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Photosynthetic semiconductor biohybrids for solar-driven biocatalysis

Abstract

Photosynthetic semiconductor biohybrids integrate the best attributes of biological whole-cell catalysts and semiconducting nanomaterials. Enzymatic machinery enveloped in its native cellular environment offers exquisite product selectivity and low substrate activation barriers while semiconducting nanomaterials harvest light energy stably and efficiently. In this Review Article, we illustrate the evolution and advances of photosynthetic semiconductor biohybrids focusing on the conversion of CO2 to value-added chemicals. We begin by considering the potential of this nascent field to meet global energy challenges while comparing it to alternate approaches. This is followed by a discussion of the advantageous coupling of electrotrophic organisms with light-active electrodes for solar-to-chemical conversion. We detail the dynamic investigation of photosensitized microorganisms creating direct light harvesting within unicellular organisms while describing complementary developments in the understanding of charge transfer mechanisms and cytoprotection. Lastly, we focus on trends and improvements needed in photosynthetic semiconductor biohybrids in order to address future challenges and enhance their widespread adoption for the production of solar chemicals.

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Fig. 1: Photoelectrochemical semiconductor biohybrids.
Fig. 2: Methods for visualization of light-active nanoparticles on cells.
Fig. 3: Map of photosensitized microorganisms.
Fig. 4: Exploration of charge transfer mechanisms in microbial cells.
Fig. 5: Cytoprotective strategies for unicellular organisms.

References

  1. Sellers, P. J. et al. Comparison of radiative and physiological effects of doubled atmospheric CO2 on climate. Science 271, 1402–1406 (1996).

    Article  CAS  Google Scholar 

  2. Barber, J. Photosynthetic energy conversion: natural and artificial. Chem. Soc. Rev. 38, 185–196 (2009).

    Article  CAS  PubMed  Google Scholar 

  3. Lewis, N. S. Research opportunities to advance solar energy utilization. Science 351, aad1920 (2016).

    Article  CAS  PubMed  Google Scholar 

  4. Cook, T. R. et al. Solar energy supply and storage for the legacy and nonlegacy worlds. Chem. Rev. 110, 6474–6502 (2010).

    Article  CAS  PubMed  Google Scholar 

  5. Nelson, N. & Ben-Shem, A. The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 5, 971–982 (2004).

    Article  PubMed  Google Scholar 

  6. Williams, P. J. L. B. & Laurens, L. M. L. Microalgae as biodiesel & biomass feedstocks: review & analysis of the biochemistry, energetics & economics. Energy Environ. Sci. 3, 554–590 (2010).

    Article  CAS  Google Scholar 

  7. Hill, J., Nelson, E., Tilman, D., Polasky, S. & Tiffany, D. Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc. Natl Acad. Sci. USA 103, 11206–11210 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhu, X.-G., Long, S. P. & Ort, D. R. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 61, 235–261 (2010).

    Article  CAS  PubMed  Google Scholar 

  9. Green, M. A. et al. Solar cell efficiency tables (version 53). Prog. Photovolt. Res. Appl. 27, 3–12 (2019).

    Article  Google Scholar 

  10. Blankenship, R. E. et al. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332, 805–809 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Luo, J. et al. Water photolysis at 12.3% efficiency via perovskite photovoltaics and Earth-abundant catalysts. Science 345, 1593–1596 (2014).

    Article  CAS  PubMed  Google Scholar 

  12. Zhu, X. G., Long, S. P. & Ort, D. R. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr. Opin. Biotechnol. 19, 153–159 (2008).

    Article  CAS  PubMed  Google Scholar 

  13. Mao, J., Li, K. & Peng, T. Recent advances in the photocatalytic CO2 reduction over semiconductors. Catal. Sci. Technol. 3, 2481–2498 (2013).

    Article  CAS  Google Scholar 

  14. Ross, M. B. et al. Designing materials for electrochemical carbon dioxide recycling. Nat. Catal. 2, 648–658 (2019).

    Article  CAS  Google Scholar 

  15. Barton, E. E., Rampulla, D. M. & Bocarsly, A. B. Selective solar-driven reduction of CO2 to methanol using a catalyzed p-GaP based photoelectrochemical cell. J. Am. Chem. Soc. 130, 6342–6344 (2008).

