Journal Home > Volume 17 , Issue 2
Nano Research 2024, 17(2): 866-874 https://doi.org/10.1007/s12274-023-6396-1
Research Article | Issue | Published: 25 January 2024

Polydopamine-coated photoautotrophic bacteria for improving extracellular electron transfer in living photovoltaics

Show Author's Information Melania Reggente1( ),  Charlotte Roullier1,  Mohammed Mouhib1,  Patricia Brandl1,  Hanxuan Wang1,  Stefano Tacconi2,  Francesco Mura3,  Luciana Dini2,  Rossella Labarile4,  Massimo Trotta4,  Fabian Fischer5,6,  Ardemis A. Boghossian1( )
Institute of Chemical Sciences and Engineering (ISIC), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland
Department of Biology and Biotechnology Charles Darwin, Sapienza University of Rome, Rome 00185, Italy
Research Center on Nanotechnology Applied for Engineering of Sapienza (CNIS), University of Rome Sapienza, Rome 00185, Italy
CNR-IPCF Consiglio Nazionale delle Ricerche – Istituto per i Processi Chimico Fisici, Bari 70126, Italy
Institute of Life Technologies, HES-SO Valais-Wallis, Sion 1950, Switzerland
Institute for Renewable Energy, HES-SO Valais-Wallis, Sion 1950, Switzerland
Keywords:
bioelectronics, polydopamine, biophotovoltaics, cyanobacteria, adherence, photosynthetic bacteria
Topics:
Bacteria BiocompatibilityBioelectric phenomenaBiomaterials BiopolymersBiosynthesisBiotechnologyNanobiotechnology
Cite this article:
Reggente M, Roullier C, Mouhib M, et al. Polydopamine-coated photoautotrophic bacteria for improving extracellular electron transfer in living photovoltaics. Nano Research, 2024, 17(2): 866-874. https://doi.org/10.1007/s12274-023-6396-1
Download citation
EndNote(RIS)
BibTeX

610

Views

64

Downloads

Citations

2

Crossref

1

WoS

2

Scopus

0

CSCD

Abstract Full text Electronic supplementary material About this article

Living photovoltaics are microbial electrochemical devices that use whole cell–electrode interactions to convert solar energy to electricity. The bottleneck in these technologies is the limited electron transfer between the microbe and the electrode surface. This study focuses on enhancing this transfer by engineering a polydopamine (PDA) coating on the outer membrane of the photosynthetic microbe Synechocystis sp. PCC6803. This coating provides a conductive nanoparticle shell to increase electrode adhesion and improve microbial charge extraction. A combination of scanning electron microscopy (SEM), transmission electron microscopy (TEM), UV–Vis absorption, and Raman spectroscopy measurements were used to characterize the nanoparticle shell under various synthesis conditions. The cell viability and activity were further assessed through oxygen evolution, growth curve, and confocal fluorescence microscopy measurements. The results show sustained cell growth and detectable PDA surface coverage under slightly alkaline conditions (pH 7.5) and at low initial dopamine (DA) concentrations (1 mM). The exoelectrogenicity of the cells prepared under these conditions was also characterized through cyclic voltammetry (CV) and chronoamperometry (CA). The measurements show a three-fold enhancement in the photocurrent at an applied bias of 0.3 V (vs. Ag/AgCl [3 M KCl]) compared to non-coated cells. This study thus lays the framework for engineering the next generation of living photovoltaics with improved performances using biosynthetic electrodes.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

Polydopamine-coated photoautotrophic bacteria for improving extracellular electron transfer in living photovoltaics

