On the pathways feeding the H2 production process in nutrient-replete, hypoxic conditions. Commentary on the article "Low oxygen levels contribute to improve photohydrogen production in mixotrophic non-stressed Chlamydomonas cultures", by Jurado-Oller et al., Biotechnology for Biofuels, published September 7, 2015; 8:149

Abstract

Background: Under low O₂ concentration (hypoxia) and low light, Chlamydomonas cells can produce H₂ gas in nutrient-replete conditions. This process is hindered by the presence of O₂, which inactivates the [FeFe]-hydrogenase enzyme responsible for H₂ gas production shifting algal cultures back to normal growth. The main pathways accounting for H₂ production in hypoxia are not entirely understood, as much as culture conditions setting the optimal redox state in the chloroplast supporting long-lasting H₂ production. The reducing power for H₂ production can be provided by photosystem II (PSII) and photofermentative processes during which proteins are degraded via yet unknown pathways. In hetero- or mixotrophic conditions, acetate respiration was proposed to indirectly contribute to H₂ evolution, although this pathway has not been described in detail.

Main body: Recently, Jurado-Oller et al. (Biotechnol Biofuels 8: 149, 7) proposed that acetate respiration may substantially support H₂ production in nutrient-replete hypoxic conditions. Addition of low amounts of O₂ enhanced acetate respiration rate, particularly in the light, resulting in improved H₂ production. The authors surmised that acetate oxidation through the glyoxylate pathway generates intermediates such as succinate and malate, which would be in turn oxidized in the chloroplast generating FADH₂ and NADH. The latter would enter a PSII-independent pathway at the level of the plastoquinone pool, consistent with the light dependence of H₂ production. The authors concluded that the water-splitting activity of PSII has a minor role in H₂ evolution in nutrient-replete, mixotrophic cultures under hypoxia. However, their results with the PSII inhibitor DCMU also reveal that O₂ or acetate additions promoted acetate respiration over the usually dominant PSII-dependent pathway. The more oxidized state experienced by these cultures in combination with the relatively short experimental time prevented acclimation to hypoxia, thus precluding the PSII-dependent pathway from contributing to H₂ production.

Conclusions: In Chlamydomonas, continuous H₂ gas evolution is expected once low O₂ partial pressure and optimal reducing conditions are set. Under nutrient-replete conditions, the electrogenic processes involved in H₂ photoproduction may rely on various electron transport pathways. Understanding how physiological conditions select for specific metabolic routes is key to achieve economic viability of this renewable energy source.

Keywords: Acetate; Biophotolysis; Chlamydomonas reinhardtii; Fermentation; Green alga; H2 production; Hydrogenase; Hypoxia; Photosystem II; Respiration.