Please wait a minute...
Journal of Zhejiang University (Science Edition)  2023, Vol. 50 Issue (1): 69-82    DOI: 10.3785/j.issn.1008-9497.2023.01.011
Chemistry     
Progress of photobiological hydrogen production by green algae
Yaqin ZHANG1,2(),Ruikang TANG1,2,Weimin MA3,Wei XIONG4,Xurong XU2()
1.Department of Chemistry,Zhejiang University,Hangzhou 310027,China
2.Qiushi Academy for Advanced Studies,Zhejiang University,Hangzhou 310027,China
3.College of Life Sciences,Shanghai Normal University,Shanghai 200234,China
4.School of Chemistry and Chemical Engineering,Nanchang University,Nanchang 330031,China
Download: HTML( 16 )   PDF(2607KB)
Export: BibTeX | EndNote (RIS)      

Abstract  

Photobiological hydrogen production by green algae exhibits a bright application prospect in solar energy utilization and hydrogen energy production due to the advantages of high energy conversion efficiency, environmental friendliness as well as abundant raw materials. This paper analyzes the potential factors limiting photobiological hydrogen production by green algae based on the mechanism, and summarizes various methods to improve the efficiency of photobiological hydrogen production by green algae. The main problems and development trends in the commercial application of photobiological hydrogen production by green algae are briefly reviewed, which are referable for the large-scale application of photobiological hydrogen production by green algae in the future.



Key wordsgreen algae      photobiological hydrogen      hydrogenase      O2 sensitivity      electronic sources     
Received: 30 March 2022      Published: 13 January 2023
CLC:  Q 949  
Corresponding Authors: Xurong XU     E-mail: 11837050@zju.edu.cn;xrxu@zju.edu.cn
Cite this article:

Yaqin ZHANG,Ruikang TANG,Weimin MA,Wei XIONG,Xurong XU. Progress of photobiological hydrogen production by green algae. Journal of Zhejiang University (Science Edition), 2023, 50(1): 69-82.

URL:

https://www.zjujournals.com/sci/EN/Y2023/V50/I1/69


绿藻光合产氢的研究进展

绿藻光合产氢具有能量转化效率高、环境友好、原料丰富等优势,在太阳能利用和氢能生产方面具有光明的应用前景。从绿藻光合产氢的生物学机理出发,分析了限制绿藻光合产氢的潜在因素,总结了各类提升绿藻光合产氢效率的方法,并简要评述了绿藻光合产氢实现商业化应用所面临的主要问题及发展趋势,为未来绿藻光合产氢的大规模应用提供参考。


关键词: 绿藻,  光合产氢,  氢化酶,  氧敏感性,  电子源 
Fig.1 Schematic representation of the H2 production pathway in green alga12
Fig.2 Model scheme for reaction of CO and O2 with oxidation state of the H-cluster22
产氢方法绿藻种类产氢条件产氢总量/(mL·L-1产氢持续时间/d参考文献
氮气吹扫法C. reinhardtii氮气吹扫,补充二氧化碳<206031
添加除氧剂C. reinhardtii CC50313 mol·L-1 NaHSO3,逐步添加法~112338
C. reinhardtii葡萄糖氧化酶组合、氢氧化镁7782639
藻菌共培养Chlorella sp. MACC 360与大肠杆菌共培养~91140
控制光照法C. reinhardtii CC124脉冲光照条件(1 s光照/9 s黑暗)~732.2541
细胞聚集法ChlorellaPDADMAC诱导矿化17242
代谢调控法Chlorella protothecoidesTAP-S(0.35 mM NH4Cl)2344.1743
Chlorella sorokiniana strain CeTAP-S~1507.3844
基因突变法C. reinhardtii 突变体stm6TAP-S5401445
C. reinhardtii 质子梯度突变体pgr5TAP-S850946
C. reinhardtii D1蛋白突变体L159I-N230YTAP-S5041247
基因改造法C. reinhardtii CC849基因改造hemHc-lbacTAP-S、氮气吹扫82.5548
C. reinhardtii 基因改造hydA-SOD融合酶葡萄糖氧化酶组合1841449
Table 1 Hydrogen production of various methods
Fig.3 Photobiological H2 production with C. pyrenoidosa by construction of a laccase-modulated anaerobic layer60
Fig.4 Schematic of photobiological and fermentative H2 production with the algae-bacteria cocultures (Chlamydomonas and E. coli cocultures)61
Fig.5 Spatial differentiation of chlorella aggregates for hydrogen production42
Fig.6 Schematics of the intracellular processes and pathways that occur under normal, sulfur-replete conditions and during sulfur-deprivation71
Fig.7 Summary of methods to improve photobiological hydrogen productionThe more the number of " + ", the higher the potential of improving hydrogen production efficiency.