Show Author's information Melania Reggente1( ), Charlotte Roullier1, Mohammed Mouhib1, Patricia Brandl1, Hanxuan Wang1, Stefano Tacconi2, Francesco Mura3, Luciana Dini2, Rossella Labarile4, Massimo Trotta4, Fabian Fischer5,6, Ardemis A. Boghossian1( )
Institute of Chemical Sciences and Engineering (ISIC), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland
Department of Biology and Biotechnology Charles Darwin, Sapienza University of Rome, Rome 00185, Italy
Research Center on Nanotechnology Applied for Engineering of Sapienza (CNIS), University of Rome Sapienza, Rome 00185, Italy
CNR-IPCF Consiglio Nazionale delle Ricerche – Istituto per i Processi Chimico Fisici, Bari 70126, Italy
Institute of Life Technologies, HES-SO Valais-Wallis, Sion 1950, Switzerland
Institute for Renewable Energy, HES-SO Valais-Wallis, Sion 1950, Switzerland

Abstract

Living photovoltaics are microbial electrochemical devices that use whole cell–electrode interactions to convert solar energy to electricity. The bottleneck in these technologies is the limited electron transfer between the microbe and the electrode surface. This study focuses on enhancing this transfer by engineering a polydopamine (PDA) coating on the outer membrane of the photosynthetic microbe Synechocystis sp. PCC6803. This coating provides a conductive nanoparticle shell to increase electrode adhesion and improve microbial charge extraction. A combination of scanning electron microscopy (SEM), transmission electron microscopy (TEM), UV–Vis absorption, and Raman spectroscopy measurements were used to characterize the nanoparticle shell under various synthesis conditions. The cell viability and activity were further assessed through oxygen evolution, growth curve, and confocal fluorescence microscopy measurements. The results show sustained cell growth and detectable PDA surface coverage under slightly alkaline conditions (pH 7.5) and at low initial dopamine (DA) concentrations (1 mM). The exoelectrogenicity of the cells prepared under these conditions was also characterized through cyclic voltammetry (CV) and chronoamperometry (CA). The measurements show a three-fold enhancement in the photocurrent at an applied bias of 0.3 V (vs. Ag/AgCl [3 M KCl]) compared to non-coated cells. This study thus lays the framework for engineering the next generation of living photovoltaics with improved performances using biosynthetic electrodes.

Keywords: bioelectronics, polydopamine, biophotovoltaics, cyanobacteria, adherence, photosynthetic bacteria

References(59)

[1]

McCormick, A. J.; Bombelli, P.; Bradley, R. W.; Thorne, R.; Wenzel, T.; Howe, C. J. Biophotovoltaics: Oxygenic photosynthetic organisms in the world of bioelectrochemical systems. Energy Environ. Sci. 2015, 8, 1092–1109.
DOI Google Scholar
[2]

Mouhib, M.; Antonucci, A.; Reggente, M.; Amirjani, A.; Gillen, A. J.; Boghossian, A. A. Enhancing bioelectricity generation in microbial fuel cells and biophotovoltaics using nanomaterials. Nano Res. 2019, 12, 2184–2199.
DOI Google Scholar
[3]

Schuergers, N.; Werlang, C.; Ajo-Franklin, C. M.; Boghossian, A. A. A synthetic biology approach to engineering living photovoltaics. Energy Environ. Sci. 2017, 10, 1102–1115.
DOI Google Scholar
[4]

Tschörtner, J.; Lai, B.; Krömer, J. O. Biophotovoltaics: Green power generation from sunlight and water. Front. Microbiol. 2019, 10, 866.
DOI Google Scholar
[5]

Wey, L. T.; Bombelli, P.; Chen, X. L.; Lawrence, J. M.; Rabideau, C. M.; Rowden, S. J.; Zhang, Z.; Howe, C. J. The development of biophotovoltaic systems for power generation and biological analysis. ChemElectroChem 2019, 6, 5375–5386.
DOI Google Scholar
[6]

Lea-Smith, D. J.; Bombelli, P.; Vasudevan, R.; Howe, C. J. Photosynthetic, respiratory and extracellular electron transport pathways in cyanobacteria. Biochim. Biophys. Acta 2016, 1857, 247–255.
DOI Google Scholar
[7]

