Abstract
Unicellular green algae Chlamydomonas reinhardtii are known to make hydrogen photoproduction under the anaerobic condition with water molecules as the hydrogen source. Since the hydrogen photoproduction occurs for a cell to circumvent crisis of its survival, it is only temporary. It is a challenge to realize persistent hydrogen production because the cells must withstand stressful conditions to survive with alternation of generations in the cell culture. In this paper, we have found a simple and cost-effective method to sustain the hydrogen production over 14 days in the original culture, without supply of fresh cells nor exchange of the culture medium. This is achieved for the cells under hydrogen production in a sulfur-deprived culture solution on the {anaerobic, intense light} condition in a desiccator, by periodically providing a short period of the recovery time (2 h) with a small amount of TAP(+S) supplied outside of the desiccator. As this operation is repeated, the response time of transition into hydrogen production (preparation time) is shortened and the rate of hydrogen production (build up time) is increased. The optimum states of these properties favorable to the hydrogen production are attained in a few days and stably sustained for more than 10 days. Since generations are alternated during this consecutive hydrogen production experiment, it is suggested that the improved hydrogen production properties are inherited to next generations without genetic mutation. The properties are reset only when the cells are placed on the {sulfur-sufficient, aerobic, moderate light} conditions for a long time (more than 1 day at least).
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References
Allakhverdiev SI (2012) Photosynthetic and biomimetic hydrogen production. Int J Hydrog Energy 37:8744–8752
Allakhverdiev SI, Kreslavski VD, Thavasi V, Zharmukhamedov SK, Klimov VV, Nagata T, Nishihara H, Ramakrishna S (2009) Hydrogen photoproduction by use of photosynthetic organisms and biomimetic systems. Photochem Photobiol S 8:148–156
Allakhverdiev SI, Thavasi V, Kreslavski VD, Zharmukhamedov SK, Klimov VV, Ramakrishna S, Los DA, Mimuro M, Nishihara H, Carpentier R (2010) Photosynthetic hydrogen production. Photochem Photobiol C Photochem Rev 11:101–113
Amos WA (2004) Updated cost analysis of photobiological hydrogen production from Chlamydomonas reinhardtii green algae. National Renewable Energy Laboratory, Golden, CO, NREL/MP-560-35593. https://www.hydrogen.energy.gov/analysis_repository/project.cfm/PID=110. Accessed 06 Apr 2016
Antal TK, Krendeleva TE, Laurinavichene TV, Makarova VV, Ghirardi ML, Rubin AB, Tsygankov AA, Seibert M (2003) The dependence of algal H2 production on photosystem II and O2 consumption activities in sulfur-deprived Chlamydomonas reinhardtii cells. Biochim Biophys Acta 1607:153–160
Antal TK, Volgusheva AA, Kukarskih GP, Krendeleva TE, Rubin AB (2009) Relationships between H2 photoproduction and different electron transport pathways in sulfur-deprived Chlamydomonas reinhardtii. Int J Hydrog Energy 34:9087–9094
Antal TK, Krendeleva TE, Rubin AB (2011) Acclimation of green algae to sulfur deficiency: underlying mechanisms and application for hydrogen production. Appl Microbiol Biotechnol 89:3–15
Antal TK, Matorin DN, Kukarskikh GP, Lambreva MD, Tyystjarvi E, Krendeleva TE, Tsygankov AA, Rubin AB (2014) Pathways of hydrogen photoproduction by immobilized Chlamydomonas reinhardtii cells deprived of sulfur. Int J Hydrog Energy 39:18194–18203
Atsumi S, Cann AF, Connor MR, Shen CR, Smith KM, Brynildsen MP, Chou KJY, Hanai T, Liao JC (2008) Metabolic engineering of Escherichia coli for 1-butanol production. Metab Eng 10:305–311
Babu VJ, Kumar MK, Nair AS, Kheng TL, Allakhverdiev SI (2012) Visible light photocatalytic water splitting for hydrogen production from N–TiO2 rice grain shaped electrospun nanostructures. Int J Hydrog Energy 37:8897–8904
