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  • Review Article
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Hybrid bilayer membranes as platforms for biomimicry and catalysis

Nature Reviews Chemistry volume 6, pages 862–880 (2022)Cite this article

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Abstract

Hybrid bilayer membrane (HBM) platforms represent an emerging nanoscale bio-inspired interface that has broad implications in energy catalysis and smart molecular devices. An HBM contains multiple modular components that include an underlying inorganic surface with a biological layer appended on top. The inorganic interface serves as a support with robust mechanical properties that can also be decorated with functional moieties, sensing units and catalytic active sites. The biological layer contains lipids and membrane-bound entities that facilitate or alter the activity and selectivity of the embedded functional motifs. With their structural complexity and functional flexibility, HBMs have been demonstrated to enhance catalytic turnover frequency and regulate product selectivity of the O2 and CO2 reduction reactions, which have applications in fuel cells and electrolysers. HBMs can also steer the mechanistic pathways of proton-coupled electron transfer (PCET) reactions of quinones and metal complexes by tuning electron and proton delivery rates. Beyond energy catalysis, HBMs have been equipped with enzyme mimics and membrane-bound redox agents to recapitulate natural energy transport chains. With channels and carriers incorporated, HBM sensors can quantify transmembrane events. This Review serves to summarize the major accomplishments achieved using HBMs in the past decade.

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Fig. 1: HBM platforms at a glance.
Fig. 2: HBM development timeline.
Fig. 3: HBM preparation schemes.
Fig. 4: Morphological and compositional characterization of HBMs.
Fig. 5: Application of HBM platforms towards electrocatalysis.
Fig. 6: Application of HBM platforms towards biomimicry.
Fig. 7: Application of HBM platforms towards molecular switches.
Fig. 8: Application of HBM platforms towards sensors.
Fig. 9: A roadmap presenting future research directions for HBMs.

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References

  1. Chen, H., Dong, F. & Minteer, S. D. The progress and outlook of bioelectrocatalysis for the production of chemicals, fuels and materials. Nat. Catal. 3, 225–244 (2020).

    Article  Google Scholar 

  2. Morello, G., Megarity, C. F. & Armstrong, F. A. The power of electrified nanoconfinement for energising, controlling and observing long enzyme cascades. Nat. Commun. 12, 340 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Weliwatte, N. S. & Minteer, S. D. Photo-bioelectrocatalytic CO2 reduction for a circular energy landscape. Joule 5, 2564–2592 (2021).

    Article  CAS  Google Scholar 

  4. Das, J. et al. Reagentless biomolecular analysis using a molecular pendulum. Nat. Chem. 13, 428–434 (2021).

    Article  CAS  PubMed  Google Scholar 

  5. Saunders, S. H. et al. Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. Cell 182, 919–932 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sempionatto, J. R. et al. An epidermal patch for the simultaneous monitoring of haemodynamic and metabolic biomarkers. Nat. Biomed. Eng. 5, 737–748 (2021).

    Article  CAS  PubMed  Google Scholar 

  7. Evans, R. M. et al. The value of enzymes in solar fuels research — efficient electrocatalysts through evolution. Chem. Soc. Rev. 48, 2039–2052 (2019).

    Article  CAS  PubMed  Google Scholar 

  8. Guo, Y., Stroka, J. R., Kandemir, B., Dickerson, C. E. & Bren, K. L. Cobalt metallopeptide electrocatalyst for the selective reduction of nitrite to ammonium. J. Am. Chem. Soc. 140, 16888–16892 (2018).

    Article  CAS  PubMed  Google Scholar 

  9. Le, J. M. & Bren, K. L. Engineered enzymes and bioinspired catalysts for energy conversion. ACS Energy Lett. 4, 2168–2180 (2019).

    Article  CAS  Google Scholar 

  10. Kim, J., Campbell, A. S., de Ávila, B. E.-F. & Wang, J. Wearable biosensors for healthcare monitoring. Nat. Biotechnol. 37, 389–406 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yang, Y. et al. A laser-engraved wearable sensor for sensitive detection of uric acid and tyrosine in sweat. Nat. Biotechnol. 38, 217–224 (2020).

    Article  CAS  PubMed  Google Scholar 

  12. Ngo, F. M. & Tse, E. C. M. Bioinorganic platforms for sensing, biomimicry, and energy catalysis. Chem. Lett. 50, 974–986 (2021).

    Article  Google Scholar 

  13. Hosseini, A. et al. Hybrid bilayer membrane: a platform to study the role of proton flux on the efficiency of oxygen reduction by a molecular electrocatalyst. J. Am. Chem. Soc. 133, 11100–11102 (2011). This paper showcases an early work in controlling the oxygen reduction performance of an Fe porphyrin through modulating the proton flux through an artificial lipid membrane.

    Article  CAS  PubMed  Google Scholar 

  14. Krueger, S. et al. Investigation of hybrid bilayer membranes with neutron reflectometry: probing the interactions of melittin. Langmuir 17, 511–521 (2001).

    Article  CAS  Google Scholar 

  15. Barile, C. J. et al. The flip-flop diffusion mechanism across lipids in a hybrid bilayer membrane. Biophys. J. 110, 2451–2462 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Plant, A. L. Self-assembled phospholipid/alkanethiol biomimetic bilayers on gold. Langmuir 9, 2764–2767 (1993). This work lays the foundation of HBM electrodes for biomimicry and electrochemistry.

    Article  CAS  Google Scholar 

  17. Silin, V. I. et al. The role of surface free energy on the formation of hybrid bilayer membranes. J. Am. Chem. Soc. 124, 14676–14683 (2002).

    Article  CAS  PubMed  Google Scholar 

  18. Barile, C. J. et al. Proton switch for modulating oxygen reduction by a copper electrocatalyst embedded in a hybrid bilayer membrane. Nat. Mater. 13, 619–623 (2014). This work was the first to describe designing a pH-sensitive switch that can turn on and off the oxygen reduction activity of a Cu complex inside an HBM on demand.