Tanaka, K.; Kashiwagi, N.; Ogawa, T. Effects of light on the electrical output of bioelectrochemical fuel-cells containing Anabaena variabilis M-2: Mechanism of the post-illumination burst. J. Chem. Technol. Biotechnol. 1988, 42, 235–240.
DOI Google Scholar
[8]

Pisciotta, J. M.; Zou, Y. J.; Baskakov, I. V. Light-dependent electrogenic activity of cyanobacteria. PLoS One 2010, 5, e10821.
DOI Google Scholar
[9]

Pisciotta, J. M.; Zou, Y. J.; Baskakov, I. V. Role of the photosynthetic electron transfer chain in electrogenic activity of cyanobacteria. Appl. Microbiol. Biotechnol. 2011, 91, 377–385.
DOI Google Scholar
[10]

Saper, G.; Kallmann, D.; Conzuelo, F.; Zhao, F. Y.; Tóth, T. N.; Liveanu, V.; Meir, S.; Szymanski, J.; Aharoni, A.; Schuhmann, W. et al. Live cyanobacteria produce photocurrent and hydrogen using both the respiratory and photosynthetic systems. Nat. Commun. 2018, 9, 2168.
DOI Google Scholar
[11]
Mouhib, M.; Reggente, M.; Li, L.; Schuergers, N.; Boghossian, A. A. Tailored extracellular electron transfer pathways enhance the electroactivity of Escherichia coli. bioRxiv 2021 , https://www.biorxiv.org/content/10.1101/2021.08.28.458029v1 (accessed Jun 19, 2023).
DOI
[12]

Longatte, G.; Rappaport, F.; Wollman, F. A.; Guille-Collignon, M.; Lemaître, F. Electrochemical harvesting of photosynthetic electrons from unicellular algae population at the preparative scale by using 2, 6-dichlorobenzoquinone. Electrochim. Acta 2017, 236, 337–342.
DOI Google Scholar
[13]

Bombelli, P.; Zarrouati, M.; Thorne, R. J.; Schneider, K.; Rowden, S. J. L.; Ali, A.; Yunus, K.; Cameron, P. J.; Fisher, A. C.; Ian Wilson, D.; et al. Surface morphology and surface energy of anode materials influence power outputs in a multi-channel mediatorless bio-photovoltaic (BPV) system. Phys. Chem. Chem. Phys. 2012, 14, 12221–12229.
DOI Google Scholar
[14]

Liu, L.; Choi, S. Self-sustainable, high-power-density bio-solar cells for lab-on-a-chip applications. Lab Chip 2017, 17, 3817–3825.
DOI Google Scholar
[15]

Wenzel, T.; Härtter, D.; Bombelli, P.; Howe, C. J.; Steiner, U. Porous translucent electrodes enhance current generation from photosynthetic biofilms. Nat. Commun. 2018, 9, 1299.
DOI Google Scholar
[16]

Hasan, K.; Yildiz, H. B.; Sperling, E.; Conghaile, P. Ó.; Packer, M. A.; Leech, D.; Hägerhäll, C.; Gorton, L. Photo-electrochemical communication between cyanobacteria ( Leptolyngbia sp) and osmium redox polymer modified electrodes. Phys. Chem. Chem. Phys. 2014, 16, 24676–24680.
DOI Google Scholar
[17]

Hasan, K.; Çevik, E.; Sperling, E.; Packer, M. A.; Leech, D.; Gorton, L. Photoelectrochemical wiring of Paulschulzia pseudovolvox (algae) to osmium polymer modified electrodes for harnessing solar energy. Adv. Energy Mater. 2015, 5, 1501100.
DOI Google Scholar
[18]

Hasan, K.; Grippo, V.; Sperling, E.; Packer, M. A.; Leech, D.; Gorton, L. Evaluation of photocurrent generation from different photosynthetic organisms. ChemElectroChem 2017, 4, 412–417.
DOI Google Scholar
[19]

Sekar, N.; Umasankar, Y.; Ramasamy, R. P. Photocurrent generation by immobilized cyanobacteria via direct electron transport in photo-bioelectrochemical cells. Phys. Chem. Chem. Phys. 2014, 16, 7862–7871.
DOI Google Scholar
[20]

