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3D-printed hierarchical pillar array electrodes for high-performance semi-artificial photosynthesis


The rewiring of photosynthetic biomachineries to electrodes is a forward-looking semi-artificial route for sustainable bio-electricity and fuel generation. Currently, it is unclear how the electrode and biomaterial interface can be designed to meet the complex requirements for high biophotoelectrochemical performance. Here we developed an aerosol jet printing method for generating hierarchical electrode structures using indium tin oxide nanoparticles. We printed libraries of micropillar array electrodes varying in height and submicrometre surface features, and studied the energy/electron transfer processes across the bio-electrode interfaces. When wired to the cyanobacterium Synechocystis sp. PCC 6803, micropillar array electrodes with microbranches exhibited favourable biocatalyst loading, light utilization and electron flux output, ultimately almost doubling the photocurrent of state-of-the-art porous structures of the same height. When the micropillars’ heights were increased to 600 µm, milestone mediated photocurrent densities of 245 µA cm–2 (the closest thus far to theoretical predictions) and external quantum efficiencies of up to 29% could be reached. This study demonstrates how bio-energy from photosynthesis could be more efficiently harnessed in the future and provide new tools for three-dimensional electrode design.

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Fig. 1: Next-generation electrodes for biophotoelectrochemistry.
Fig. 2: Aerosol jet printing of micropillar array electrodes.
Fig. 3: Printed micropillar electrodes exhibit high light transmission and cell loading.
Fig. 4: The photoelectrochemical performance of the Synechocystis-loaded electrodes.
Fig. 5: Structure–activity relationship analysis.

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All data used in this paper are available via the Apollo repository ( or on GitHub (

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  1. Kornienko, N., Zhang, J. Z., Sakimoto, K. K., Yang, P. D. & Reisner, E. Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis. Nat. Nanotechnol. 13, 890–899 (2018).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. King, P. W. Semi-synthetic strategy. Nat. Energy 3, 921–922 (2018).

    Article  Google Scholar 

  4. Léger, C. & Bertrand, P. Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem. Rev. 108, 2379–2438 (2008).

    Article  CAS  Google Scholar 

  5. Saar, K. L. et al. Enhancing power density of biophotovoltaics by decoupling storage and power delivery. Nat. Energy 3, 75–81 (2018).

    Article  CAS  Google Scholar 

  6. Wey, L. T. et al. The development of biophotovoltaic systems for power generation and biological analysis. ChemElectroChem 6, 5375–5386 (2019).

    Article  CAS  Google Scholar 

  7. Zhang, J. Z. et al. Photoelectrochemistry of photosystem II in vitro vs in vivo. J. Am. Chem. Soc. 140, 6–9 (2018).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Bradley, R. W., Bombelli, P., Lea-Smith, D. J. & Howe, C. J. Terminal oxidase mutants of the cyanobacterium Synechocystis sp. PCC 6803 show increased electrogenic activity in biological photo-voltaic systems. Phys. Chem. Chem. Phys. 15, 13611–13618 (2013).

    Article  CAS  Google Scholar 

  10. Sekar, N., Jain, R., Yan, Y. & Ramasamy, R. P. Enhanced photo-bioelectrochemical energy conversion by genetically engineered cyanobacteria. Biotechnol. Bioeng. 113, 675–679 (2016).

    Article  CAS  Google Scholar 

  11. Liu, C., Dasgupta, N. P. & Yang, P. Semiconductor nanowires for artificial photosynthesis. Chem. Mater. 26, 415–422 (2014).

    Article  CAS  Google Scholar 

  12. Mersch, D. et al. Wiring of photosystem II to hydrogenase for photoelectrochemical water splitting. J. Am. Chem. Soc. 137, 8541–8549 (2015).

    Article  CAS  Google Scholar 

  13. Wijnhoven, J. E. & Vos, W. L. Preparation of photonic crystals made of air spheres in titania. Science 281, 802–804 (1998).

    Article  CAS  Google Scholar 

  14. Liu, Y. et al. Macroporous indium tin oxide electrode layers as conducting substrates for immobilization of bulky electroactive guests. Electrochim. Acta 140, 108–115 (2014).

    Article  CAS  Google Scholar 

  15. Riedel, M. & Lisdat, F. Integration of enzymes in polyaniline-sensitized 3D inverse opal TiO2 architectures for light-driven biocatalysis and light-to-current conversion. ACS Appl. Mater. Interfaces 10, 267–277 (2018).

