Biological basis of exoelectrogenesis in cyanobacteria

Laura Wey^a, Jenny Zhang^b, Christopher Howe^a

^aUniversity of Cambridge, Department of Biochemistry, United Kingdom, Tennis Court Road, 8, United Kingdom

^bUniversity of Cambridge , Department of Chemistry, United Kingdom, Lensfield Road, United Kingdom

Proceedings of International Online Conference on Bio-hybrid Approaches to Solar Energy Conversion (Biohybrid)

Online, Spain, 2020 October 27th - 29th

Organizers: Jenny Zhang, Vincent Friebe and Lars Jeuken

Contributed talk, Laura Wey, presentation 033
Publication date: 8th October 2020

Certain photosynthetic micro-organisms exhibit the ability to export electrons/reducing equivalents upon illumination in a phenomenon called exoelectrogenic activity. There is great potential to harness exoelectrogenesis of photosynthetic micro-organisms in biophotovoltaic systems to renewably generate electricity, but power outputs remain low^[1]. Rational optimisation of biophotovoltaic systems is being held back by present limited understanding of the biological basis of exoelectrogenesis of photosynthetic micro-organisms.

We know the most about exoelectrogenesis in the cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis), which is a model organism for the study of photosynthesis due to the endosymbiotic origin of the chloroplast^[2]. The electrons eventually exported upon illumination are known to originate from water by photosystem II action at the start of the photosynthetic electron transfer chain in the thylakoid membrane, and are thought to exit the downstream of photosystem I^[3,4]. It is not known how the electrons/reducing equivalents transverse the many boundary layers of the cell from the thylakoid membranes to outside the cell.

A three-electrode set-up can be used to study the photo-electrochemistry of photosynthetic micro-organisms and their isolated photosynthetic machineries^[5,6]. In chronoamperometric experiments, the net current is recorded at an electrode as it evolves from the photosynthetic material over time under chopped light (i.e. light/dark cycles). A previous study compared the photoelectrochemistry of whole Synechocystis cells and isolated photosystem II from another cyanobacterium, both using state-of-the-art hierarchically structured inverse opal indium-tin oxide (IO-ITO) working electrodes^[7]. These exhibited markedly different photocurrent profiles: whole cells gave a complex photocurrent profile, whereas isolated photosystem II gave a monophasic photocurrent profile.

Presented here is a follow up study of the photoelectrochemistry of intermediate sub-cellular fractions of Synechocystis to identify which topological features of the cyanobacterial cell are responsible for the complexity in the photocurrent profile of whole cells. We found that the periplasmic space, significantly contributes to the complex photocurrent profile of Synechocystis cells, not the surface layer or type IV pili, enhancing our understanding of the exoelectrogenic routes in this model photosynthetic micro-organism.

References:

[1] McCormick, A. J. et al. Biophotovoltaics: Oxygenic photosynthetic organisms in the world of bioelectrochemical systems. Energy Environ. Sci. 8, 1092–1109 (2015).

[2] Howe, C. J., Barbrook, A. C., Nisbet, R. E. R., Lockhart, P. J. & Larkum, A. W. D. The origin of plastids. in Philosophical Transactions of the Royal Society B: Biological Sciences 363, 2675–2685 (2008).

[3] Pisciotta, J. M., Zou, Y. & Baskakov, I. V. Role of the photosynthetic electron transfer chain in electrogenic activity of cyanobacteria. Appl. Microbiol. Biotechnol. 91, 377–385 (2011).

[4] Bombelli, P. et al. Quantitative analysis of the factors limiting solar power transduction by Synechocystis sp. PCC 6803 in biological photovoltaic devices. Energy Environ. Sci. 4, 4690–4698 (2011).

[5] Wey, L. T. et al. The Development of Biophotovoltaic Systems for Power Generation and Biological Analysis. ChemElectroChem 6, 5375–5386 (2019).

[6] Zhang, J. Z. & Reisner, E. Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis. Nat. Rev. Chem. 4, 6–21 (2020).

[7] Zhang, J. Z. et al. Photoelectrochemistry of Photosystem II in Vitro vs in Vivo. J. Am. Chem. Soc. 140, 6–9 (2018).

Acknowledgements:

The authors acknowledge the Cambridge Trust International Scholarship the Biotechnology and Biological Sciences Research Council David Phillips Fellowship for their support. The authors acknowledge Prof. Annegret Wilde (University of Freiburg, Germany) and Prof. Conrad Mullineaux (Queen Mary University of London, UK) for the gift of the pilus mutants used in this study, and Dr. David Lea-Smith (University of East Anglia, UK) for generating the surface-layer mutant used in this study. Joshua Lawrence and Xiaolong Chen also worked on this project.

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