Zou, Y. J.; Pisciotta, J.; Billmyre, R. B.; Baskakov, I. V. Photosynthetic microbial fuel cells with positive light response. Biotechnol. Bioeng. 2009, 104, 939–946.
DOI Google Scholar
[21]

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. 2020, 5, 1900931.
DOI Google Scholar
[22]
Chen, X. L.; Lawrence, J. M.; Wey, L. T.; Schertel, L.; Jing, Q. S.; Vignolini, S.; Howe, C. J.; Kar-Narayan, S.; Zhang, J. Z. 3D-printed hierarchical pillar array electrodes for high-performance semi-artificial photosynthesis. Nat. Mater. 2022 , 21, 811–818.
DOI
[23]

Roullier, C.; Reggente, M.; Gilibert, P.; Boghossian, A. A. Polypyrrole electrodes show strain-specific enhancement of photocurrent from cyanobacteria. Adv. Mater. Technol. 2023, 8, 2201839.
DOI Google Scholar
[24]

Clifford, E. R.; Bradley, R. W.; Wey, L. T.; Lawrence, J. M.; Chen, X. L.; Howe, C. J.; Zhang, J. Z. Phenazines as model low-midpoint potential electron shuttles for photosynthetic bioelectrochemical systems. Chem. Sci. 2021, 12, 3328–3338.
DOI Google Scholar
[25]

Sekar, N.; Jain, R.; Yan, Y. J.; Ramasamy, R. P. Enhanced photo-bioelectrochemical energy conversion by genetically engineered cyanobacteria. Biotechnol. Bioeng. 2016, 113, 675–679.
DOI Google Scholar
[26]
Reggente, M.; Schurgers, N.; Mouhib, M.; Politi, S.; Antonucci, A.; Boghossian, A. A. Living photovoltaics based on recombinant expression of MtrA decaheme in photosynthetic bacteria. bioRxiv 2023.
DOI
[27]

Meng, H. K.; Zhang, W.; Zhu, H. W.; Yang, F.; Zhang, Y. P.; Zhou, J.; Li, Y. Over-expression of an electron transport protein OmcS provides sufficient NADH for D-lactate production in cyanobacterium. Biotechnol. Biofuels 2021, 14, 109.
DOI Google Scholar
[28]

Antonucci, A.; Reggente, M.; Roullier, C.; Gillen, A. J.; Schuergers, N.; Zubkovs, V.; Lambert, B. P.; Mouhib, M.; Carata, E.; Dini, L. et al. Carbon nanotube uptake in cyanobacteria for near-infrared imaging and enhanced bioelectricity generation in living photovoltaics. Nat. Nanotechnol. 2022, 17, 1111–1119.
DOI Google Scholar
[29]

Liu, L.; Choi, S. Enhanced biophotoelectricity generation in cyanobacterial biophotovoltaics with intracellularly biosynthesized gold nanoparticles. J. Power Sources 2021, 506, 230251.
DOI Google Scholar
[30]

Wang, S.; Guo, Z. G. Bio-inspired encapsulation and functionalization of living cells with artificial shells. Colloids Surf. B Biointerfaces 2014, 113, 483–500.
DOI Google Scholar
[31]

Yang, S. H.; Lee, K. B.; Kong, B.; Kim, J. H.; Kim, H. S.; Choi, I. S. Biomimetic encapsulation of individual cells with silica. Angew. Chem., Int. Ed. 2009, 48, 9160–9163.
DOI Google Scholar
[32]

Fakhrullin, R. F.; Minullina, R. T. Hybrid cellular-inorganic core-shell microparticles: Encapsulation of individual living cells in calcium carbonate microshells. Langmuir 2009, 25, 6617–6621.
DOI Google Scholar
[33]

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 2012, 28, 2151–2155.
DOI Google Scholar
[34]