    Article  CAS  Google Scholar 

  16. Xia, L. et al. Zinc oxide inverse opal electrodes modified by glucose oxidase for electrochemical and photoelectrochemical biosensor. Biosens. Bioelectron. 59, 350–357 (2014).

    Article  CAS  Google Scholar 

  17. Arsenault, E., Soheilnia, N. & Ozin, G. A. Periodic macroporous nanocrystalline antimony-doped tin oxide electrode. ACS Nano 5, 2984–2988 (2011).

    Article  CAS  Google Scholar 

  18. Wenzel, T., Härtter, D., Bombelli, P., Howe, C. J. & Steiner, U. Porous translucent electrodes enhance current generation from photosynthetic biofilms. Nat. Commun. 9, 1299 (2018).

    Article  CAS  Google Scholar 

  19. Fang, X., Kalathil, S., Divitini, G., Wang, Q. & Reisner, E. A three-dimensional hybrid electrode with electroactive microbes for efficient electrogenesis and chemical synthesis. Proc. Natl Acad. Sci. USA 117, 5074–5080 (2020).

    Article  CAS  Google Scholar 

  20. Sturmberg, B. C. P. et al. Modal analysis of enhanced absorption in silicon nanowire arrays. Opt. Express 19, A1067–A1081 (2011).

    Article  CAS  Google Scholar 

  21. Ali, M. et al. Nanostructured photoelectrochemical solar cell for nitrogen reduction using plasmon-enhanced black silicon. Nat. Commun. 7, 11335 (2016).

    Article  CAS  Google Scholar 

  22. Wang, K., Chang, Y.-H., Zhang, C. & Wang, B. Conductive-on-demand: tailorable polyimide/carbon nanotube nanocomposite thin film by dual-material aerosol jet printing. Carbon 98, 397–403 (2016).

    Article  CAS  Google Scholar 

  23. Saleh, M. S., Li, J., Park, J. & Panat, R. 3D printed hierarchically-porous microlattice electrode materials for exceptionally high specific capacity and areal capacity lithium ion batteries. Addit. Manuf. 23, 70–78 (2018).

    CAS  Google Scholar 

  24. Saleh, M. S., Hu, C. & Panat, R. Three-dimensional microarchitected materials and devices using nanoparticle assembly by pointwise spatial printing. Sci. Adv. 3, e1601986 (2017).

    Article  CAS  Google Scholar 

  25. Ćatić, N. et al. Aerosol-jet printing facilitates the rapid prototyping of microfluidic devices with versatile geometries and precise channel functionalization. Appl. Mater. Today 19, 100618 (2020).

    Article  Google Scholar 

  26. Jabari, E. & Toyserkani, E. Micro-scale aerosol-jet printing of graphene interconnects. Carbon 91, 321–329 (2015).

    Article  CAS  Google Scholar 

  27. Sukeshini, A. M. et al. Aerosol jet printing and microstructure of SOFC electrolyte and cathode layers. ECS Trans. 35, 2151 (2011).

    Article  CAS  Google Scholar 

  28. Kalio, A. et al. Development of lead-free silver ink for front contact metallization. Sol. Energy Mater. Sol. Cells 106, 51–54 (2012).

    Article  CAS  Google Scholar 

  29. Lu, S. et al. Flexible, print-in-place 1D–2D thin-film transistors using aerosol jet printing. ACS Nano 13, 11263–11272 (2019).

    Article  CAS  Google Scholar 

  30. Hong, K. et al. Aerosol jet printed, sub-2 V complementary circuits constructed from P- and N-type electrolyte gated transistors. Adv. Mater. 26, 7032–7037 (2014).

    Article  CAS  Google Scholar 

  31. Lin, J.-T. et al. A high-efficiency HIT solar cell with pillar texturing. IEEE J. Photovolt. 8, 669–675 (2018).

    Article  Google Scholar 

  32. Saini, D. K., Pabbi, S. & Shukla, P. Cyanobacterial pigments: perspectives and biotechnological approaches. Food Chem. Toxicol. 120, 616–624 (2018).

    Article  CAS  Google Scholar 

  33. Wey, L. T. et al. A biophotoelectrochemical approach to unravelling the role of cyanobacterial cell structures in exoelectrogenesis. Electrochim. Acta 395, 139214 (2021).