    Article  CAS  PubMed  Google Scholar 

  19. Vockenroth, I. K. et al. Stable insulating tethered bilayer lipid membranes. Biointerphases 3, FA68–FA73 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Stelzle, M., Weissmueller, G. & Sackmann, E. On the application of supported bilayers as receptive layers for biosensors with electrical detection. J. Phys. Chem. 97, 2974–2981 (1993).

    Article  CAS  Google Scholar 

  21. Hosseini, A. et al. Ferrocene embedded in an electrode-supported hybrid lipid bilayer membrane: a model system for electrocatalysis in a biomimetic environment. Langmuir 26, 17674–17678 (2010).

    Article  CAS  PubMed  Google Scholar 

  22. Tse, E. C. M. et al. Proton transfer dynamics control the mechanism of O2 reduction by a non-precious metal electrocatalyst. Nat. Mater. 15, 754–759 (2016). This work demonstrates for the first time that an HBM oxygen reduction catalyst that intrinsically undergoes a mixture of 2e– and 4e– pathways can be steered toward facilitating the 4e– pathway exclusively through tuning the transmembrane proton transfer kinetics without covalent modifications.

    Article  CAS  PubMed  Google Scholar 

  23. Gautam, R. P. et al. Controlling proton and electron transfer rates to enhance the activity of an oxygen reduction electrocatalyst. Angew. Chem. Int. Ed. 57, 13480–13483 (2018). This pioneering work establishes the simultaneous control of both electron and proton transfer rates in oxygen reduction to achieve precise regulation of electrocatalytic activity and product selectivity without altering the core molecular structure of an HBM construct.

    Article  CAS  Google Scholar 

  24. Paleos, C. M., Sideratou, Z. & Tsiourvas, D. Molecular recognition of complementary liposomes in modeling cell–cell recognition. ChemBioChem 2, 305–310 (2001).

    Article  CAS  PubMed  Google Scholar 

  25. Ma, W. et al. Investigating electron-transfer processes using a biomimetic hybrid bilayer membrane system. Nat. Protoc. 8, 439–450 (2013). This landmark paper details the preparation procedure of a trilayer HBM platform with a lipid bilayer membrane appended on top of a self-assembled monolayer.

    Article  CAS  PubMed  Google Scholar 

  26. Tamm, L. K. & McConnell, H. M. Supported phospholipid bilayers. Biophys. J. 47, 105–113 (1985). This work is one of the pioneering papers that conceptualizes the idea of HBM.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ries, R. S., Choi, H., Blunck, R., Bezanilla, F. & Heath, J. R. Black lipid membranes: visualizing the structure, dynamics, and substrate dependence of membranes. J. Phys. Chem. B 108, 16040–16049 (2004).

    Article  CAS  Google Scholar 

  28. Sackmann, E. Supported membranes: scientific and practical applications. Science 271, 43–48 (1996).

    Article  CAS  PubMed  Google Scholar 

  29. Collman James, P. et al. A cytochrome c oxidase model catalyzes oxygen to water reduction under rate-limiting electron flux. Science 315, 1565–1568 (2007). This exemplary work establishes how electron flux can be used to control the oxygen reduction behaviour of an Fe porphyrin that has been attached onto self-assembled monolayers with various electron transfer rates.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Plant, A. L., Gueguetchkeri, M. & Yap, W. Supported phospholipid/alkanethiol biomimetic membranes: insulating properties. Biophys. J. 67, 1126–1133 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Collman, J. P. & Boulatov, R. Electrocatalytic O2 reduction by synthetic analogues of the Heme/Cu site of cytochrome oxidase incorporated in a lipid film. Angew. Chem. Int. Ed. 41, 3487–3489 (2002). This paper is among the first examples to suppress partially reduced oxygen products such as deleterious H2O2 from being produced by an electrocatalyst embedded in a lipid enclosure.

    Article  CAS  Google Scholar 

  32. Anderson, N. A., Richter, L. J., Stephenson, J. C. & Briggman, K. A. Characterization and control of lipid layer fluidity in hybrid bilayer membranes. J. Am. Chem. Soc. 129, 2094–2100 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. Krysinski, P., Moncelli, M. R. & Tadini-Buoninsegni, F. A voltammetric study of monolayers and bilayers self-assembled on metal electrodes. Electrochim. Acta 45, 1885–1892 (2000).

    Article  CAS  Google Scholar 

  34. Troiano, J. M. et al. Direct probes of 4 nm diameter gold nanoparticles interacting with supported lipid bilayers. J. Phys. Chem. C 119, 534–546 (2015).

    Article  CAS  Google Scholar 

  35. Montal, M. & Mueller, P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl Acad. Sci. USA 69, 3561–3566 (1972).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zeng, T., Gautam, R. P., Barile, C. J., Li, Y. & Tse, E. C. M. Nitrile-facilitated proton transfer for enhanced oxygen reduction by hybrid electrocatalysts. ACS Catal. 10, 13149–13155 (2020). This work presents a uniquely designed alkyl-nitrile that can facilitate proton transfer in alkaline conditions, enabling the development of a base-activated switch for use in HBMs.

    Article  CAS  Google Scholar 

  37. Han, X., Wang, L., Qi, B., Yang, X. & Wang, E. A strategy for constructing a hybrid bilayer membrane based on a carbon substrate. Anal. Chem. 75, 6566–6570 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Su, Z., Leitch, J. J. & Lipkowski, J. Electrode-supported biomimetic membranes: an electrochemical and surface science approach for characterizing biological cell membranes. Curr. Opin. Electrochem. 12, 60–72 (2018).