Chochois V, Dauvillee D, Beyly A, Tolleter D, Cuine S, Timpano H, Ball S, Cournac L, Peltier G (2009) Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism. Plant Physiol 151:631–640
Clowez S, Godaux D, Cardol P, Wollman FA, Rappaport F (2015) The involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia. Biol Chem 290:8666–8676
Cox GM, McCrimmon BMD, Nemati TA, Olson CM (2013) The production of hydrogen gas by Chlamydomonas reinhardtii in sulfur-deprived conditions under red light and white light. Exped Arch 3:1–18
Das D, Dutta T, Nath K, Kotay SM, Das AK, Veziroglu TN (2006) Role of Fe-hydrogenase in biological hydrogen production. Curr Sci 90:1627–1637
Fouchard S, Hemschemeier A, Caruana A, Pruvost J, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Appl Environ Microbiol 10:6199–6205
Fritsch J, Scheerer P, Frielingsdorf S, Kroschinsky S, Friedrich B, Lenz O, Spahn CMT (2011) The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479:249–252
Grewe S, Ballottari M, Alcocer M, D’Andrea C, Blifernez-Klassen O, Hankamer B, Mussgnug JH, Bassi R, Krusea O (2014) Light-harvesting complex protein LHCBM9 is critical for photosystem II activity and hydrogen production in Chlamydomonas reinhardtii. Plant Cell 26:1598–1611
Hankamera B, Lehrb F, Rupprechta J, Mussgnugc JH, Postenb C, Krusec O (2007) Photosynthetic biomass and H2 production by green algae: from bioengineering to bioreactor scale-up. Physiol Plant 131:10–21
Isono T, Yamashita K, Momose D, Kobayashi H, Kitamura M, Nishiyama Y, Hosoya T, Kanda H, Kudo A, Okada N, Yagi T, Nakata K, Mineki S, Tokunaga E (2015) Scan-free absorbance spectral imaging A(x, y, λ) of single live algal cells for quantifying absorbance of cell suspensions. PLoS One 10:1–16
Jablonka E, Lamb MJ (1998) Epigenetic inheritance in evolution. Evol Biol 11:159–183
Jablonka E, Lachmann M, Lamb MJ (1992) Evidence, mechanisms and models for the inheritance of acquired characters. Theor Biol 158:245–268
Kim JP, Kang CD, Sim SJ, Kim MS, Park TH, Lee DH, Kim DJ, Kim JH, Lee YK, Pak DW (2005) Cell age optimization for hydrogen production induced by sulfur deprivation using a green alga Chlamydomonas reinhardtii UTEX 90. Microbiol Biotechnol 15:131–135
Kim JP, Kang CD, Park TH, Kim MS, Sim SJ (2006) Enhanced hydrogen production by controlling light intensity in sulfur-deprived Chlamydomonas reinhardtii culture. Int J Hydrog Energy 31:1585–1590
Kruse O, Rupprecht J, Bader KP, Thormas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells. Biol Chem 280:34170–34177
Levin MD (2003) Noise in gene expression as the source of non-genetic individuality in the chemotactic response of Escherichia coli. FEBS Lett 550:135–138
Li X, Huang S, Yu J, Wang Q, Wu S (2013) Improvement of hydrogen production of Chlamydomonas reinhardtii by co-cultivation with isolated bacteria. Int J Hydrog Energy 38:10779–10787
Mameli M (2004) Nongenetic selevtion and nongenetic inheritance. Br J Philos Sci 55:35–71
Markov SA, Eivazova ER, Greenwood J (2006) Photostimulation of H2 production in the green alga Chlamydomonas reinhardtii upon photoinhibition of its O2-evolving system. Int J Hydrog Energy 31:1314–1317
Masukawa H, Sakurai H, Hausinger RP, Inoue K (2014) Sustained photobiological hydrogen production in the presence of N2 by nitrogenase mutants of the heterocyst-forming cyanobacterium Anabaena. Int J Hydrog Energy 39:19444–19451
Matsumura K, Yagi T, Yasuda K (2003) Role of timer and sizer in regulation of Chlamydomonas cell cycle. Biochem Biophys Res Commun 306:1042–1049
Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748
Morsy FM (2011) Acetate versus sulfur deprivation role in creating anaerobiosis in light for hydrogen production by Chlamydomonas reinhardtii and Spirulina platensis: two different organisms and two different mechanisms. Photochem Photobiol 87:137–142
Najafpour MM, Allakhverdiev SI (2012) Manganese compounds as water oxidizing catalysts for hydrogen production via water splitting: from manganese complexes to nano-sized manganese oxides. Int J Hydrog Energy 37:8753–8764