Apetrei, R. M.; Carac, G.; Bahrim, G.; Ramanaviciene, A.; Ramanavicius, A. Modification of Aspergillus niger by conducting polymer, Polypyrrole, and the evaluation of electrochemical properties of modified cells. Bioelectrochemistry 2018, 121, 46–55.
DOI Google Scholar
[35]

Song, R. B.; Wu, Y. C.; Lin, Z. Q.; Xie, J.; Tan, C. H.; Loo, J. S. C.; Cao, B.; Zhang, J. R.; Zhu, J. J.; Zhang, Q. C. Living and conducting: Coating individual bacterial cells with in situ formed polypyrrole. Angew. Chem. 2017, 129, 10652–10656.
DOI Google Scholar
[36]

Labarile, R.; Varsalona, M.; Vona, D.; Stufano, P.; Grattieri, M.; Farinola, G. M.; Trotta, M. A novel route for anoxygenic polymerization of dopamine via purple photosynthetic bacteria metabolism. MRS Adv. 2023, 8, 423–428.
DOI Google Scholar
[37]

Liu, Y. L.; Ai, K. L.; Lu, L. H. Polydopamine and its derivative materials: Synthesis and promising applications in energy, environmental, and biomedical fields. Chem. Rev. 2014, 114, 5057–5115.
DOI Google Scholar
[38]

Kim, J. H.; Lee, M.; Park, C. B. Polydopamine as a biomimetic electron gate for artificial photosynthesis. Angew. Chem. 2014, 126, 6482–6486.
DOI Google Scholar
[39]

Du, Q.; Li, T.; Li, N.; Wang, X. Protection of electroactive biofilm from extreme acid shock by polydopamine encapsulation. Environ. Sci. Technol. Lett. 2017, 4, 345–349.
DOI Google Scholar
[40]

Yang, S. H.; Kang, S. M.; Lee, K. B.; Chung, T. D.; Lee, H.; Choi, I. S. Mussel-inspired encapsulation and functionalization of individual yeast cells. J. Am. Chem. Soc. 2011, 133, 2795–2797.
DOI Google Scholar
[41]

Dreyer, D. R.; Miller, D. J.; Freeman, B. D.; Paul, D. R.; Bielawski, C. W. Perspectives on poly(dopamine). Chem. Sci. 2013, 4, 3796–3802.
DOI Google Scholar
[42]

Wang, L.; Hu, Z. Y.; Yang, X. Y.; Zhang, B. B.; Geng, W.; van Tendeloo, G.; Su, B. L. Polydopamine nanocoated whole-cell asymmetric biocatalysts. Chem. Commun. 2017, 53, 6617–6620.
DOI Google Scholar
[43]

Liu, S. R.; Cai, L. F.; Wang, L. Y.; Yi, X. F.; Peng, Y. J.; He, N.; Xue, X. E.; Wang, Y. P. Polydopamine coating on individual cells for enhanced extracellular electron transfer. Chem. Commun. 2019, 55, 10535–10538.
DOI Google Scholar
[44]

Buscemi, G.; Vona, D.; Stufano, P.; Labarile, R.; Cosma, P.; Agostiano, A.; Trotta, M.; Farinola, G. M.; Grattieri, M. Bio-inspired redox-adhesive polydopamine matrix for intact bacteria biohybrid photoanodes. ACS Appl. Mater. Interfaces 2022, 14, 26631–26641.
DOI Google Scholar
[45]

Rippka, R.; Deruelles, J.; Waterbury, J. B.; Herdman, M.; Stanier, R. Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 1979, 111, 1–61.
DOI Google Scholar
[46]

Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosyn. Res. 2006, 89, 27–41.
DOI Google Scholar
[47]

Zubkovs, V.; Antonucci, A.; Schuergers, N.; Lambert, B.; Latini, A.; Ceccarelli, R.; Santinelli, A.; Rogov, A.; Ciepielewski, D.; Boghossian, A. A. Spinning-disc confocal microscopy in the second near-infrared window (NIR-II). Sci. Rep. 2018, 8, 13770.
DOI Google Scholar
[48]