    Article  CAS  Google Scholar 

  39. Sabirovas, T., Valiūnienė, A. & Valincius, G. Hybrid bilayer membranes on metallurgical polished aluminum. Sci. Rep. 11, 9648 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sabirovas, T., Valiūnienė, A., Gabriunaite, I. & Valincius, G. Mixed hybrid bilayer lipid membranes on mechanically polished titanium surface. Biochim. Biophys. Acta 1862, 183232 (2020).

    Article  CAS  Google Scholar 

  41. Wang, X., Zhang, Y., Bi, H. & Han, X. Supported lipid bilayer membrane arrays on micro-patterned ITO electrodes. RSC Adv. 6, 72821–72826 (2016).

    Article  CAS  Google Scholar 

  42. Lee, B. K., Lee, H. Y., Kim, P., Suh, K. Y. & Kawai, T. Nanoarrays of tethered lipid bilayer rafts on poly(vinyl alcohol) hydrogels. Lab Chip 9, 132–139 (2009).

    Article  CAS  PubMed  Google Scholar 

  43. Zhou, X., Moran-Mirabal, J. M., Craighead, H. G. & McEuen, P. L. Supported lipid bilayer/carbon nanotube hybrids. Nat. Nanotechnol. 2, 185–190 (2007). This pioneering work describes the formation of HBM on single-walled carbon nanotube transistors for biosensing and molecular recognition.

    Article  CAS  PubMed  Google Scholar 

  44. Fabre, R. M. & Talham, D. R. Stable supported lipid bilayers on zirconium phosphonate surfaces. Langmuir 25, 12644–12652 (2009).

    Article  CAS  PubMed  Google Scholar 

  45. Su, Z. et al. Electrochemical and PM-IRRAS studies of floating lipid bilayers assembled at the Au(111) electrode pre-modified with a hydrophilic monolayer. J. Electroanal. Chem. 688, 76–85 (2013).

    Article  CAS  Google Scholar 

  46. Su, Z., Ho, D., Merrill, A. R. & Lipkowski, J. In situ electrochemical and PM-IRRAS studies of colicin E1 ion channels in the floating bilayer lipid membrane. Langmuir 35, 8452–8459 (2019).

    CAS  PubMed  Google Scholar 

  47. Quinn, J. G. & O’Kennedy, R. Transduction platforms and biointerfacial design of biosensors for ‘real-time’ biomolecular interaction analysis. Anal. Lett. 32, 1475–1517 (1999).

    Article  CAS  Google Scholar 

  48. Deng, Y. et al. Fluidic and air-stable supported lipid bilayer and cell-mimicking microarrays. J. Am. Chem. Soc. 130, 6267–6271 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Castellana, E. T. & Cremer, P. S. Solid supported lipid bilayers: from biophysical studies to sensor design. Surf. Sci. Rep. 61, 429–444 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. van Weerd, J., Karperien, M. & Jonkheijm, P. Supported lipid bilayers for the generation of dynamic cell–material interfaces. Adv. Healthc. Mater. 4, 2743–2779 (2015).

    Article  PubMed  Google Scholar 

  51. Meuse, C. W. et al. Hybrid bilayer membranes in air and water: infrared spectroscopy and neutron reflectivity studies. Biophys. J. 74, 1388–1398 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Knoll, W. et al. Functional tethered lipid bilayers. Rev. Mol. Biotechnol. 74, 137–158 (2000).

    Article  CAS  Google Scholar 

  53. Sek, S., Xu, S., Chen, M., Szymanski, G. & Lipkowski, J. STM studies of fusion of cholesterol suspensions and mixed 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC)/cholesterol vesicles onto a Au(111) electrode surface. J. Am. Chem. Soc. 130, 5736–5743 (2008).

    Article  CAS  PubMed  Google Scholar 

  54. Berti, D., Caminati, G. & Baglioni, P. Functional liposomes and supported lipid bilayers: towards the complexity of biological archetypes. Phys. Chem. Chem. Phys. 13, 8769–8782 (2011).

    Article  CAS  PubMed  Google Scholar 

  55. Suraniti, E., Tumolo, T., Baptista, M. S., Livache, T. & Calemczuk, R. Construction of hybrid bilayer membrane (HBM) biochips and characterization of the cooperative binding between cytochrome-c and HBM. Langmuir 23, 6835–6842 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. Tse, E. C. M. et al. Anion transport through lipids in a hybrid bilayer membrane. Anal. Chem. 87, 2403–2409 (2015).

    Article  CAS  PubMed  Google Scholar 

  57. Barnaba, C., Taylor, E. & Brozik, J. A. Dissociation constants of cytochrome P450 2C9/cytochrome P450 reductase complexes in a lipid bilayer membrane depend on NADPH: a single-protein tracking study. J. Am. Chem. Soc. 139, 17923–17934 (2017).

    Article  CAS  PubMed  Google Scholar 

  58. Barnaba, C., Martinez, M. J., Taylor, E., Barden, A. O. & Brozik, J. A. Single-protein tracking reveals that NADPH mediates the insertion of cytochrome P450 reductase into a biomimetic of the endoplasmic reticulum. J. Am. Chem. Soc. 139, 5420–5430 (2017). This work shows that HBMs can mimic a native lipid environment and reveal the membrane integration process of proteins in the presence of NADPH.

    Article  CAS  PubMed  Google Scholar 

  59. Phillips, K. S., Kang, K. M., Licata, L. & Allbritton, N. L. Air-stable supported membranes for single-cell cytometry on PDMS microchips. Lab Chip 10, 864–870 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhan, W. & Jiang, K. A modular photocurrent generation system based on phospholipid-assembled fullerenes. Langmuir 24, 13258–13261 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Jiang, K., Xie, H. & Zhan, W. Photocurrent generation from Ru(bpy)32+ immobilized on phospholipid/alkanethiol hybrid bilayers. Langmuir 25, 11129–11136 (2009).