Nath K, Najafpour MM, Voloshin RA, Balaghi SE, Tyystjarvi E, Timilsina R, Eaton-Rye JJ, Tomo T, Nam HG, Nishihara H, Ramakrishna S, Shen JR, Allakhverdiev SI (2015) Photobiological hydrogen production and artificial photosynthesis for clean energy: from bio to nanotechnologies. Photosynth Res 126:237–247
Omata T, Ogawa T (1985) Changes in the polypeptide composition of the cytoplasmic membrane in the cyanobacterium Anacystis nidulans during adaptation to low CO2 conditions. Plant Cell Physiol 26:1075–1081
Pal C, Miklos I (1999) Epigenetic inheritance, genetic assimilation and speciation. J Theor Biol 200:19–37
Saenz ME, Bisova K, Touloupakis E, Faraloni C, Marzio WDD, Torzillo G (2015) Evidences of oxidative stress during hydrogen photoproduction in sulfur-deprived cultures of Chlamydomonas reinhardtii. Int J Hydrog Energy 40:10410–10417
Saito K, Rutherfordc AW, Ishikita H (2013) Mechanism of proton-coupled quinone reduction in photosystem II. Proc Natl Acad Sci USA 110:954–959
Sakurai H, Masukawa H, Kitashima M, Inoue K (2013) Photobiological hydrogen production Bioenergetics and challenges for its practical application. Photochem Photobiol 17:1–25
Saleem M, Chakrabarti MH, Raman AAA, Hasan DB, Daud WMAW, Mustafa A (2012) Hydrogen production by Chlamydomonas reinhardtii in a two-stage process with and without illumination at alkaline pH. Int J Hydrog Energy 37:4930–4934
Solomon F (1981) Specification of cell morphology by endogenous determinants. Cell Biol 90:547–553
Spudich JL, Koshland DK Jr (1976) Non-genetic individuality: chance in the single cell. Nature 262:467–471
Stojkovic D, Torzillo G, Faraloni C, Valant M (2015) Hydrogen production by sulfur-deprived TiO2- encapsulated Chlamydomonas reinhardtii cells. Int J Hydrog Energy 40:3201–3206
The Chlamydomonas sourcebook 2 (2008) Organellar and metabolic processes 2nd edition by David Stern (Ed.)
Tsygankov AA, Kosourov SN, Tolstygina IV, Ghirardi ML, Seibert M (2006) Hydrogen production by sulfur-deprived Chlamydomonas reinhardtii under photoautotrophic conditions. Int J Hydrog Energy 31:1574–1584
Volgusheva A, Styring S, Mamedov F (2013) Increased photosystem II stability promotes H2 production in sulfur-deprived Chlamydomonas reinhardtii. P Natl Acad Sci USA 110:7223–7228
Volgusheva A, Kukarskikh G, Krendeleva T, Rubina A, Mamedov F (2015) Hydrogen photoproduction in green algae Chlamydomonas reinhardtii under magnesium deprivation. R Soc Chem 5:5633–5637
Wakamoto Y, Yasuda K (2006) Epigenetic inheritance of elongated phenotypes between generations revealed by individual-cell-based direct observation. Meas Sci Technol 17:3171–3177
White S, Anandraj A, Trois C (2014) NADPH fluorescence as an indicator of hydrogen production in the green algae Chlamydomonas reinhardtii. Int J Hydrog Energy 39:1640–1647
Williams CR, Bees MA (2014) Mechanistic modeling of sulfur-deprived photosynthesis and hydrogen production in suspensions of Chlamydomonas reinhardtii. Biotechnol Bioeng 111:320–335
Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–987
Zhang D, Vassiliadis VS (2015) Chlamydomonas reinhardtii metabolic pathway analysis for biohydrogen production under non-steady-state operation. Ind Eng Chem Res 54:10593–10605
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We thank Toshitaka Niwase for his helping T.Y. to measure the correction curve from the sensor voltage to the hydrogen concentration.
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Yagi, T., Yamashita, K., Okada, N. et al. Hydrogen photoproduction in green algae Chlamydomonas reinhardtii sustainable over 2 weeks with the original cell culture without supply of fresh cells nor exchange of the whole culture medium. J Plant Res 129, 771–779 (2016). https://doi.org/10.1007/s10265-016-0825-0
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DOI: https://doi.org/10.1007/s10265-016-0825-0