[1]   BOGDANOV D, FARFAN J, SADOVSKAIA K, et al. Radical transformation pathway towards sustainable electricity via evolutionary steps[J]. Nature Communications, 2019, 10(1): 1077-1093. DOI:10.1038/s41467-019-08855-1
doi: 10.1038/s41467-019-08855-1
[2]   LEWIS N S. Developing a scalable artificial photosynthesis technology through nanomaterials by design[J]. Nature Nanotechnology, 2016, 11(12): 1010-1019. DOI:10.1038/nnano.2016.194
doi: 10.1038/nnano.2016.194
[3]   WARNAN J, REISNER E. Synthetic organic design for solar fuel systems[J]. Angewandte Chemie International Edition, 2020, 59(40): 17344-17354. DOI:10.1002/anie.202006013
doi: 10.1002/anie.202006013
[4]   GREGORY D P, PANGBORN J B. Hydrogen energy[J]. Annual Review of Energy, 1976, 1: 279-310. DOI:10.1146/annurev.eg.01. 110176.001431
doi: 10.1146/annurev.eg.01. 110176.001431
[5]   RAMACHANDRAN R, MENON R K. An overview of industrial uses of hydrogen[J]. International Journal of Hydrogen Energy, 1998, 23(7): 593-598. DOI:10.1016/S0360-3199(97)00112-2
doi: 10.1016/S0360-3199(97)00112-2
[6]   GUPTA R, JALIL M F. An Overview of Using Hydrogen in Transportation Sector as Fuel[M]. Singapore: Springer, 2021. DOI:10.1007/978-981-33-4080-0_49
doi: 10.1007/978-981-33-4080-0_49
[7]   TURNER J A. A realizable renewable energy future[J]. Science, 1999, 285(5428): 687-689. DOI:10.1126/science.285.5428.687 .
doi: 10.1126/science.285.5428.687
[8]   KORNIENKO N, ZHANG J Z, SAKIMOTO K K, et al. Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis[J]. Nature Nanotechnology, 2018, 13(10): 890-899. DOI:10.1038/s41565-018-0251-7
doi: 10.1038/s41565-018-0251-7
[9]   GAFFRON H, RUBIN J. Fermentative and photochemical production of hydrogen in algae[J]. The Journal of General Physiology, 1942, 26(2): 219-240. DOI:10.1085/jgp.26.2.219
doi: 10.1085/jgp.26.2.219
[10]   MELIS A. Solar energy conversion efficiencies in photosynthesis: Minimizing the chlorophyll antennae to maximize efficiency[J]. Plant Science, 2009, 177(4): 272-280. DOI:10.1016/j.plantsci.2009.06.005
doi: 10.1016/j.plantsci.2009.06.005
[11]   KUVYKIN I V, VERSHUBSKⅡ A V, TIKHONOV A N. Alternative pathways of photoinduced electron transport in chloroplasts[J]. Russian Journal of Physical Chemistry B, 2009, 3(2): 230-241. DOI:10.1134/S1990793109020092
doi: 10.1134/S1990793109020092
[12]   EROGLU E, MELIS A. Microalgal hydrogen production research[J]. International Journal of Hydrogen Energy, 2016, 41(30): 12772-12798. DOI:10.1016/j.ijhydene.2016.05.115
doi: 10.1016/j.ijhydene.2016.05.115
[13]   HEMSCHEMEIER A, HAPPE T. Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii [J]. Biochimica et Biophysica Acta-Bioenergetics, 2011, 1807(8): 919-926. DOI:10. 1016/j.bbabio.2011.02.010
doi: 10. 1016/j.bbabio.2011.02.010
[14]   YANG W J, CATALANOTTI C, WITTKOPP T M, et al. Algae after dark: Mechanisms to cope with anoxic/hypoxic conditions[J]. The Plant Journal, 2015, 82(3): 481-503. DOI:10.1111/tpj.12823
doi: 10.1111/tpj.12823
[15]   BATYROVA K, HALLENBECK P C. Recent Developments in Light‑Driven H2 Production by the Green Alga, Chlamydomonas Reinhardtii [M]. London: Future Science, 2015: 82-95. DOI:10. 4155/fseb2013.14.269
doi: 10. 4155/fseb2013.14.269
[16]   MEUSER J E, ANANYEV G, WITTIG L E, et al. Phenotypic diversity of hydrogen production in chlorophycean algae reflects distinct anaerobic metabolisms[J]. Journal of Biotechnology, 2009, 142(1): 21-30. DOI:10.1016/j.jbiotec.2009.01.015
