu J.-Z., Ge Y.-M., Xia S.-Y., Sun J.-Y., Mu J. Photoautotrophic hydrogen production by Chlorella pyrenoidosa without sulfur-deprivation // Int J Hydrogen Energy. – 2016. – Vol. 41. – P. 8427–32. https://doi.org/10.1016/j.ijhydene.2016.03.191
Boboescu I.Z., Gherman V.D., Lakatos G., Pap B., BıroT., Maroti G. Surpassing the current limitations of biohydrogen production systems: the case for a novel hybrid approach // Bioresour Technol. – 2016. – Vol. 204. – P. 192–201. https://doi.org/10.1016/j.biortech.2015.12.083.
Lopez-Hidalgo A.M., Alvarado-Cuevas Z.D., De LeonRodriguez A. Biohydrogen production from mixtures of agro-industrial wastes: chemometric analysis, optimization and scaling up // Energy. – 2018. – Vol. 159. – P. 32–41. https://doi.org/10.1016/j.energy.2018.06.124.
Ramchandran S., Mitsui A. Recycling of hydrogen photoproduction system using an immobilized marine blue green algae Oscillatoria sp. Miami BG7, solar energy and seawater [abstract] // VII International Biotechnology Symposium. 1984. pp. 183–4.
Moezelaar R., Bijvank S.M., Stal L.J. Fermentation and Sulfur Reduction in the Mat-Building Cyanobacterium Microcoleus chthonoplastes // Appl Environ Microbiol. – 1996. – Vol. 62, No 5. – P. 1752–8.
Datta M., Nikki G., Shah V. Cyanobacterial hydrogen production // World J Microbiol Biotechnol – 2000. – Vol. 16. – P. 8–9.
Aoyama K., Uemura I., Miyake J., Asada Y. Fermentative metabolism to produce hydrogen gas and organic compounds in a cyanobacterium, Spirulina platensis // J Ferment Bioeng. – 1997. – Vol. 83. – P. 17–20.
Zayadan B.K., Kossalbayev B.D., Tomo T., Allakhverdiev S.I., Sadvakasova A.K., Bolatkhan K., Kakimova А. Study of promising heterocystic cyanobacterial strains for biohydrogen production // series of biological and medical. – 2020. – Vol. 3, No 339. – P. 41–8.
Lambert G.R., Daday A., Smith G.D. Hydrogen evolution from immobilized cultures of the cyanobacterium Anabaena cylindrica B629 // FEBS Lett. – 1979. – Vol. 101, No 1. – P. 125–8.
Radway J.C., Yozua B.A., Benemann J.R., Chini Zitelli G., Malda J., Babcock R.W., Jr, Tredici M.R. Evaluation of a near-horizontal tubular photobioreactor system in Hawaii [abstracts] 8th International Conference on Applied Algology: Montecassini, Italy. 1999.
Vargas S.R., Santos P.V., Zaiat M., Calijuri M.C. Optimization of biomass and hydrogen production by Anabaena sp. (UTEX 1448) in nitrogen-deprived cultures // Biomass and Bioenergy. – 2018. – Vol. 111. – P. 70–6.
Cassier-Chauvat C., Veaudor T., Chauvat F. Advances in the function and regulation of hydrogenase in the cyanobacterium Synechocystis PCC6803 // Int. J. Mol. Sci. – 2014. – Vol. 15. – P. 19938–51.
Nyberg M., Heidorn T., Lindblad P. Hydrogen production by the engineered cyanobacterial strain Nostoc PCC 7120 ΔhupW examined in a flat panel photobioreactor system // Journal of Biotechnology. – 2015. – Vol. 215. – P. 35–43.
Jeffries T.W., Timourian T.H., Ward R.L. Hydrogen Production by Anabaena cylindrica: Effects of Varying Ammonium and Ferric Ions, pH, and Light // Applied and environmental microbiology. – 1978. – Vol. 1 – P. 704–10.
Tsygankov A.A., Borodin V.B., Rao K.K., Hall D.O. H2 photoproduction by batch culture of Anabaena variabilis ATCC 29413 and its mutant PK84 in a photobioreactor // Biotechnol Bioeng. – 1999. – Vol. 64, No 6. – P. P. 709-15.
Shah V., Garg N., Madamwar D. Ultrastructure of the cyanobacterium Nostoc muscorum and exploitation of the culture for hydrogen production // Folia Microbiol (Praha). – 2003. – Vol. 48(1). – P. 65-70.
Hallenbeck P.C., Kochian L.V., Weissmann J.C., Benemann J.R. Solar energy conversion with Hydrogen producing cultures of the blue green alga, Anabaena cylindrica // Biotechnology and Bioengineering Symposium. – 1978. – Vol. 8. – P. 283–97.
Bakonyi P., Kumar G., Belafi-Bak o K., Kim S.-H., Koter S., Kujawski W., et al. A review of the innovative gas separation membrane bioreactor with mechanisms for integrated production and purification of biohydrogen // Bioresour Technol. – 2018. https://doi.org/10.1016/j.biortech.2018.09.020.
Rashid N., Lee K., Han J.I,. Gross M. Hydrogen production by immobilized Chlorella vulgaris: optimizing pH, carbon source and light // Bioproc Biosyst Eng. – 2013. – Vol. 36. – P. 867–72. https://doi.org/10.1007/s00449-012-0819-9.
Qiao H., Wang G. Effect of carbon source on growth and lipid accumulation in Chlorella sorokiniana GXNN01 // Chin J Oceanol Limnol. – 2009. – Vol. 27. – P. 762–8. https://doi.org/10.1007/s00343-009-9216-x
Ernst A., Kerfin W., Spiller H., Boger P. External factors influencing light-induced H2 evolution by the blue-green algae, Nostoc muscorum // Zeitschrift fur Naturforschung. – 1979. – Vol. 34. – P. 820–5.