    Article  CAS  PubMed  Google Scholar 

  62. Kim, S. et al. Plasmonic nanoparticle-interfaced lipid bilayer membranes. Acc. Chem. Res. 52, 2793–2805 (2019).

    Article  CAS  PubMed  Google Scholar 

  63. Zhou, W. & Burke, P. J. Versatile bottom-up synthesis of tethered bilayer lipid membranes on nanoelectronic biosensor devices. ACS Appl. Mater. Interf. 9, 14618–14632 (2017).

    Article  CAS  Google Scholar 

  64. Favero, G. et al. Glutamate receptor incorporated in a mixed hybrid bilayer lipid membrane array, as a sensing element of a biosensor working under flowing conditions. J. Am. Chem. Soc. 127, 8103–8111 (2005). This work describes the development of HBM arrays embedded with glutamate receptors as flow-based bioelectroanalytical sensors with nanomolar sensitivity.

    Article  CAS  PubMed  Google Scholar 

  65. Zare, M., Kitt, J. P., Wen, X., Heider, E. C. & Harris, J. M. Hybrid-lipid bilayers induce n-alkyl-chain order in reversed-phase chromatographic surfaces, impacting their shape selectivity for aromatic hydrocarbon partitioning. Anal. Chem. 93, 4118–4125 (2021).

    Article  CAS  PubMed  Google Scholar 

  66. Kornienko, N. et al. Oxygenic photoreactivity in photosystem II studied by rotating ring disk electrochemistry. J. Am. Chem. Soc. 140, 17923–17931 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Young, I. D. et al. Structure of photosystem II and substrate binding at room temperature. Nature 540, 453–457 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Barile, C. J. et al. Inhibiting platelet-stimulated blood coagulation by inhibition of mitochondrial respiration. Proc. Natl Acad. Sci. USA 109, 2539–2543 (2012). Electrochemical results from this HBM work contribute to the understanding of how heterocycles deter mitochondrial platelet stimulation and subsequently inhibit blood clotting.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Collman, J. P., Dey, A., Barile, C. J., Ghosh, S. & Decréau, R. A. Inhibition of electrocatalytic O2 reduction of functional CcO models by competitive, non-competitive, and mixed inhibitors. Inorg. Chem. 48, 10528–10534 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ma, W. et al. Reversible redox of NADH and NAD+ at a hybrid lipid bilayer membrane using ubiquinone. J. Am. Chem. Soc. 133, 12366–12369 (2011). This work demonstrates the ability to replicate biological redox cycling of NADH through HBM-bound ubiquinones to mimic the initial stages of respiration.

    Article  CAS  PubMed  Google Scholar 

  71. Jones, S. M. & Solomon, E. I. Electron transfer and reaction mechanism of laccases. Cell. Mol. Life Sci. 72, 869–883 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hakulinen, N. & Rouvinen, J. Three-dimensional structures of laccases. Cell. Mol. Life Sci. 72, 857–868 (2015).

    Article  CAS  PubMed  Google Scholar 

  73. Tse, E. C. M. et al. Proton transfer dynamics dictate quinone speciation at lipid-modified electrodes. Phys. Chem. Chem. Phys. 19, 7086–7093 (2017).

    Article  CAS  PubMed  Google Scholar 

  74. Supakul, S. N. & Barile, C. J. Membrane-modified metal triazole complexes for the electrocatalytic reduction of oxygen and carbon dioxide. Front. Chem. 6, 543–550 (2018). This work extends the applicability of HBMs to regulating the proton-coupled electron transfer pathway and product distribution of carbon dioxide reduction.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang, M., Chen, J., Lian, T. & Zhan, W. Mimicking photosynthesis with supercomplexed lipid nanoassemblies: design, performance, and enhancement role of cholesterol. Langmuir 32, 7326–7338 (2016).

    Article  CAS  PubMed  Google Scholar 

  76. Wang, M. & Zhan, W. Mimicking photosynthesis with electrode-supported lipid nanoassemblies. Acc. Chem. Res. 49, 2551–2559 (2016).

    Article  CAS  PubMed  Google Scholar 

  77. Xie, H., Jiang, K. & Zhan, W. A modular molecular photovoltaic system based on phospholipid/alkanethiol hybrid bilayers: photocurrent generation and modulation. Phys. Chem. Chem. Phys. 13, 17712–17721 (2011).

    Article  CAS  PubMed  Google Scholar 

  78. Kim, Y., Ding, H. & Zheng, Y. Enhancing surface capture and sensing of proteins with low-power optothermal bubbles in a biphasic liquid. Nano Lett. 20, 7020–7027 (2020). This work shows that HBM model surfaces can serve as high-fidelity biosensors that capture target proteins under high-velocity fluid flows.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kim, S. & Choi, S.-J. A lipid-based method for the preparation of a piezoelectric DNA biosensor. Anal. Biochem. 458, 1–3 (2014).

    Article  CAS  PubMed  Google Scholar 

  80. Phillips, K. S., Dong, Y., Carter, D. & Cheng, Q. Stable and fluid ethylphosphocholine membranes in a poly(dimethylsiloxane) microsensor for toxin detection in flooded waters. Anal. Chem. 77, 2960–2965 (2005).

    Article  CAS  PubMed  Google Scholar 

  81. Phillips, K. S., Kottegoda, S., Kang, K. M., Sims, C. E. & Allbritton, N. L. Separations in poly(dimethylsiloxane) microchips coated with supported bilayer membranes. Anal. Chem. 80, 9756–9762 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Reimhult, E. & Kumar, K. Membrane biosensor platforms using nano- and microporous supports. Trends Biotechnol. 26, 82–89 (2008).

    Article  CAS  PubMed  Google Scholar 

  83. Alvarez-Malmagro, J. et al. Molecular recognition between guanine and cytosine-functionalized nucleolipid hybrid bilayers supported on gold (111) electrodes. Bioelectrochemistry 132, 107416 (2020).