doi: 10.1016/j.jbiotec.2009.01.015
[17]   FLORIN L, TSOKOGLOU A, HAPPE T. A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain[J]. Journal of Biological Chemistry, 2001, 276(9): 6125-6132. DOI:10.1074/jbc.M008470200
doi: 10.1074/jbc.M008470200
[18]   BRODERICK J B, BYER A S, DUSCHENE K S, et al. H-cluster assembly during maturation of the [FeFe]-hydrogenase[J]. JBIC Journal of Biological Inorganic Chemistry, 2014, 19(6): 747-757. DOI:10.1007/s00775-014-1168-8
doi: 10.1007/s00775-014-1168-8
[19]   PETROVA E V, KUKARSKIKH G P, KRENDELEVA T E, et al. The mechanisms and role of photosynthetic hydrogen production by green microalgae[J]. Microbiology, 2020, 89(3): 251-265. DOI:10.1134/S0026261720030169
doi: 10.1134/S0026261720030169
[20]   GHIRARDI M L, KING P W, POSEWITZ M C, et al. Approaches to developing biological H2-photoproducing organisms and processes[J]. Biochemical Society Transactions, 2005, 33(1): 70-72. DOI:10.1042/BST0330070
doi: 10.1042/BST0330070
[21]   GHIRARDI M L, POSEWITZ M C, MANESS P C, et al. Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms[J]. Annual Review of Plant Biology, 2007, 58(1): 71-91. DOI:10.1146/annurev.arplant.58.032806.103848
doi: 10.1146/annurev.arplant.58.032806.103848
[22]   STRIPP S T, GOLDET G, BRANDMAYR C, et al. How oxygen attacks [FeFe] hydrogenase from photosynthetic organisms[J]. Proceedings of the National Academy of Sciences, 2009, 106(41): 17331-17336. DOI:10.1073/pnas.0905343106
doi: 10.1073/pnas.0905343106
[23]   MEUSER J E, D’ADAMO S, JINKERSON R E, et al. Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: Insight into the role of HYDA2 in H2 production[J]. Biochemical & Biophysical Research Communications, 2012, 417: 704-709. DOI:10.1016/j.bbrc.2011.12.002
doi: 10.1016/j.bbrc.2011.12.002
[24]   APPEL J, SCHULZ R. Hydrogen metabolism in organisms with oxygenic photosynthesis: Hydrogenases as important regulatory devices for a proper redox poising?[J]. Journal of Photochemistry & Photobiology B: Biology, 1998, 47(1): 1-11. DOI:10.1016/S1011-1344(98)00179-1
doi: 10.1016/S1011-1344(98)00179-1
[25]   ROCHAIX J D. REPRINT of: Regulation of photosynthetic electron transport[J]. Biochimica et Biophysica Acta(BBA)-Bioenergetics, 2011, 1807(8): 878-886. DOI:10.1016/j.bbabio.2011.05.009
doi: 10.1016/j.bbabio.2011.05.009
[26]   TOSHIHARU H, PETER S, DAVID B K. The Interaction of ferredoxin with ferredoxin-dependent enzymes[J]. Advances in Photosynthesis & Respiration, 2006, 24: 477-498. DOI:10.1007/978-1-4020-4256-0_28
doi: 10.1007/978-1-4020-4256-0_28
[27]   YACOBY I, POCHEKAILOV S, TOPORIK H, et al. Photosynthetic electron partitioning between [FeFe]- hydrogenase and ferredoxin: NADP+-oxidoreductase (FNR) enzymes in vitro[J]. Proceedings of the National Academy of Sciences, 2011, 108(23): 9396-9401. DOI:10.1073/pnas.1103659108
doi: 10.1073/pnas.1103659108
[28]   GODAUX D, BAILLEUL B, BERNE N, et al. Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-like1-mediated cyclic electron flow in Chlamydomonas reinhardtii [J]. Plant Physiology, 2015, 168(2): 648-658. DOI:10.1104/pp.15.00105
doi: 10.1104/pp.15.00105
[29]   LEE J W, GREENBAUM E, et al. A new oxygen sensitivity and its potential application in photosynthetic H2 production[J]. Applied Biochemistry and Biotechnology, 2003, 4(25): 303-313.