    Article  CAS  PubMed  Google Scholar 

  16. Sahara, G. et al. Photoelectrochemical Reduction of CO2 coupled to water oxidation using a photocathode with a Ru(ii)–Re(i) complex photocatalyst and a CoOx/TaON photoanode. J. Am. Chem. Soc. 138, 14152–14158 (2016).

    Article  CAS  PubMed  Google Scholar 

  17. Zhou, X. et al. Solar-driven reduction of 1 atm of CO2 to formate at 10% energy-conversion efficiency by use of a TiO2-protected iii-v tandem photoanode in conjunction with a bipolar membrane and a Pd/C cathode. ACS Energy Lett. 1, 764–770 (2016).

    Article  CAS  Google Scholar 

  18. Bourzac, K. Liquid sunlight: fuels created by artificial photosynthesis are getting much closer to reality. Proc. Natl Acad. Sci. USA 113, 4545–4548 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kim, D., Sakimoto, K. K., Hong, D. & Yang, P. Artificial photosynthesis for sustainable fuel and chemical production. Angew. Chem. Int. Ed. 54, 3259–3266 (2015).

    Article  CAS  Google Scholar 

  20. Yoshikawa, K. et al. Silicon heterojunction solar cell with interdigitated back contacts for a photoconversion efficiency over 26%. Nat. Energy 2, 17032 (2017).

    Article  CAS  Google Scholar 

  21. Chang, X., Wang, T. & Gong, J. CO2 photo-reduction: insights into CO2 activation and reaction on surfaces of photocatalysts. Energy Environ. Sci. 9, 2177–2196 (2016).

    Article  CAS  Google Scholar 

  22. Kong, Q. et al. Directed assembly of nanoparticle catalysts on nanowire photoelectrodes for photoelectrochemical CO2 reduction. Nano Lett. 16, 5675–5680 (2016).

    Article  CAS  PubMed  Google Scholar 

  23. Varela, A. S., Ju, W., Reier, T. & Strasser, P. Tuning the catalytic activity and selectivity of Cu for CO2 electroreduction in the presence of halides. ACS Catal. 6, 2136–2144 (2016).

    Article  CAS  Google Scholar 

  24. Das, A. & Ljungdahl, L. G. in Biochemistry and Physiology of Anaerobic Bacteria 191–204 (Springer, 2006).

  25. Liang, J.-Y. & Lipscomb, W. N. Binding of substrate CO2 to the active site of human carbonic anhydrase II: a molecular dynamics study (zinc enzyme/binding pathway/enzyme-substrate interaction). Proc. Natl Acad. Sci. USA 87, 3675–3679 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gray, H. B. & Winkler, J. R. Electron transfer in proteins. Annu. Rev. Biochem. 65, 537–561 (1996).

    Article  CAS  PubMed  Google Scholar 

  27. Cooney, M. J., Svoboda, V., Lau, C., Martin, G. & Minteer, S. D. Enzyme catalysed biofuel cells. Energy Environ. Sci. 1, 320–337 (2008).

    Article  CAS  Google Scholar 

  28. Schlager, S. et al. Electrochemical reduction of carbon dioxide to methanol by direct injection of electrons into immobilized enzymes on a modified electrode. ChemSusChem 9, 631–635 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lamle, S. E., Vincent, K. A., Halliwell, L. M., Albracht, S. P. J. & Armstrong, F. A. Hydrogenase on an electrode: a remarkable heterogeneous catalyst. J. Chem. Soc. Dalt. Trans. 3, 4152–4157 (2003).

    Article  Google Scholar 

  30. Pinyou, P., Blay, V., Muresan, L. M. & Noguer, T. Enzyme-modified electrodes for biosensors and biofuel cells. Mater. Horiz. 6, 1336–1358 (2019).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. Sarma, A. K., Vatsyayan, P., Goswami, P. & Minteer, S. D. Recent advances in material science for developing enzyme electrodes. Biosens. Bioelectron. 24, 2313–2322 (2009).

    Article  CAS  PubMed  Google Scholar 

  33. Sakimoto, K. K. et al. Physical Biology of the Materials–Microorganism Interface. J. Am. Chem. Soc. 140, 1978–1985 (2018).

