Ca2+ enhances algal photolysis hydrogen production by improving the direct and indirect pathways

https://doi.org/10.1016/j.ijhydene.2018.11.075Get rights and content

Highlights

  • Ca2+ enhances the algal photolysis H2 production by protecting PS II activity.

  • Ca2+ improves the direct and indirect photolysis pathway of H2 production.

  • Ca2+ reduces ROS by activating the activities of CAT and SOD.

  • Ca2+ promotes the assimilation of acetic acid and starch synthesis.

Abstract

In this study, Ca2+ was applied to enhance the photolysis H2 production of Chlamydomonas reinhardtii grown in pure culture or co-cultivated with bacterium. With addition of Ca2+, the chlorophyll and protein contents in algal cells were maintained at high levels and the reactive oxygen species (ROS) were scavenged to tolerable levels by activities of catalase (CAT) and superoxide dismutase (SOD). High chlorophyll and low ROS are benefit to protect the photosystem II (PS II) activity that responsible for the direct photolysis H2 production. Moreover, addition of Ca2+ was able to promote the acetic acid assimilation as well as the starch synthesis. The starch degradation, in return, contributed to the H2 production via the indirect photolysis pathway. Based on the improvements of direct and indirect photolysis pathways, the H2 production of algae grown in co-cultivation adding with 5 mM Ca2+ reached a maximum value of 306 mL L−1, which was 2.4 times higher than the production without Ca2+ addition. This study gives an efficient and easy strategy to improve the algal photolysis H2 production, and gets an insight into the mechanisms of the improvement.

Introduction

The increasing demand for carbon emission reduction makes H2 an attractive fuel [1], [2]. However, conventional technologies of H2 production via the reformation of natural gas and oil, coal gasification, and water electrolysis are mainly based on the conversion of fossil fuel, which are costly and emit large amount of CO2 [3]. In comparison, the algal photolysis that uses solar energy to split water into O2 and H2 is carbon negative and less energy intensive, which has a great potential to become an immense source for H2; moreover, algae have high biomass productivity and solar energy conversion efficiency and could be grown on non-arable land, which make it more attractive [3], [4].

H2 production in green algae (such as the model species Chlamydomonas reinhardtii) is predominantly due [FeFe] hydrogenase; however, this enzyme is highly O2 sensitive, which has been documented to be the main bottleneck for the algal photolysis H2 production [5], [6]. At present, some solutions have been devised to reduce the O2 level during H2 producing process. For instance, the sulfur deprivation strategy that proposed by Melis in 2010, is currently a widely used method; it partially inactivates PS II activity, thus limiting the photolysis O2 generation and maintaining the O2 level below the rate of mitochondrial respiration, which in turn results in the required anaerobic condition for H2 production [3], [5], [7], [8]. However, sulfur deprivation reduces the rate of repair of a PS II reaction center protein D1 and results in the reduction of PS II to ∼25% of the original level [3], [8]. Though it improves the algal photolysis H2 production, the reduction of PS II activity would limit the overall efficiency of H2 production by inhibiting the electron (e) transport via direct photolysis pathway.

To overcome the limitations because of sulfur deprivation, several approaches aiming to balance the efficiency of H2 production and the reduction of PS II activity were developed. For instance, utilization of microdosing of sulfur to allow PS II repair; magnesium deprivation decreases photosynthetic activity but increases respiration; co-cultivation of algae and bacteria to archive algal anaerobiosis by increasing bacterial respiration [3], [8]. During the cooperation between algal and bacterial cells, the bacterial respiration removes the O2 sensitivity from algal hydrogenase while the algae supplies O2 and organics for bacterial growth for return [9]. Based on the algal-bacterial co-cultivation associating with sulfur deprivation, the H2 productions via algal photolysis have been reported as high as 170, 194, 164, 6 and 34 mL L−1 when co-cultivated with bacterial strains Pseudomonas sp. D, Bradyrhizobium japonicum, Azotobacter chroococcum, Escherichia coli and Pseudomonas species, respectively [9], [10], [11], [12], [13]. Besides the reduction of O2 level, algal-bacterial cooperation was reported to be capable of keeping the direct photolysis pathway that transports e to hydrogenase by decreasing the reduction of PS II system [9]. It has been demonstrated that approximate 80% of the H2 production derives directly from PS II activity [14]. Then, maintaining a high level of PS II activity is benefit to the algal photolysis H2 production.

Ca2+ has been found to help plants to adapt environmental stresses (such as heat, salt, irradiance, etc.) by inducing gene expressions and/or activating biochemical responses [15]. For instance, Ca2+ could maintain plant photosynthesis via the protection of PS II reaction center protein D1 from the photodamage that induced by intracellular ROS; because the presence of Ca2+ induces the expression of some antioxidant enzymes, which are responsible for the ROS scavenging [15], [16], [17], [18]. In this study, we aimed to enhance the algal photolysis H2 production by using Ca2+ and analyze the potential mechanism that mainly responsible for the enhancement on the levels of chlorophyll reduction, starch and protein syntheses, intracellular and extracellular acids and alcohols metabolisms, and ROS-scavenging enzymes activities.

Section snippets

Algal and bacterial strains

Algal strain Chlamydomonas reinhardtii FACHB-265 was obtained from the Freshwater Algae Culture Collection at the Institute of Hydrobiology (FACHB, http://algae.ihb.ac.cn/). Algal cultivation was performed in 250-mL glass flasks filled up with 100 mL of Tris-Acetate-Phosphate (TAP) medium, which contains 20 mM Tris base, 7 mM NH4Cl, 0.83 mM MgSO4, 0.45 mM CaCl2, 1.05 mM KH2PO4, 1.65 mM K2HPO4, 134 μM Na2EDTA, 136 μM ZnCl2, 184 μM H3BO3, 40 μM MnCl2, 32.9 μM FeCl2, 12.3 μM CoCl2, 10 μM CuCl2,

Ca2+ enhances the algal H2 production

As results shown in Fig. 1, the higher the concentration of Ca2+ added, the more the H2 produced by algae grown in pure cultures; after 15 days cultivation, the H2 accumulation reached 54.2 mL L−1 with the addition of 20 mM Ca2+, which was about 3.8 times higher than the production of algal culture grown without Ca2+ addition (Fig. 1a). In the same way, addition of Ca2+ was benefit to the H2 production of algae co-cultivated with bacterium Pseudomonas sp. strain D. With addition of 5 mM Ca2+,

Conclusions

Ca2+ was found to be able to enhance the photolysis H2 production of algae grown in pure culture or co-cultivated with bacterium. During the period of algal H2 production, addition of Ca2+ was capable of decreasing the rate of chlorophyll reduction, maintaining the protein content and inducing the ROS scavenging. These positive effects induced by Ca2+ protected the PS II activity that responsible for the direct photolysis H2 production. In addition, the presence of Ca2+ was able to enhance the

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 41473072).

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