[30]   KOSOUROV S N, BATYROVA K A, PETUSHKOVA E P, et al. Maximizing the hydrogen photoproduction yields in Chlamydomonas reinhardtii cultures: The effect of the H2 partial pressure[J]. International Journal of Hydrogen Energy, 2012, 37(10): 8850-8858. DOI:10.1016/j.ijhydene.2012.01.082
doi: 10.1016/j.ijhydene.2012.01.082
[31]   GREENBAUM E, BLANKINSHIP S L, LEE J W, et al. Solar photobiochemistry: Simultaneous photoproduction of hydrogen and oxygen in a confined bioreactor[J]. The Journal of Physical Chemistry B, 2001, 105(17): 3605-3609. doi:10.1021/jp0042821
doi: 10.1021/jp0042821
[32]   SUBRAMANIAN V, DUBINI A, ASTLING D P, et al. Profiling Chlamydomonas metabolism under dark, anoxic H2-producing conditions using a combined proteomic, transcriptomic, and metabolomic approach[J]. Journal of Proteome Research, 2014, 13(12): 5431-5451. DOI:10.1021/pr500342j
doi: 10.1021/pr500342j
[33]   TSYGANKOV A A, KOSOUROV S N, TOLSTYGINA I V, et al. Hydrogen production by sulfur-deprived Chlamydomonas reinhardtii under photoautotrophic conditions[J]. International Journal of Hydrogen Energy, 2006, 31(11): 1574-1584. DOI:10.1016/j.ijhydene.2006.06.024
doi: 10.1016/j.ijhydene.2006.06.024
[34]   HAHN J J, GHIRARDI M L, JACOBY W A. Effect of process variables on photosynthetic algal hydrogen production[J]. Biotechnology Progress, 2004, 20(3): 989-991. doi:10.1021/bp0341287
doi: 10.1021/bp0341287
[35]   JO J H, LEE D S, PARK J M. Modeling and optimization of photosynthetic hydrogen gas production by green alga Chlamydomonas reinhardtii in sulfur-deprived circumstance[J]. Biotechnol Progress, 2006, 22(2): 431-437. DOI:10.1021/bp050258z
doi: 10.1021/bp050258z
[36]   WEI L Z, YI J, WANG L J, et al. Light intensity is important for hydrogen production in NaHSO3-treated Chlamydomonas reinhardtii [J]. Plant & Cell Physiology, 2017, 58(3): 451-457. DOI:10.1093/pcp/pcw216
doi: 10.1093/pcp/pcw216
[37]   KOSOUROV S, SEIBERT M, GHIRARDI M L. Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures[J]. Plant & Cell Physiology, 2003, 44(2): 146-155. DOI:10.1093/pcp/pcg020
doi: 10.1093/pcp/pcg020
[38]   WEI L Z, LI X, FAN B Q, et al. A stepwise NaHSO3 addition mode greatly improves H2 photoproduction in Chlamydomonas reinhardtii [J]. Frontiers in Plant Science, 2018, 9: 1532-1539. DOI:10.3389/fpls.2018.01532.eCollection2018
doi: 10.3389/fpls.2018.01532.eCollection2018
[39]   CHEN J, LI J, LI Q, et al. Engineering a chemoenzymatic cascade for sustainable photobiological hydrogen production with green algae[J]. Energy & Environmental Science, 2020, 13(7): 2064-2068. DOI:10.1039/d0ee00993h
doi: 10.1039/d0ee00993h
[40]   LAKATOS G, BALOGH D, FARKAS A, et al. Factors influencing algal photobiohydrogen production in algal-bacterial co-cultures[J]. Algal Research, 2017, 28: 161-171. DOI:10.1016/j.algal.2017.10.024
doi: 10.1016/j.algal.2017.10.024
[41]   KOSOUROV S, JOKEL M, ARO E M, et al. A new approach for sustained and efficient H2 photoproduction by Chlamydomonas reinhardtii [J]. Energy & Environmental Science, 2018, 11(6): 1431-1436. DOI:10.1039/c8ee00054a
doi: 10.1039/c8ee00054a
[42]   XIONG W, ZHAO X H, ZHU G X, et al. Silicification-induced cell aggregation for the sustainable production of H2 under aerobic conditions[J]. Angewandte Chemie International Edition, 2015, 54(41): 11961-11965. DOI:10.1002/anie.201504634
doi: 10.1002/anie.201504634
[43]   HE M L, LI L, ZHANG L T, et al. The enhancement of hydrogen photoproduction in Chlorella protothecoides exposed to nitrogen limitation and sulfur deprivation[J]. International Journal of Hydrogen Energy, 2012, 37(22): 16903-16915. DOI:10.1016/j.ijhydene.2012.08.121