    Article  CAS  PubMed  Google Scholar 

  84. Vykoukal, J., Vykoukal, D. M., Sharma, S., Becker, F. F. & Gascoyne, P. R. C. Dielectrically addressable microspheres engineered using self-assembled monolayers. Langmuir 19, 2425–2433 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Gallagher, E. S. et al. Hybrid phospholipid bilayer coatings for separations of cationic proteins in capillary zone electrophoresis. Electrophoresis 35, 1099–1105 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Podolsky, K. A. & Devaraj, N. K. Synthesis of lipid membranes for artificial cells. Nat. Rev. Chem. 5, 676–694 (2021).

    Article  CAS  Google Scholar 

  87. Langton, M. J. Engineering of stimuli-responsive lipid-bilayer membranes using supramolecular systems. Nat. Rev. Chem. 5, 46–61 (2021).

    Article  CAS  Google Scholar 

  88. Herrmann, I. K., Wood, M. J. A. & Fuhrmann, G. Extracellular vesicles as a next-generation drug delivery platform. Nat. Nanotechnol. 16, 748–759 (2021).

    Article  CAS  PubMed  Google Scholar 

  89. Murphy, D. E. et al. Extracellular vesicle-based therapeutics: natural versus engineered targeting and trafficking. Exp. Mol. Med. 51, 1–12 (2019).

    Article  CAS  PubMed  Google Scholar 

  90. Brevnov, D. A. & Finklea, H. O. Alternating current voltammetry studies of the effect of melittin on heterogeneous electron transfer across a hybrid bilayer membrane supported on a gold electrode. Langmuir 16, 5973–5979 (2000).

    Article  CAS  Google Scholar 

  91. Peng, Z., Tang, J., Han, X., Wang, E. & Dong, S. Formation of a supported hybrid bilayer membrane on gold: a sterically enhanced hydrophobic effect. Langmuir 18, 4834–4839 (2002).

    Article  CAS  Google Scholar 

  92. Love, J. C., Estroff, L. A., Kriebel, J. K., Nuzzo, R. G. & Whitesides, G. M. Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem. Rev. 105, 1103–1170 (2005).

    Article  CAS  PubMed  Google Scholar 

  93. Bain, C. D. et al. Formation of monolayer films by the spontaneous assembly of organic thiols from solution onto gold. J. Am. Chem. Soc. 111, 321–335 (1989).

    Article  CAS  Google Scholar 

  94. Li, Y., Tse, E. C. M., Barile, C. J., Gewirth, A. A. & Zimmerman, S. C. Photoresponsive molecular switch for regulating transmembrane proton-transfer kinetics. J. Am. Chem. Soc. 137, 14059–14062 (2015). This work details the development of a light-gated HBM switch that can initiate and stall electrocatalysis in real time, paving the way to turning photo-electro-protonic devices into reality.

    Article  CAS  PubMed  Google Scholar 

  95. Zeng, T., Wu, H.-L., Li, Y., Tse, E. C. M. & Barile, C. J. Physical and electrochemical characterization of a Cu-based oxygen reduction electrocatalyst inside and outside a lipid membrane with controlled proton transfer kinetics. Electrochim. Acta 320, 134611 (2019).

    Article  CAS  Google Scholar 

  96. Cheng, N., Bao, P., Evans, S. D., Leggett, G. J. & Armes, S. P. Facile formation of highly mobile supported lipid bilayers on surface-quaternized pH-responsive polymer brushes. Macromolecules 48, 3095–3103 (2015).

    Article  CAS  Google Scholar 

  97. Chung, P. J., Hwang, H. L., Dasbiswas, K., Leong, A. & Lee, K. Y. C. Osmotic shock-triggered assembly of highly charged, nanoparticle-supported membranes. Langmuir 34, 13000–13005 (2018).

    Article  CAS  PubMed  Google Scholar 

  98. Troutier, A.-L. & Ladavière, C. An overview of lipid membrane supported by colloidal particles. Adv. Colloid Interf. Sci. 133, 1–21 (2007).

    Article  CAS  Google Scholar 

  99. Ziaco, M. et al. Development of clickable monophosphoryl lipid a derivatives toward semisynthetic conjugates with tumor-associated carbohydrate antigens. J. Med. Chem. 60, 9757–9768 (2017).

    Article  CAS  PubMed  Google Scholar 

  100. Alam, S. et al. A clickable and photocleavable lipid analogue for cell membrane delivery and release. Bioconjug. Chem. 26, 1021–1031 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Li, M. et al. AFM studies of solid-supported lipid bilayers formed at a Au(111) electrode surface using vesicle fusion and a combination of Langmuir−Blodgett and Langmuir−Schaefer techniques. Langmuir 24, 10313–10323 (2008).

    Article  CAS  PubMed  Google Scholar 

  102. Su, Z., Goodall, B., Leitch, J. J. & Lipkowski, J. Ion transport mechanism in gramicidin A channels formed in floating bilayer lipid membranes supported on gold electrodes. Electrochim. Acta 375, 137892 (2021).

    Article  CAS  Google Scholar 

  103. Mun, S. & Choi, S.-J. Optimization of the hybrid bilayer membrane method for immobilization of avidin on quartz crystal microbalance. Biosens. Bioelectron. 24, 2522–2527 (2009).

    Article  CAS  PubMed  Google Scholar 

  104. Smith, M. B., Tong, J., Genzer, J., Fischer, D. & Kilpatrick, P. K. Effects of synthetic amphiphilic α-helical peptides on the electrochemical and structural properties of supported hybrid bilayers on gold. Langmuir 22, 1919–1927 (2006).

    Article  CAS  PubMed  Google Scholar 

  105. Nikolov, V., Radisic, A., Hristova, K. & Searson, P. C. Bias-dependent admittance in hybrid bilayer membranes. Langmuir 22, 7156–7158 (2006).

