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      Mechanistic modeling of sulfur-deprived photosynthesis and hydrogen production in suspensions of Chlamydomonas reinhardtii

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          Abstract

          The ability of unicellular green algal species such as Chlamydomonas reinhardtii to produce hydrogen gas via iron-hydrogenase is well known. However, the oxygen-sensitive hydrogenase is closely linked to the photosynthetic chain in such a way that hydrogen and oxygen production need to be separated temporally for sustained photo-production. Under illumination, sulfur-deprivation has been shown to accommodate the production of hydrogen gas by partially-deactivating O 2 evolution activity, leading to anaerobiosis in a sealed culture. As these facets are coupled, and the system complex, mathematical approaches potentially are of significant value since they may reveal improved or even optimal schemes for maximizing hydrogen production. Here, a mechanistic model of the system is constructed from consideration of the essential pathways and processes. The role of sulfur in photosynthesis (via PSII) and the storage and catabolism of endogenous substrate, and thus growth and decay of culture density, are explicitly modeled in order to describe and explore the complex interactions that lead to H 2 production during sulfur-deprivation. As far as possible, functional forms and parameter values are determined or estimated from experimental data. The model is compared with published experimental studies and, encouragingly, qualitative agreement for trends in hydrogen yield and initiation time are found. It is then employed to probe optimal external sulfur and illumination conditions for hydrogen production, which are found to differ depending on whether a maximum yield of gas or initial production rate is required. The model constitutes a powerful theoretical tool for investigating novel sulfur cycling regimes that may ultimately be used to improve the commercial viability of hydrogen gas production from microorganisms. Biotechnol. Bioeng. 2014;111: 320–335. © 2013 The Authors. Biotechnology and Bioengineering Published by Wiley Periodicals, Inc.

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              FERMENTATIVE AND PHOTOCHEMICAL PRODUCTION OF HYDROGEN IN ALGAE

              1.. After 2 hours of fermentation in nitrogen the metabolism of those algae which were found capable of photoreduction with hydrogen changes in such a way that molecular hydrogen is released from the cell in addition to carbon dioxide. 2. The amount of hydrogen formed anaerobically in the dark depends on the amount of some unknown reserve substance in the cell. More hydrogen is formed in presence of added glucose, but no proportionality has been found between the amount of substrate added and that of hydrogen formed. This is probably due to the fact that two types of fermentation reactions exist, with little or no connection between them. Whereas mainly unknown organic acids are formed during the autofermentation, the addition of glucose causes a considerable increase in the production of lactic acid. 3. Algae which have been fermenting for several hours in the dark produce upon illumination free hydrogen at several times the rate observed in the dark, provided carbon dioxide is absent. 4. Certain concentrations of dinitrophenol strongly inhibit the evolution of hydrogen in the dark. Fermentation then continues mainly as a reaction leading to lactic acid. In such poisoned algae the photochemical liberation of hydrogen still continues. 5. If the algae are poisoned with dinitrophenol the presence of carbon dioxide will not interfere with the photochemical evolution of hydrogen. 6. The amount of hydrogen released in this new photochemical reaction depends on the presence of an unknown hydrogen donor in the cell; it can be increased by the addition of glucose but not in proportion to the amount added. 7. The results obtained allow for a more correct explanation of the anaerobic induction period previously described for Scenedesmus and similar algae. The possibility of a photochemical evolution of hydrogen had not been taken into account in the earlier experiments. 8. The origin of the hydrogen released under the influence of light is discussed.
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                Author and article information

                Journal
                Biotechnol Bioeng
                Biotechnol. Bioeng
                bit
                Biotechnology and Bioengineering
                Wiley Periodicals, Inc.
                0006-3592
                1097-0290
                February 2014
                11 September 2013
                : 111
                : 2
                : 320-335
                Affiliations
                [1 ]British Antarctic Survey, Natural Environment Research Council High Cross, Madingley Road, Cambridge, CB3 0ET, UK
                [2 ]Department of Mathematics, University of York York, YO10 5DD, UK
                Author notes
                Correspondence to: C. R. Williams e-mail: chll1@ 123456bas.ac.uk

                Work conducted at School of Mathematics and Statistics, University of Glasgow, 15 University Gardens, Glasgow G12 8QW, UK.

                Contract grant sponsor: EPSRC

                Contract grant number: EP/D073398/1

                Article
                10.1002/bit.25023
                3920635
                24026984
                26ce11bf-7787-44fb-a418-68717702a5b1
                © 2013 The Authors. Biotechnology and Bioengineering Published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 14 June 2013
                : 26 July 2013
                : 09 August 2013
                Categories
                Articles

                Biotechnology
                light limitation,chlamydomonas reinhardtii,sulfur deprivation,photosynthetic growth,mechanistic model,hydrogen production

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