doi: 10.1016/j.ijhydene.2012.08.121
[44]   CHADER S, HACENE H, AGATHOS S N. Study of hydrogen production by three strains of Chlorella isolated from the soil in the Algerian Sahara[J]. International Journal of Hydrogen Energy, 2009, 34(11): 4941-4946. DOI:10.1016/j.ijhydene.2008.10.058
doi: 10.1016/j.ijhydene.2008.10.058
[45]   KRUSE O, RUPPRECHT J, BADER K P, et al. Improved photobiological H2 production in engineered green algal cells[J]. Journal of Biological Chemistry, 2005, 280(40): 34170-34177. DOI:10. 1074/jbc.M503840200
doi: 10. 1074/jbc.M503840200
[46]   STEINBECK J, NIKOLOVA D, WEINGARTEN R, et al. Deletion of proton gradient regulation 5 (PGR5) and PGR5-Like 1 (PGRL1) proteins promote sustainable light-driven hydrogen production in Chlamydomonas reinhardtii due to increased PSⅡ activity under sulfur deprivation[J]. Frontiers in Plant Science, 2015, 6: 1-11. DOI:10.3389/fpls.2015.00892
doi: 10.3389/fpls.2015.00892
[47]   TORZILLO G, SCOMA A, FARALONI C, et al. Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant[J]. International Journal of Hydrogen Energy, 2009, 34(10): 4529-4536. DOI:10.1016/j.ijhydene.2008.07.093
doi: 10.1016/j.ijhydene.2008.07.093
[48]   WU S X, HUANG R, XU L L, et al. Improved hydrogen production with expression of hemH and lba genes in chloroplast of Chlamydomonas reinhardtii [J]. Journal of Biotechnology, 2010, 146(3): 120-125. DOI:10.1016/j.jbiotec.2010.01.023
doi: 10.1016/j.jbiotec.2010.01.023
[49]   BEN-ZVI O, DAFNI E, FELDMAN Y, et al. Re-routing photosynthetic energy for continuous hydrogen production in vivo[J]. Biotechnology for Biofuels, 2019, 12(1): 1-13. DOI:10.1186/s13068-019-1608-3
doi: 10.1186/s13068-019-1608-3
[50]   BENEMANN J R. Hydrogen production by microalgae[J]. Journal of Applied Phycology, 2000, 12(3/4/5): 291-300. DOI:10.1023/A:1008175 112704
doi: 10.1023/A:1008175 112704
[51]   POW T, KRASNA A I. Photoproduction of hydrogen from water in hydrogenase-containing algae[J]. Archives of Biochemistry and Biophysics, 1979, 194(2): 413-421. DOI:10.1016/0003-9861(79)90635-0
doi: 10.1016/0003-9861(79)90635-0
[52]   MARQUEZ-REYES L A, SÁNCHEZ-SAAVEDRA M P, VALDEZ-VAZQUEZ I. Improvement of hydrogen production by reduction of the photosynthetic oxygen in microalgae cultures of Chlamydomonas gloeopara and Scenedesmus obliquus [J]. International Journal of Hydrogen Energy, 2015, 40(23): 7291-7300. DOI:10.1016/j.ijhydene.2015.04.060
doi: 10.1016/j.ijhydene.2015.04.060
[53]   WYKOFF D D, DAVIES J P, MELIS A, et al. The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii [J]. Plant Physiology, 1998, 117(1): 129-139. DOI:10.1104/pp.117.1.129
doi: 10.1104/pp.117.1.129
[54]   MELIS A, ZHANG L, FORESTIER M, et al. Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii [J]. Plant Physiology, 2000, 122(1): 127-136. DOI:10.1104/pp.122.1.127
doi: 10.1104/pp.122.1.127
[55]   NOONE S, RATCLIFF K, DAVIS R A, et al. Expression of a clostridial [FeFe]-hydrogenase in Chlamydomonas reinhardtii prolongs photo-production of hydrogen from water splitting[J]. Algal Research, 2017, 22: 116-121. DOI:10.1016/j.algal.2016.12.014
doi: 10.1016/j.algal.2016.12.014
[56]   GREENBAUM E. Photosynthetic hydrogen and oxygen production: Kinetic studies[J]. Science, 1982, 215(4530): 291-293. DOI:10.1126/science. 215.4530.291
doi: 10.1126/science. 215.4530.291
[57]   GIBBS M, GFELLER R P, CHEN C. Fermentative metabolism of Chlamydomonas reinhardtii: Ⅲ photoassimilation of acetate[J]. Plant Physiology, 1986, 82(1):160-166. DOI:10.1104/pp.82.1.160