    Article  CAS  PubMed  Google Scholar 

  106. Abbasi, F., Leitch, J. J., Su, Z., Szymanski, G. & Lipkowski, J. Direct visualization of alamethicin ion pores formed in a floating phospholipid membrane supported on a gold electrode surface. Electrochim. Acta 267, 195–205 (2018).

    Article  CAS  Google Scholar 

  107. Wu, H.-L., Tong, Y., Peng, Q., Li, N. & Ye, S. Phase transition behaviors of the supported DPPC bilayer investigated by sum frequency generation (SFG) vibrational spectroscopy and atomic force microscopy (AFM). Phys. Chem. Chem. Phys. 18, 1411–1421 (2016).

    Article  CAS  PubMed  Google Scholar 

  108. Kett, P. J. N., Casford, M. T. L. & Davies, P. B. Sum frequency generation (SFG) vibrational spectroscopy of planar phosphatidylethanolamine hybrid bilayer membranes under water. Langmuir 26, 9710–9719 (2010).

    Article  CAS  PubMed  Google Scholar 

  109. Parikh, A. N., Beers, J. D., Shreve, A. P. & Swanson, B. I. Infrared spectroscopic characterization of lipid−alkylsiloxane hybrid bilayer membranes at oxide substrates. Langmuir 15, 5369–5381 (1999).

    Article  CAS  Google Scholar 

  110. Millo, D. et al. Characterization of hybrid bilayer membranes on silver electrodes as biocompatible SERS substrates to study membrane–protein interactions. Colloids Surf. B 81, 212–216 (2010).

    Article  CAS  Google Scholar 

  111. Plant, A. L., Brighamburke, M., Petrella, E. C. & Oshannessy, D. J. Phospholipid/alkanethiol bilayers for cell-surface receptor studies by surface plasmon resonance. Anal. Biochem. 226, 342–348 (1995).

    Article  CAS  PubMed  Google Scholar 

  112. Twardowski, M. & Nuzzo, R. G. Phase dependent electrochemical properties of polar self-assembled monolayers (SAMs) modified via the fusion of mixed phospholipid vesicles. Langmuir 20, 175–180 (2004).

    Article  CAS  PubMed  Google Scholar 

  113. Twardowski, M. & Nuzzo, R. G. Molecular recognition at model organic interfaces: electrochemical discrimination using self-assembled monolayers (SAMs) modified via the fusion of phospholipid vesicles. Langmuir 19, 9781–9791 (2003).

    Article  CAS  Google Scholar 

  114. Nam, D.-H. et al. Molecular enhancement of heterogeneous CO2 reduction. Nat. Mater. 19, 266–276 (2020).

    Article  CAS  PubMed  Google Scholar 

  115. Chen, B. W. J. & Mavrikakis, M. Effects of composition and morphology on the hydrogen storage properties of transition metal hydrides: insights from PtPd nanoclusters. Nano Energy 63, 103858 (2019).

    Article  CAS  Google Scholar 

  116. Bhandari, S., Rangarajan, S. & Mavrikakis, M. Combining computational modeling with reaction kinetics experiments for elucidating the in situ nature of the active site in catalysis. Acc. Chem. Res. 53, 1893–1904 (2020).

    Article  CAS  PubMed  Google Scholar 

  117. Liao, S., Holmes, K.-A., Tsaprailis, H. & Birss, V. I. High performance PtRuIr catalysts supported on carbon nanotubes for the anodic oxidation of methanol. J. Am. Chem. Soc. 128, 3504–3505 (2006).

    Article  CAS  PubMed  Google Scholar 

  118. Liu, T. et al. Exceptional capacitive deionization rate and capacity by block copolymer based porous carbon fibers. Sci. Adv. 6, eaaz0906 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Liu, T., Zhou, Z., Guo, Y., Guo, D. & Liu, G. Block copolymer derived uniform mesopores enable ultrafast electron and ion transport at high mass loadings. Nat. Commun. 10, 675 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Ryu, J. et al. Thermochemical aerobic oxidation catalysis in water can be analysed as two coupled electrochemical half-reactions. Nat. Catal. 4, 742–752 (2021).

    Article  CAS  Google Scholar 

  121. Haider, R. et al. High temperature proton exchange membrane fuel cells: progress in advanced materials and key technologies. Chem. Soc. Rev. 50, 1138–1187 (2021).

    Article  CAS  PubMed  Google Scholar 

  122. Liang, J. et al. Ferrocene-based metal–organic framework nanosheets as a robust oxygen evolution catalyst. Angew. Chem. Int. Ed. 60, 12770–12774 (2021).

    Article  CAS  Google Scholar 

  123. Liu, M. et al. Enhanced electrocatalytic CO2 reduction via field-induced reagent concentration. Nature 537, 382–386 (2016).

    Article  CAS  PubMed  Google Scholar 

  124. Dinh, C.-T. et al. CO2 electroreduction to ethylene via hydroxide-mediated copper catalysis at an abrupt interface. Science 360, 783–787 (2018).

    Article  CAS  PubMed  Google Scholar 

  125. Xia, C. et al. General synthesis of single-atom catalysts with high metal loading using graphene quantum dots. Nat. Chem. 13, 887–894 (2021).

    Article  CAS  PubMed  Google Scholar 

  126. Cutsail, G. E., Ross, M. O., Rosenzweig, A. C. & DeBeer, S. Towards a unified understanding of the copper sites in particulate methane monooxygenase: an X-ray absorption spectroscopic investigation. Chem. Sci. 12, 6194–6209 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Cutsail, G. E. III, Gagnon, N. L., Spaeth, A. D., Tolman, W. B. & DeBeer, S. Valence-to-core X-ray emission spectroscopy as a probe of O−O bond activation in Cu2O2 complexes. Angew. Chem. Int. Ed. 58, 9114–9119 (2019).