    Article  CAS  PubMed  Google Scholar 

  34. Rabaey, K. & Rozendal, R. A. Microbial electrosynthesis — revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8, 706–716 (2010).

    Article  CAS  PubMed  Google Scholar 

  35. Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016). Comprehensive review of active electron transfer pathways and mechanisms between microorganisms and inorganic minerals.

    Article  CAS  PubMed  Google Scholar 

  36. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M. & Lovley, D. R. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 1, e00103–10 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ragsdale, S. W. & Pierce, E. Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim. Biophys. Acta 1784, 1873–1898 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Aryal, N., Halder, A., Tremblay, P. L., Chi, Q. & Zhang, T. Enhanced microbial electrosynthesis with three-dimensional graphene functionalized cathodes fabricated via solvothermal synthesis. Electrochim. Acta 217, 117–122 (2016).

    Article  CAS  Google Scholar 

  39. Su, L. & Ajo-Franklin, C. M. Reaching full potential: bioelectrochemical systems for storing renewable energy in chemical bonds. Curr. Opin. Biotechnol. 57, 66–72 (2019).

    Article  CAS  PubMed  Google Scholar 

  40. Zhang, T. et al. Improved cathode materials for microbial electrosynthesis. Energy Environ. Sci. 6, 217–224 (2013).

    Article  CAS  Google Scholar 

  41. Tremblay, P. L., Höglund, D., Koza, A., Bonde, I. & Zhang, T. Adaptation of the autotrophic acetogen Sporomusa ovata to methanol accelerates the conversion of CO2 to organic products. Sci. Rep. 5, 16168 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Marshall, C. W., Ross, D. E., Fichot, E. B., Norman, R. S. & May, H. D. Long-term operation of microbial electrosynthesis systems improves acetate production by autotrophic microbiomes. Environ. Sci. Technol. 47, 6023–6029 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Li, H. et al. Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335, 1596 (2012).

    Article  CAS  PubMed  Google Scholar 

  44. Liu, C. et al. Nanowire-bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett. 15, 3634–3639 (2015). This work demonstrates the ability to pair acetogenic microorganisms with light-active nanostructured electrodes for CO 2 reduction.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Shively, J. M., van Keulen, G. & Meijer, W. G. Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu. Rev. Microbiol. 52, 191–230 (1998).

    Article  CAS  PubMed  Google Scholar 

  46. Wang, H. & Ren, Z. J. A comprehensive review of microbial electrochemical systems as a platform technology. Biotechnol. Adv. 31, 1796–1807 (2013).

    Article  CAS  PubMed  Google Scholar 

  47. Nichols, E. M. et al. Hybrid bioinorganic approach to solar-to-chemical conversion. Proc. Natl Acad. Sci. USA 112, 11461–11466 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Liu, C., Colón, B. C., Ziesack, M., Silver, P. A. & Nocera, D. G. Water splitting–biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352, 1210–1213 (2016). The authors present a highly energy efficient device consisting of self-regenerating non-toxic electrodes and CO 2-fixing bacteria for production of bioplastics and biofuels.

    Article  CAS  PubMed  Google Scholar 

  49. Dogutan, D. K. & Nocera, D. G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis. Acc. Chem. Res. 52, 3143–3148 (2019).

    Article  CAS  PubMed  Google Scholar 

  50. Liu, C., Sakimoto, K. K., Colón, B. C., Silver, P. A. & Nocera, D. G. Ambient nitrogen reduction cycle using a hybrid inorganic–biological system. Proc. Natl Acad. Sci. USA 114, 6450–6455 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Rodrigues, R. M. et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction. Nat. Catal. 2, 407–414 (2019).

    Article  CAS  Google Scholar 

  52. Quintana, N., Van Der Kooy, F., Van De Rhee, M. D., Voshol, G. P. & Verpoorte, R. Renewable energy from Cyanobacteria: Energy production optimization by metabolic pathway engineering. Appl. Microbiol. Biotechnol. 91, 471–490 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Utschig, L. M., Soltau, S. R., Mulfort, K. L., Niklas, J. & Poluektov, O. G. Z-scheme solar water splitting: via self-assembly of photosystem I–catalyst hybrids in thylakoid membranes. Chem. Sci. 9, 8504–8512 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Brown, K. A. et al. Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid. Science 352, 448–450 (2016).