doi: 10.1104/pp.82.1.160
[58]   MA W M, CHEN M, WANG L J, et al. Treatment with NaHSO3 greatly enhances photobiological H2 production in the green alga Chlamydomonas reinhardtii [J]. Bioresource Technology, 2011, 102(18): 8635-8638. DOI:10.1016/j.biortech.2011. 03.052
doi: 10.1016/j.biortech.2011. 03.052
[59]   NAGY V, PODMANICZKI A, VIDAL-MEIRELES A, et al. Water-splitting-based, sustainable and efficient H2 production in green algae as achieved by substrate limitation of the Calvin-Benson-Bassham cycle[J]. Biotechnology for Biofuels, 2018, 11(1): 69-85. DOI:10.1186/s13068-018-1069-0
doi: 10.1186/s13068-018-1069-0
[60]   SU D Y, QI J R, LIU X M, et al. Enzyme-modulated anaerobic encapsulation of Chlorella cells allows switching from O2 to H2 production[J]. Angewandte Chemie International Edition, 2019, 58(12): 3992-3995. DOI:10.1002/anie.201900255
doi: 10.1002/anie.201900255
[61]   FAKHIMI N, DUBINI A, TAVAKOLI O, et al. Acetic acid is key for synergetic hydrogen production in Chlamydomonas-bacteria co-cultures[J]. Bioresource Technology, 2019, 289: 121648-121657. DOI:10.1016/j.biortech.2019.121648
doi: 10.1016/j.biortech.2019.121648
[62]   LAKATOS G, DEÁK Z, VASS I, et al. Bacterial symbionts enhance photo-fermentative hydrogen evolution of Chlamydomonas algae[J]. Green Chemistry, 2014, 16(11): 4716-4727. DOI:10. 1039/C4GC00745J
doi: 10. 1039/C4GC00745J
[63]   BAN S D, LIN W T, WU F Y, et al. Algal-bacterial cooperation improves algal photolysis-mediated hydrogen production[J]. Bioresource Technology, 2017, 251: 350-357. DOI:10.1016/j.biortech.2017.12.072
doi: 10.1016/j.biortech.2017.12.072
[64]   PACHAPUR V L, SARMA S J, BRAR S K, et al. Co-culture strategies for increased biohydrogen production[J]. International Journal of Energy Research, 2015, 39(11): 1479-1504. DOI:10.1002/er.3364
doi: 10.1002/er.3364
[65]   MARKOV S A, EIVAZOVA E R, GREENWOOD J. Photostimulation of H2 production in the green alga Chlamydomonas reinhardtii upon photoinhibition of its O2-evolving system[J]. International Journal of Hydrogen Energy, 2006, 31(10): 1314-1317. DOI:10.1016/j.ijhydene.2005.11.017
doi: 10.1016/j.ijhydene.2005.11.017
[66]   HOSHINO T, JOHNSON D J, CUELLO J L. Design of new strategy for green algal photo-hydrogen production: Spectral-selective photosystem Ⅰactivation and photosystem Ⅱ deactivation[J]. Bioresource Technology, 2012, 120: 233-240. DOI:10.1016/j.biortech.2012.06.011
doi: 10.1016/j.biortech.2012.06.011
[67]   SHU L, XIONG W, SHAO C Y, et al. Improvement in the photobiological hydrogen production of aggregated Chlorella by dimethyl sulfoxide[J]. Chembiochem, 2018, 19(7): 669-673. DOI:10.1002/cbic.201700637
doi: 10.1002/cbic.201700637
[68]   WYKOFF D D, DAVIES J P, MELIS A, et al. The regulation of photosynthetic electron transport during nutrient deprivation in chlamydomonas reinhardtii [J]. Plant Physiology, 1988, 117(1): 129-139. DOI:10.1104/pp.117.1.129
doi: 10.1104/pp.117.1.129
[69]   MELIS A, ZHANG L, FORESTIER M, et al. Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii [J]. Plant Physiology, 2000, 122(1): 127-136. DOI:10.1104/pp.122.1.127
doi: 10.1104/pp.122.1.127
[70]   MELIS A, HAPPE T. Hydrogen production. green algae as a source of energy[J]. Plant Physiology, 2001, 127(3): 740-748. doi:10.1104/pp.010498
doi: 10.1104/pp.010498
[71]   WILLIAMS C R, BEES M A. Mechanistic modeling of sulfur-deprived photosynthesis and hydrogen production in suspensions of Chlamydomonas reinhardtii [J]. Biotechnology and Bioengineering, 2014, 111(2): 320-335. DOI:10.1002/bit.25023