    Article  CAS  Google Scholar 

  128. Wuttig, A., Yoon, Y., Ryu, J. & Surendranath, Y. Bicarbonate is not a general acid in Au-catalyzed CO2 electroreduction. J. Am. Chem. Soc. 139, 17109–17113 (2017).

    Article  CAS  PubMed  Google Scholar 

  129. Marshall-Roth, T. et al. A pyridinic Fe–N4 macrocycle models the active sites in Fe/N-doped carbon electrocatalysts. Nat. Commun. 11, 5283 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Yan, B., Concannon, N. M., Milshtein, J. D., Brushett, F. R. & Surendranath, Y. A membrane-free neutral pH formate fuel cell enabled by a selective nickel sulfide oxygen reduction catalyst. Angew. Chem. Int. Ed. 56, 7496–7499 (2017).

    Article  CAS  Google Scholar 

  131. Liu, M. et al. Atomically dispersed metal catalysts for the oxygen reduction reaction: synthesis, characterization, reaction mechanisms and electrochemical energy applications. Energy Environ. Sci. 12, 2890–2923 (2019).

    Article  CAS  Google Scholar 

  132. Atwa, M. et al. Scalable nanoporous carbon films allow line-of-sight 3D atomic layer deposition of Pt: towards a new generation catalyst layer for PEM fuel cells. Mater. Horiz. 8, 2451–2462 (2021).

    Article  CAS  PubMed  Google Scholar 

  133. Tse, E. C. M., Schilter, D., Gray, D. L., Rauchfuss, T. B. & Gewirth, A. A. Multicopper models for the laccase active site: effect of nuclearity on electrocatalytic oxygen reduction. Inorg. Chem. 53, 8505–8516 (2014).

    Article  CAS  PubMed  Google Scholar 

  134. Mondol, P. & Barile, C. J. Four-electron electrocatalytic O2 reduction by a ferrocene-modified glutathione complex of Cu. ACS Appl. Energy Mater. 4, 9611–9617 (2021).

    Article  CAS  Google Scholar 

  135. Varnell, J. A. et al. Identification of carbon-encapsulated iron nanoparticles as active species in non-precious metal oxygen reduction catalysts. Nat. Commun. 7, 12582 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Xia, C. et al. Continuous production of pure liquid fuel solutions via electrocatalytic CO2 reduction using solid-electrolyte devices. Nat. Energy 4, 776–785 (2019).

    Article  CAS  Google Scholar 

  137. Schreier, M., Yoon, Y., Jackson, M. N. & Surendranath, Y. Competition between H and CO for active sites governs copper-mediated electrosynthesis of hydrocarbon fuels. Angew. Chem. Int. Ed. 57, 10221–10225 (2018).

    Article  CAS  Google Scholar 

  138. Verma, S., Lu, S. & Kenis, P. J. A. Co-electrolysis of CO2 and glycerol as a pathway to carbon chemicals with improved technoeconomics due to low electricity consumption. Nat. Energy 4, 466–474 (2019).

    Article  CAS  Google Scholar 

  139. Chen, X. et al. Electrochemical CO2-to-ethylene conversion on polyamine-incorporated Cu electrodes. Nat. Catal. 4, 20–27 (2021).

    Article  Google Scholar 

  140. Pan, H. & Barile, C. J. Electrochemical CO2 reduction to methane with remarkably high Faradaic efficiency in the presence of a proton permeable membrane. Energy Environ. Sci. 13, 3567–3578 (2020).

    Article  CAS  Google Scholar 

  141. Pan, H. & Barile, C. J. Bifunctional nickel and copper electrocatalysts for CO2 reduction and the oxygen evolution reaction. J. Mater. Chem. A 8, 1741–1748 (2020).

    Article  CAS  Google Scholar 

  142. Darcy, J. W., Kolmar, S. S. & Mayer, J. M. Transition state asymmetry in C–H bond cleavage by proton-coupled electron transfer. J. Am. Chem. Soc. 141, 10777–10787 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Bullock, R. M. et al. Using nature’s blueprint to expand catalysis with Earth-abundant metals. Science 369, eabc3183 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Ding, S. et al. Hemilabile bridging thiolates as proton shuttles in bioinspired H2 production electrocatalysts. J. Am. Chem. Soc. 138, 12920–12927 (2016).

    Article  CAS  PubMed  Google Scholar 

  145. Hsieh, C.-H. et al. Redox active iron nitrosyl units in proton reduction electrocatalysis. Nat. Commun. 5, 3684 (2014).

    Article  CAS  PubMed  Google Scholar 

  146. Chan, S. I. & Yu, S. S. F. Copper protein constructs for methane oxidation. Nat. Catal. 2, 286–287 (2019).

    Article  CAS  Google Scholar 

  147. Wang, Y., Wang, D. & Li, Y. A fundamental comprehension and recent progress in advanced Pt-based ORR nanocatalysts. SmartMat 2, 56–75 (2021).

    Article  CAS  Google Scholar 

  148. Wang, Q., Shang, L., Sun-Waterhouse, D., Zhang, T. & Waterhouse, G. Engineering local coordination environments and site densities for high-performance Fe–N–C oxygen reduction reaction electrocatalysis. SmartMat 2, 154–175 (2021).

    Article  CAS  Google Scholar 

  149. Costentin, C., Di Giovanni, C., Giraud, M., Savéant, J.-M. & Tard, C. Nanodiffusion in electrocatalytic films. Nat. Mater. 16, 1016 (2017).

    Article  CAS  PubMed  Google Scholar 

  150. Thiyagarajan, N. et al. A carbon electrode functionalized by a tricopper cluster complex: overcoming overpotential and production of hydrogen peroxide in the oxygen reduction reaction. Angew. Chem. Int. Ed. 57, 3612–3616 (2018).

