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An evolutionary advantage of retaining this enzyme might relate to the fact that hydrogenase-mediated hydrogen evolution can oxidize NAD(P)H at the expense of only protons, not carbonbased substrates. This may provide an advantage to cells that experience microaerobic or anaerobic conditions and are therefore without the typical electron acceptor (O2, no cyanobacterium to date is known to perform anaerobic respiration (i.e. with electron acceptors other than molecular oxygen)). Given the limited choice between the reduction of protons or carbon-substrates and subsequent excretion (e.g. pyruvate?lactate production), cells that only reduce protons do not waste previously-fixed carbon, which requires an investment of ATP to produce. Likewise, hydrogen generated from proton reduction will diffuse out and away from cells more easily than organic acids or alcohols. On the other hand, it is possible that the reduced state of the cell may change faster than the diffusion of hydrogen away from the cellular environment.Thus, because of the reversibility of the Hox hydrogenase, hydrogen may serve as only a temporary ‘‘reserve’’ for electrons (and protons), which can be recovered if conditions in the cell change abruptly (for example, a light-to-dark transition as discussed in Section 7.2). The NAD(P)H pool reduction state is closely linked to photosynthesis through the plastoquinone (PQ) pool, which is also linked to respiration (Peschek et al., 2004). Support for the link between NAD(P)H and the PQ pool includes the study of a mutant of Synechocystis sp. PCC 6803 deficient in the NDH-1 complex, an enzyme that mediates electron transfer between NAD(P)(H) and PQ pools. In a mutant lacking functional NDH-1 complexes (M55), sustained hydrogen evolution could be achieved for 30 min in the presence of glucose (Cournac et al., 2004). Later, Gutthannetal. (2007) systematically studied the effects on photosynthetic hydrogen production by mutants with modifications to the electron transport chain in Synechocystis sp. PCC 6803. This work included single, double,and triple mutants of terminal oxidases as well as nitrate removal in wild-type cells. They concluded that three different ‘electron sinks’ compete for the light-derived electrons with Hox hydrogenase,including oxygen, nitrate, and CO2 (via the Calvin cycle), consistent with later results from A. maxima (Ananyev et al., 2008).Collectively, this evidence supports the interplay of Hox hydrogenase with photosynthesis and respiration via NAD(P)(H) pools among certain cyanobacteria. A working model for the relationship between photosynthesis,fermentation, and hydrogen metabolism in cyanobacteria is provided in Fig. 3. As shown, reductant can be formed either by oxidation of water by PSII, followed by a series of reactions (also involving PSI) for reduction of NADPH from ferredoxin via ferredoxin NADPH oxidoreductase, or by production of NADH via breakdown of osmolytes and glycogen during fermentation. Nitrogen assimilation from nitrate, respiration via terminal oxidases, and production of biosynthetic precursors from CO2 (via the Calvin cycle) all consume electron equivalents. When the PQ pool is mostly oxidized, electrons can also be used to reduce PQ pools via the Type I NDH, thus diverting electrons from hydrogen production. The Hox hydrogenase can act as an indirect relief for cells that have over-reduced PQ pools under microoxic conditions in the light and elevated NAD(P)H pools (reduced via fermentation) in the dark. |
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