doi: 10.1002/bit.25023
[72]   MASWANNA T, PHUNPRUCH S, LINDBLAD P, et al. Enhanced hydrogen production by optimization of immobilized cells of the green alga Tetraspora sp. CU2551 grown under anaerobic condition[J]. Biomass and Bioenergy, 2018, 111: 88-95. DOI:10.1016/j.biombioe.2018.01.005
doi: 10.1016/j.biombioe.2018.01.005
[73]   KOSOUROV S N, SEIBERT M. Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions[J]. Biotechnology and Bioengineering, 2010, 102(1): 50-58. DOI:10.1002/bit.22050
doi: 10.1002/bit.22050
[74]   LAURINAVICHENE T V, FEDOROV A S, GHIRARDI M L, et al. Demonstration of sustained hydrogen photoproduction by immobilized, sulfur-deprived Chlamydomonas reinhardtii cells[J]. International Journal of Hydrogen Energy, 2006, 31(5): 659-667. DOI:10.1016/j.ijhydene.2005. 05.002
doi: 10.1016/j.ijhydene.2005. 05.002
[75]   PHILIPPS G, HAPPE T, HEMSCHEMEIER A. Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii [J]. Planta, 2012, 235(4): 729-745. DOI:10.1007/s00425-011-1537-2
doi: 10.1007/s00425-011-1537-2
[76]   APARICIO P J, AZUARA M P, BALLESTEROS A, et al. Effects of light intensity and oxidized nitrogen sources on hydrogen production by Chlamydomonas reinhardtii [J]. Plant Physiology, 1985, 78(4): 803-806. DOI:10.1104/pp.78.4.803
doi: 10.1104/pp.78.4.803
[77]   BATYROVA K A, TSYGANKOV A A, KOSOUROV S N. Sustained hydrogen photoproduction by phosphorus-deprived Chlamydomonas reinhardtii cultures[J]. International Journal of Hydrogen Energy, 2012, 37(10): 8834-8839. DOI:10.1016/j.ijhydene.2012. 01.068
doi: 10.1016/j.ijhydene.2012. 01.068
[78]   BATYROVA K, GAVRISHEVA A, IVANOVA E, et al. Sustainable hydrogen photoproduction by phosphorus-deprived marine green microalgae Chlorella sp.[J]. International Journal of Molecular Sciences, 2015, 16(2): 2705-2716. DOI:10.3390/ijms16022705
doi: 10.3390/ijms16022705
[79]   VOLGUSHEVA A, KUKARSKIKH G, KRENDELEVA T, et al. Hydrogen photoproduction in green algae Chlamydomonas reinhardtii under magnesium deprivation[J]. RSC Advances, 2015, 5(8): 5633-5637. DOI:10.1039/C4RA12710B
doi: 10.1039/C4RA12710B
[80]   PAPAZI A, GJINDALI A I, KASTANAKI E, et al. Potassium deficiency, a "smart" cellular switch for sustained high yield hydrogen production by the green alga Scenedesmus obliquus [J]. International Journal of Hydrogen Energy, 2014, 39(34): 19452-19464. DOI:10.1016/j.ijhydene.2014.09.096
doi: 10.1016/j.ijhydene.2014.09.096
[81]   GHIRARDI M L, TOGASAKI R K, SEIBERT M. Oxygen sensitivity of algal H2-production[J]. Applied Biochemistry and Biotechnology, 1997, 63-65(1): 141-151. DOI:10.1007/BF02920420
doi: 10.1007/BF02920420
[82]   STAPLETON J A, SWARTZ J R. Development of an in vitro compartmentalization screen for high-throughput directed evolution of [FeFe] hydrogenases[J]. PloS One, 2010, 5(12): e15275. DOI:10.1371/journal.pone.0015275
doi: 10.1371/journal.pone.0015275
[83]   RÜHLE T, HEMSCHEMEIER A, MELIS A, et al. A novel screening protocol for the isolation of hydrogen producing Chlamydomonas reinhardtii strains[J]. BMC Plant Biology, 2008, 8: 107. DOI:10.1186/1471-2229-8-107
doi: 10.1186/1471-2229-8-107
[84]   XIONG J, SUBRAMANIAM S, GOVINDJEE. A knowledge-based three dimensional model of the Photosystem Ⅱ reaction center of Chlamydomonas reinhardtii [J]. Photosynthesis Research, 1998, 56(3): 229-254. DOI:10.1023/A:1006061918025
doi: 10.1023/A:1006061918025
[85]   SCOMA A, KRAWIETZ D, FARALONI C, et al. Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant[J]. Journal of Biotechnology, 2012, 157(4): 613-619. DOI:10. 1016/j.jbiotec.2011.06.019