    Article  CAS  PubMed  Google Scholar 

  55. Fast, A. G. & Papoutsakis, E. T. Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr. Opin. Chem. Eng. 1, 380–395 (2012).

    Article  Google Scholar 

  56. Sakimoto, K. K., Wong, A. B. & Yang, P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2016). This work illustrates the concept of membrane-bound self-precipitated quantum dots to power CO 2 fixation of live whole-cell biocatalysts.

    Article  CAS  PubMed  Google Scholar 

  57. Sweeney, R. Y. et al. Bacterial biosynthesis of cadmium sulfide nanocrystals. Chem. Biol. 11, 1553–1559 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. Oguri, T., Schneider, B. & Reitzer, L. Cysteine catabolism and cysteine desulfhydrase (CdsH/STM0458) in Salmonella enterica serovar typhimurium. J. Bacteriol. 194, 4366–4376 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Drake, H. L. & Daniel, S. L. Physiology of the thermophilic acetogen Moorella thermoacetica. Res. Microbiol. 155, 869–883 (2004).

    Article  PubMed  Google Scholar 

  60. Kloepfer, J. A., Mielke, R. E. & Nadeau, J. L. Uptake of CdSe and CdSe/ZnS quantum dots into bacteria via purine-dependent mechanisms. Appl. Environ. Microbiol. 71, 2548–2557 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Goldberg, M., Langer, R. & Jia, X. Nanostructured materials for applications in drug delivery and tissue engineering. J. Biomater. Sci. Polym. Ed. 18, 241–268 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang, B., Jiang, Z., Yu, J. C., Wang, J. & Wong, P. K. Enhanced CO2 reduction and valuable C2+ chemical production by a CdS-photosynthetic hybrid system. Nanoscale 11, 9296–9301 (2019).

    Article  CAS  PubMed  Google Scholar 

  63. Chen, M. et al. Light-driven nitrous oxide production via autotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Environ. Int. 127, 353–360 (2019).

    Article  CAS  PubMed  Google Scholar 

  64. Begg, S. L. et al. Dysregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae. Nat. Commun. 6, 6418 (2015).

    Article  CAS  PubMed  Google Scholar 

  65. Li, K. G. et al. Intracellular oxidative stress and cadmium ions release induce cytotoxicity of unmodified cadmium sulfide quantum dots. Toxicol. Vitr. 23, 1007–1013 (2009).

    Article  CAS  Google Scholar 

  66. Godt, J. et al. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 1, 22 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Jin, R., Zeng, C., Zhou, M. & Chen, Y. Atomically precise colloidal metal nanoclusters and nanoparticles: fundamentals and opportunities. Chem. Rev. 116, 10346–10413 (2016).

    Article  CAS  PubMed  Google Scholar 

  68. Zhou, M. et al. Three-orders-of-magnitude variation of carrier lifetimes with crystal phase of gold nanoclusters. Science 364, 279–282 (2019).

    Article  CAS  PubMed  Google Scholar 

  69. Santiago-Gonzalez, B. et al. Permanent excimer superstructures by supramolecular networking of metal quantum clusters. Science 353, 571–575 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. Zhao, S. et al. Gold nanoclusters promote electrocatalytic water oxidation at the nanocluster/CoSe2 interface. J. Am. Chem. Soc. 139, 1077–1080 (2017).

    Article  CAS  PubMed  Google Scholar 

  71. Zeng, C. et al. Structural patterns at all scales in a nonmetallic chiral Au133(SR)52 nanoparticle. Sci. Adv. 1, e1500045 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Stamplecoskie, K. G. & Swint, A. Optimizing molecule-like gold clusters for light energy conversion. J. Mater. Chem. A 4, 2075–2081 (2016).

    Article  CAS  Google Scholar 

  73. Chen, Y. S., Choi, H. & Kamat, P. V. Metal-cluster-sensitized solar cells. A new class of thiolated gold sensitizers delivering efficiency greater than 2%. J. Am. Chem. Soc. 135, 8822–8825 (2013).