    Article  CAS  Google Scholar 

  34. Clifford, E. R. et al. Phenazines as model low-midpoint potential electron shuttles for photosynthetic bioelectrochemical systems. Chem. Sci. 12, 3328–3338 (2021).

    Article  CAS  Google Scholar 

  35. Torimura, M., Miki, A., Wadano, A., Kano, K. & Ikeda, T. Electrochemical investigation of cyanobacteria Synechococcus sp. PCC7942-catalyzed photoreduction of exogenous quinones and photoelectrochemical oxidation of water. J. Electroanal. Chem. 496, 21–28 (2001).

    Article  CAS  Google Scholar 

  36. Reggente, M., Politi, S., Antonucci, A., Tamburri, E. & Boghossian, A. A. Design of optimized PEDOT-based electrodes for enhancing performance of living photovoltaics based on phototropic bacteria. Adv. Mater. Technol. 5, 1900931 (2020).

    Article  CAS  Google Scholar 

  37. Cereda, A. et al. A bioelectrochemical approach to characterize extracellular electron transfer by Synechocystis sp. PCC6803. PLoS ONE 9, e91484 (2014).

    Article  CAS  Google Scholar 

  38. Zeng, Y. et al. Photoactive conjugated polymer-based hybrid biosystems for enhancing cyanobacterial photosynthesis and regulating redox state of protein. Adv. Funct. Mater. 31, 2007814 (2021).

    Article  CAS  Google Scholar 

  39. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35, 171–205 (1971).

    Article  CAS  Google Scholar 

  40. Lea-Smith, D. J. et al. Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol. 162, 484–495 (2013).

    Article  CAS  Google Scholar 

  41. Yang, C., Zhou, E., Miyanishi, S., Hashimoto, K. & Tajima, K. Preparation of active layers in polymer solar cells by aerosol jet printing. ACS Appl. Mater. Interfaces 3, 4053–4058 (2011).

    Article  CAS  Google Scholar 

  42. Fang, X. et al. Structure–activity relationships of hierarchical three-dimensional electrodes with photosystem II for semiartificial photosynthesis. Nano Lett. 19, 1844–1850 (2019).

    Article  CAS  Google Scholar 

  43. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).

  44. Wei, T. & Simko, V. corrplot: visualization of a correlation matrix. R package version 0.84 (2017).

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This work was supported by the Biotechnology and Biological Sciences Research Council (BB/M011194/1 to J.M.L., BB/R011923/1 to J.Z. and X.C.), the Cambridge Trust (L.T.W.) and the Isaac Newton Trust (SCHERTEL SNSF3 to L.S.). S.K.-N. is grateful for support from a European Research Council (ERC) Starting Grant (ERC-2014-STG-639526, NANOGEN). S.K.-N. and Q.J. acknowledge support from the EPSRC Centre of Advanced Materials for Integrated Energy Systems (CAM-IES) (grant EP/P007767/1). We thank H. Lloyd-Laney and E. Kitson for helpful discussions in statistical analysis. We thank N. Plumeré and H. Li for helpful discussions in electrochemistry. We thank P. J. Bártolo and F. Liu for helpful discussions in 3D bioprinting.

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Authors and Affiliations



J.Z.Z. and X.C. conceived the project and wrote the manuscript. X.C. was the lead experimenter, interpreted the data and produced Figs. 14. J.M.L. helped with the preparation of the manuscript, performed and interpreted the statistical analysis, and produced Fig. 5b. L.T.W. provided biological samples and expertise. L.S. helped to design and carry out and interpret the light transmission/reflection/absorption experiments. Q.J. helped to establish the initial protocol for aerosol jet printing pillars. S.V. helped guide the light experiments. C.J.H. contributed biological expertise and samples. S.K.-N. helped to guide the initial printing experiments. All contributed comments to the manuscript.

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Correspondence to Jenny Z. Zhang.

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Nature Materials thanks Lars Jeuken and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Notes 1–4, Figs. 1–16 and Tables 1–3.

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Chen, X., Lawrence, J.M., Wey, L.T. et al. 3D-printed hierarchical pillar array electrodes for high-performance semi-artificial photosynthesis. Nat. Mater. 21, 811–818 (2022).

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