doi: 10. 1016/j.jbiotec.2011.06.019
[86]   BATYROVA K, HALLENBECK P C. Hydrogen production by a Chlamydomonas reinhardtii strain with inducible expression of photosystem Ⅱ[J]. International Journal of Molecular Sciences, 2017, 18(3): 647-661. DOI:10.3390/ijms18030647
doi: 10.3390/ijms18030647
[87]   HEMSCHEMEIER A, FOUCHARD S, COURNAC L, et al. Hydrogen production by Chlamydomonas reinhardtii: An elaborate interplay of electron sources and sinks[J]. Planta, 2008, 227(2): 397-407. DOI:10.1007/s00425-007-0626-8
doi: 10.1007/s00425-007-0626-8
[88]   PINTO T S, MALCATA F X, ARRABACA J D, et al. Rubisco mutants of Chlamydomonas reinhardtii enhance photosynthetic hydrogen production[J]. Applied Microbiology and Biotechnology, 2013, 97(12): 5635-5643. DOI:10.1007/s00253-013-4920-z
doi: 10.1007/s00253-013-4920-z
[89]   TOLLETER D, GHYSELS B, ALRIC J, et al. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii [J]. The Plant Cell, 2011, 23(7): 2619-2630. DOI:10.1105/tpc.111. 086876
doi: 10.1105/tpc.111. 086876
[90]   CHEN M, ZHANG J, ZHAO L, et al. Loss of algal proton gradient regulation 5 increases reactive oxygen species scavenging and H2 evolution[J]. Journal of Integrative Plant Biology, 2016, 58(12): 943-946. DOI:10.1111/jipb.12502
doi: 10.1111/jipb.12502
[91]   HWANG J H, KIM H C, CHOI J A, et al. Photoautotrophic hydrogen production by eukaryotic microalgae under aerobic conditions[J]. Nature Communications, 2014, 5: 3234. DOI:10.1038/ncomms4234
doi: 10.1038/ncomms4234
[92]   XU F Q, MA W M, ZHU X G. Introducing pyruvate oxidase into the chloroplast of Chlamydomonas reinhardtii increases oxygen consumption and promotes hydrogen production[J]. International Journal of Hydrogen Energy, 2011, 36(17): 10648-10654. DOI:10.1016/j.ijhydene.2011.05.130
doi: 10.1016/j.ijhydene.2011.05.130
[93]   WU S X, YAN G Y, XU L L, et al. Improvement of hydrogen production with expression of lba gene in chloroplast of Chlamydomonas reinhardtii [J]. International Journal of Hydrogen Energy, 2010, 35(24): 13419-13426. DOI:10.1016/j.ijhydene. 2009.11.118
doi: 10.1016/j.ijhydene. 2009.11.118
[94]   WU S X, XU L L, HUANG R, et al. Improved biohydrogen production with an expression of codon-optimized hemH and lba genes in the chloroplast of Chlamydomonas reinhardtii [J]. Bioresource Technology, 2011, 102(3): 2610-2616. DOI:10. 1016/j.biortech.2010.09.123
doi: 10. 1016/j.biortech.2010.09.123
[95]   NOONE S, RATCLIFF K, DAVIS R A, et al. Expression of a clostridial [FeFe]-hydrogenase in Chlamydomonas reinhardtii prolongs photo-production of hydrogen from water splitting[J]. Algal Research, 2016, 22: 116-121. DOI:10.1016/j.algal. 2016.12.014
doi: 10.1016/j.algal. 2016.12.014
[96]   DUCAT D C, SACHDEVA G, SILVER P A. Rewiring hydrogenase-dependent redox circuits in cyanobacteria[J]. Proceedings of the National Academy of Sciences, 2011, 108(10): 3941-3946. DOI:10.1073/pnas.1016026108
doi: 10.1073/pnas.1016026108
[97]   EILENBERG H, WEINER I, BEN-ZVI O, et al. The dual effect of a ferredoxin-hydrogenase fusion protein in vivo: Successful divergence of the photosynthetic electron flux towards hydrogen production and elevated oxygen tolerance[J]. Biotechnology for Biofuels, 2016, 9(1): 182-193. DOI:10.1186/s13068-016-0601-3
doi: 10.1186/s13068-016-0601-3
[1] Cheng Qiong Xi Lingling Shi Qingzhao  . Biosensor of Glucose Dehydrogenase Immobilized by Regenerated Silk Fibroin [J]. Journal of Zhejiang University (Science Edition), 1998, 25(4): 63-65.