    Article  CAS  PubMed  Google Scholar 

  74. Yu, Y. et al. Identification of a highly luminescent Au22(SG)18 nanocluster. J. Am. Chem. Soc. 136, 1246–1249 (2014).

    Article  CAS  PubMed  Google Scholar 

  75. Zhang, H. et al. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat. Nanotechnol. 13, 900–905 (2018). Demonstrates that biocompatible gold nanoclusters can be used to photosensitize CO 2-fixing bacteria.

    Article  CAS  PubMed  Google Scholar 

  76. Cestellos-Blanco, S., Zhang, H. & Yang, P. Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids. Faraday Discuss. 215, 54–65 (2019).

    Article  CAS  PubMed  Google Scholar 

  77. Schuchmann, K. & Müller, V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 12, 809–821 (2014).

    Article  CAS  PubMed  Google Scholar 

  78. Liu, T. & Khosla, C. Genetic engineering of Escherichia coli for biofuel production. Annu. Rev. Genet. 44, 53–69 (2010).

    Article  CAS  PubMed  Google Scholar 

  79. Luo, X. et al. Complete biosynthesis of cannabinoids and their unnatural analogues in yeast. Nature 567, 123–126 (2019).

    Article  CAS  PubMed  Google Scholar 

  80. Wei, W. et al. A surface-display biohybrid approach to light-driven hydrogen production in air. Sci. Adv. 4, eaap9253 (2018). The authors illustrate the use of cadmium sulfide quantum dots to provide hydrogenase within E. coli with reducing equivalents for H 2 production.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Krassen, H. et al. Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase. ACS Nano 3, 4055–4061 (2009).

    Article  CAS  PubMed  Google Scholar 

  82. Guo, J. et al. Light-driven fine chemical production in yeast biohybrids. Science 362, 813–816 (2018). In this study genetically modified yeast were enhanced with light-active indium phosphide nanoparticles in order to improve the production of shikimic acid.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ding, Y. et al. Nanorg microbial factories: light-driven renewable biochemical synthesis using quantum dot-bacteria nanobiohybrids. J. Am. Chem. Soc. 141, 10272–10282 (2019). This work broadly demonstrates that matching the band gap of semiconducting quantum dots with the redox potential of enzyme allows for efficient solar-to-chemical production.

    Article  CAS  PubMed  Google Scholar 

  84. Lovley, D. R. & Nevin, K. P. Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr. Opin. Biotechnol. 24, 385–390 (2013).

    Article  CAS  PubMed  Google Scholar 

  85. Lovley, D. R. Electromicrobiology. Annu. Rev. Microbiol 66, 391–409 (2012).

    Article  CAS  PubMed  Google Scholar 

  86. Virdis, B. et al. Analysis of electron transfer dynamics in mixed community electroactive microbial biofilms. RSC Adv. 6, 3650–3660 (2016).

    Article  CAS  Google Scholar 

  87. Kracke, F., Vassilev, I. & Krömer, J. O. Microbial electron transport and energy conservation: the foundation for optimizing bioelectrochemical systems. Front. Microbiol. 6, 575 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Light, S. H. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140–157 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Fukushima, T. et al. The molecular basis for binding of an electron transfer protein to a metal oxide surface. J. Am. Chem. Soc. 139, 12647–12654 (2017).

    Article  CAS  PubMed  Google Scholar 

  90. Deutzmann, J. S., Sahin, M. & Spormann, A. M. Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. mBio 6, e00496–15 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).

    Article  CAS  PubMed  Google Scholar 

  92. Wang, F. et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell 177, 361–369 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kornienko, N. et al. Spectroscopic elucidation of energy transfer in hybrid inorganic-biological organisms for solar-to-chemical production. Proc. Natl Acad. Sci. USA 113, 11750–11755 (2016). Determined that photosensitized bacteria exhibit spectroscopic changes that allow the authors to propose charge transfer pathways.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zhang, R. et al. Proteomic and metabolic elucidation of solar-powered biomanufacturing by bio-abiotic hybrid system. Chem 6, P234–249 (2019). This study elucidates charge transfer mechanisms of photosensitized bacteria by examining proteomics and metabolomics.