Hyun Ryu, J.; Messersmith, P. B.; Lee, H. Polydopamine surface chemistry: A decade of discovery. ACS Appl. Mater. Interfaces 2018, 10, 7523–7540.
DOI Google Scholar
[49]

Wei, Q.; Zhang, F. L.; Li, J.; Li, B. J.; Zhao, C. S. Oxidant-induced dopaminepolymerization for multifunctional coatings. Polym. Chem. 2010, 1, 1430–1433.
DOI Google Scholar
[50]

Jehlička, J.; Edwards, H. G. M.; Osterrothová, K.; Novotná, J.; Nedbalová, L.; Kopecký, J.; Němec, I.; Oren, A. Potential and limits of Raman spectroscopy for carotenoid detection in microorganisms: Implications for astrobiology. Philos. Trans. Roy. Soc. A Math. Phys. Eng. Sci. 2014, 372, 20140199.
DOI Google Scholar
[51]

Alfieri, M. L.; Panzella, L.; Oscurato, S. L.; Salvatore, M.; Avolio, R., Errico, M. E.; Maddalena, P.; Napolitano, A.; D’Ischia, M. The chemistry of polydopamine film formation: The amine-quinone interplay. Biomimetics 2018, 3, 26.
DOI Google Scholar
[52]
Scheer, H. Chlorophylls; CRC Press: Boca Raton, 1991.
[53]

Schulze, K.; López, D. A.; Tillich, U. M.; Frohme, M. A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and ImageJ. BMC Biotechnol. 2011, 11, 118.
DOI Google Scholar
[54]

Ponzio, F.; Ball, V. Persistence of dopamine and small oxidation products thereof in oxygenated dopamine solutions and in “polydopamine” films. Colloids Surf. A Physicochem. Eng. Aspects 2014, 443, 540–543.
DOI Google Scholar
[55]

Bu, T.; Tian, Y. M.; Ma, J.; Zhang, M.; Bai, F. E.; Zhao, S.; He, K. Y.; Sun, X. Y.; Wang, Y.; Wang, L. Polydopamine-mediated photothermal effect enables a new method for point-of-care testing of biothiols using a portable photothermal sensor. Sens. Actuators B Chem. 2021, 346, 130498.
DOI Google Scholar
[56]

Fan, S. B.; Lin, W. S.; Huang, Y. F.; Xia, J. J.; Xu, J. F.; Zhang, J. H.; Pi, J. Advances and potentials of polydopamine nanosystem in photothermal-based antibacterial infection therapies. Front. Pharmacol. 2022, 13, 829712.
DOI Google Scholar
[57]

Tasaka, Y.; Gombos, Z.; Nishiyama, Y.; Mohanty, P.; Ohba, T.; Ohki, K.; Murata, N. Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: Evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J. 1996, 15, 6416–6425.
DOI Google Scholar
[58]

Hasunuma, T.; Matsuda, M.; Kato, Y.; Vavricka, C. J.; Kondo, A. Temperature enhanced succinate production concurrent with increased central metabolism turnover in the cyanobacterium Synechocystis sp. PCC 6803. Metab. Eng. 2018, 48, 109–120
DOI Google Scholar
[59]

Červený, J.; Sinetova, M. A.; Zavřel, T.; Los, D. A. Mechanisms of high temperature resistance of Synechocystis sp. PCC 6803: An impact of histidine kinase 34. Life 2015, 5, 676–699
DOI Google Scholar
File
12274_2023_6396_MOESM1_ESM.pdf (1.3 MB)
Publication history
Copyright
Acknowledgements

Publication history

Received: 19 June 2023
Revised: 03 November 2023
Accepted: 04 November 2023
Published: 25 January 2024
Issue date: February 2024

Copyright

© The Author(s) 2024

Acknowledgements

Acknowledgements

The authors are thankful for support from the Swiss National Science Foundation (Sinergia Project, No. IZLIZ2_182972).

Return