    Article  Google Scholar 

  95. Sakimoto, K. K., Kornienko, N. & Yang, P. Cyborgian material design for solar fuel production: the emerging photosynthetic biohybrid systems. Acc. Chem. Res. 50, 476–481 (2017).

    Article  CAS  PubMed  Google Scholar 

  96. Lambertz, C. et al. O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J. Biol. Chem. 286, 40614–40623 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Sakimoto, K. K., Zhang, S. J. & Yang, P. Cysteine-cystine photoregeneration for oxygenic photosynthesis of acetic acid from CO2 by a tandem inorganic-biological hybrid system. Nano Lett. 16, 5883–5887 (2016).

    Article  CAS  PubMed  Google Scholar 

  98. Hirakawa, K., Mori, M., Yoshida, M., Oikawa, S. & Kawanishi, S. Photo-irradiated titanium dioxide catalyzes site specific DNA damage via generation of hydrogen peroxide. Free Radic. Res. 38, 439–447 (2004).

    Article  CAS  PubMed  Google Scholar 

  99. Mishra, M., Arukha, A. P., Bashir, T., Yadav, D. & Prasad, G. B. K. S. All new faces of diatoms: potential source of nanomaterials and beyond. Front. Microbiol. 8, 1239 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Ehling-Schulz, M. & Scherer, S. UV protection in cyanobacteria. Eur. J. Phycol. 34, 329–338 (1999).

    Article  Google Scholar 

  101. Shchukin, D. G., Shutava, T., Shchukina, E., Sukhorukov, G. B. & Lvov, Y. M. Modified polyelectrolyte microcapsules as smart defense systems. Chem. Mater. 16, 3446–3451 (2004).

    Article  CAS  Google Scholar 

  102. Yang, S. H., Ko, E. H. & Choi, I. S. Cytocompatible encapsulation of individual chlorella cells within titanium dioxide shells by a designed catalytic peptide. Langmuir 28, 2151–2155 (2012).

    Article  CAS  PubMed  Google Scholar 

  103. Yang, S. H. et al. Biomimetic encapsulation of individual cells with silica. Angew. Chem. Int. Ed. 48, 9160–9163 (2009).

    Article  CAS  Google Scholar 

  104. Liang, K. et al. Metal–organic framework coatings as cytoprotective exoskeletons for living cells. Adv. Mater. 28, 7910–7914 (2016).

    Article  CAS  PubMed  Google Scholar 

  105. Park, J. H. et al. Nanocoating of single cells: from maintenance of cell viability to manipulation of cellular activities. Adv. Mater. 26, 2001–2010 (2014).

    Article  CAS  PubMed  Google Scholar 

  106. Allan-Wojtas, P., Truelstrup Hansen, L. & Paulson, A. T. Microstructural studies of probiotic bacteria-loaded alginate microcapsules using standard electron microscopy techniques and anhydrous fixation. LWT Food Sci. Technol. 41, 101–108 (2008).

    Article  CAS  Google Scholar 

  107. Thankam Finosh, G. & Jayabalan, M. Reactive oxygen species—Control and management using amphiphilic biosynthetic hydrogels for cardiac applications. Adv. Biosci. Biotechnol. 4, 1134–1146 (2013).

    Article  CAS  Google Scholar 

  108. Kim, B. J. et al. Control of microbial growth in alginate/polydopamine core/shell microbeads. Chem. Asian J. 10, 2130–2133 (2015).

    Article  CAS  PubMed  Google Scholar 

  109. Cestellos-Blanco, S., Zhang, H. & Yang, P. Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids. Faraday Discuss. 215, 54–65 (2019).

    Article  CAS  PubMed  Google Scholar 

  110. Zhou, H.-C., Long, J. R. & Yaghi, O. M. Introduction to metal–organic frameworks. Chem. Rev. 112, 673–674 (2012).

    Article  CAS  PubMed  Google Scholar 

  111. Liang, K. et al. An enzyme-coated metal–organic framework shell for synthetically adaptive cell survival. Angew. Chem. Int. Ed. 56, 8510–8515 (2017).

    Article  CAS  Google Scholar 

  112. Zhan, W. et al. Semiconductor@metal–organic framework core–shell heterostructures: a case of ZnO@ZIF-8 nanorods with selective photoelectrochemical response. J. Am. Chem. Soc. 135, 1926–1933 (2013).

    Article  CAS  PubMed  Google Scholar 

  113. Kornienko, N. et al. Metal–organic frameworks for electrocatalytic reduction of carbon dioxide. J. Am. Chem. Soc. 137, 14129–14135 (2015).

    Article  CAS  PubMed  Google Scholar 

  114. Ji, Z., Zhang, H., Liu, H., Yaghi, O. M. & Yang, P. Cytoprotective metal-organic frameworks for anaerobic bacteria. Proc. Natl Acad. Sci. USA 115, 10582–10587 (2018). A two-dimensional zirconium-based MOF nanosheet can be used to protect bacteria from oxygen and ROS.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Robertson, S. J., Grattieri, M., Behring, J., Bestetti, M. & Minteer, S. D. Transitioning from batch to flow hypersaline microbial fuel cells. Electrochim. Acta 317, 494–501 (2019).

    Article  CAS  Google Scholar 

  116. Smith, M. J. & Francis, M. B. A designed A. vinelandii–S. elongatus coculture for chemical photoproduction from air, water, phosphate, and trace metals. ACS Synth. Biol. 5, 955–961 (2016).

    Article  CAS  PubMed  Google Scholar 

  117. Angelis, S. et al. Co-culture of microalgae, cyanobacteria, and macromycetes for exopolysaccharides production: process preliminary optimization and partial characterization. Appl. Biochem. Biotechnol. 167, 1092–1106 (2012).

    Article  CAS  PubMed  Google Scholar 

  118. Marshall, C. W., Ross, D. E., Fichot, E. B., Norman, R. S. & May, H. D. Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl. Environ. Microbiol. 78, 8412–8420 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Jia, J. et al. Solar water splitting by photovoltaic-electrolysis with a solar-to-hydrogen efficiency over 30%. Nat. Commun. 7, 13237 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. McNeely, K., Xu, Y., Bennette, N., Bryant, D. A. & Dismukes, G. C. Redirecting reductant flux into hydrogen production via metabolic engineering of fermentative carbon metabolism in a cyanobacterium. Appl. Environ. Microbiol. 76, 5032–5038 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Atsumi, S., Higashide, W. & Liao, J. C. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat. Biotechnol. 27, 1177–1180 (2009).

    Article  CAS  PubMed  Google Scholar 

  122. Antonovsky, N. et al. Sugar synthesis from CO2 in Escherichia coli. Cell 166, 115–125 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kung, Y., Runguphan, W. & Keasling, J. D. From fields to fuels: recent advances in the microbial production of biofuels. ACS Synth. Biol. 1, 498–513 (2012).

    Article  CAS  PubMed  Google Scholar 

  124. Liao, J. C., Mi, L., Pontrelli, S. & Luo, S. Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat. Rev. Microbiol. 14, 288–304 (2016).

    Article  CAS  PubMed  Google Scholar 

  125. Lu, Z.-X. et al. Cell damage induced by photocatalysis of TiO2 thin films. Langmuir 19, 8765–8768 (2003).

    Article  CAS  Google Scholar 

  126. Chan, C. H., Levar, C. E., Jiménez-Otero, F. & Bond, D. R. Genome scale mutational analysis of geobacter sulfurreducens reveals distinct molecular mechanisms for respiration and sensing of poised electrodes versus Fe(iii) oxides. J. Bacteriol. 199, e00340–17 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Ha, C.-S. & Gardella, J. A. Surface chemistry of biodegradable polymers for drug delivery systems. Chem. Rev. 105, 4205–4232 (2005).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by NASA, Center for the Utilization of Biological Engineering in Space, under award NNX17AJ31G. S.C.-B. acknowledges a fellowship from the Philomathia Foundation. H.Z. is supported by the Suzhou Industry Park Fellowship and J.M.K. is supported by the Kwanjeong Educational Foundation.

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Cestellos-Blanco, S., Zhang, H., Kim, J.M. et al. Photosynthetic semiconductor biohybrids for solar-driven biocatalysis. Nat Catal 3, 245–255 (2020). https://doi.org/10.1038/s41929-020-0428-y

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