    Article  CAS  Google Scholar 

  151. Du, L. et al. Electrocatalytic valorisation of biomass derived chemicals. Catal. Sci. Technol. 8, 3216–3232 (2018).

    Article  CAS  Google Scholar 

  152. Wei, Z. et al. Steering electron–hole migration pathways using oxygen vacancies in tungsten oxides to enhance their photocatalytic oxygen evolution performance. Angew. Chem. Int. Ed. 60, 8236–8242 (2021).

    Article  CAS  Google Scholar 

  153. Tse, E. C. M. & Gewirth, A. A. Effect of temperature and pressure on the kinetics of the oxygen reduction reaction. J. Phys. Chem. A 119, 1246–1255 (2015).

    Article  CAS  PubMed  Google Scholar 

  154. Mo, X., Chan, K. C. & Tse, E. C. M. A scalable laser-assisted method to produce active and robust graphene-supported nanoparticle electrocatalysts. Chem. Mater. 31, 8230–8238 (2019).

    Article  CAS  Google Scholar 

  155. Du, L. et al. Low-PGM and PGM-free catalysts for proton exchange membrane fuel cells: stability challenges and material solutions. Adv. Mater. 33, 1908232 (2021).

    Article  CAS  Google Scholar 

  156. Chen, Z., Vannucci, A. K., Concepcion, J. J., Jurss, J. W. & Meyer, T. J. Proton-coupled electron transfer at modified electrodes by multiple pathways. Proc. Natl Acad. Sci. USA 108, E1461–E1469 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Weinberg, D. R. et al. Proton-coupled electron transfer. Chem. Rev. 112, 4016–4093 (2012).

    Article  CAS  PubMed  Google Scholar 

  158. Li, P., Soudackov, A. V., Koronkiewicz, B., Mayer, J. M. & Hammes-Schiffer, S. Theoretical study of shallow distance dependence of proton-coupled electron transfer in oligoproline peptides. J. Am. Chem. Soc. 142, 13795–13804 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Warburton, R. E. et al. Interfacial field-driven proton-coupled electron transfer at graphite-conjugated organic acids. J. Am. Chem. Soc. 142, 20855–20864 (2020).

    Article  CAS  PubMed  Google Scholar 

  160. Tse, E. C. M., Hoang, T. T. H., Varnell, J. A. & Gewirth, A. A. Observation of an inverse kinetic isotope effect in oxygen evolution electrochemistry. ACS Catal. 6, 5706–5714 (2016).

    Article  CAS  Google Scholar 

  161. Tse, E. C. M., Varnell, J. A., Hoang, T. T. H. & Gewirth, A. A. Elucidating proton involvement in the rate-determining step for Pt/Pd-based and non-precious-metal oxygen reduction reaction catalysts using the kinetic isotope effect. J. Phys. Chem. Lett. 7, 3542–3547 (2016).

    Article  CAS  PubMed  Google Scholar 

  162. Roubelakis, M. M., Bediako, D. K., Dogutan, D. K. & Nocera, D. G. Proton-coupled electron transfer kinetics for the hydrogen evolution reaction of hangman porphyrins. Energy Environ. Sci. 5, 7737–7740 (2012).

    Article  CAS  Google Scholar 

  163. Chang, C. J., Chang, M. C. Y., Damrauer, N. H. & Nocera, D. G. Proton-coupled electron transfer: a unifying mechanism for biological charge transport, amino acid radical initiation and propagation, and bond making/breaking reactions of water and oxygen. Biochim. Biophys. Acta 1655, 13–28 (2004).

    Article  CAS  PubMed  Google Scholar 

  164. Costentin, C. Proton-coupled electron transfer catalyst: heterogeneous catalysis. application to an oxygen evolution catalyst. ACS Catal. 10, 7958–7967 (2020).

    Article  CAS  Google Scholar 

  165. Agarwal, R. G. et al. Free energies of proton-coupled electron transfer reagents and their applications. Chem. Rev. 122, 1–49 (2022).

    Article  CAS  PubMed  Google Scholar 

  166. Morris, W. D. & Mayer, J. M. Separating proton and electron transfer effects in three-component concerted proton-coupled electron transfer reactions. J. Am. Chem. Soc. 139, 10312–10319 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Gautam, R. P. & Barile, C. J. Preparation and electron-transfer properties of self-assembled monolayers of ferrocene on carbon electrodes. J. Phys. Chem. C 125, 8177–8184 (2021).

    Article  CAS  Google Scholar 

  168. Chidsey, C. E. D. Free energy and temperature dependence of electron transfer at the metal-electrolyte interface. Science 251, 919–922 (1991).

    Article  CAS  PubMed  Google Scholar 

  169. Pohl, E. E., Peterson, U., Sun, J. & Pohl, P. Changes of intrinsic membrane potentials induced by flip-flop of long-chain fatty acids. Biochemistry 39, 1834–1839 (2000).

    Article  CAS  PubMed  Google Scholar 

  170. Kamp, F. & Hamilton, J. A. pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids. Proc. Natl Acad. Sci. USA 89, 11367–11370 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Grifall-Sabo, J. C., Nolan, T., Beck, M. M. & Barile, C. J. Kinetic modeling of electrocatalytic oxygen reduction products from lipid-modified electrodes. J. Math. Chem. 57, 2195–2207 (2019).

    Article  CAS  Google Scholar 

  172. Mennel, J. A., Pan, H., Palladino, S. W. & Barile, C. J. Electrocatalytic CO2 reduction by self-assembled monolayers of metal porphyrins. J. Phys. Chem. C 124, 19716–19724 (2020).

    Article  CAS  Google Scholar 

  173. Devadoss, A. & Burgess, J. D. Detection of cholesterol through electron transfer to cholesterol oxidase in electrode-supported lipid bilayer membranes. Langmuir 18, 9617–9621 (2002).

    Article  CAS  Google Scholar 

  174. Ratajczak, M. K., Chris, Ko,Y. T., Lange, Y., Steck, T. L. & Lee, K. Y. C. Cholesterol displacement from membrane phospholipids by hexadecanol. Biophys. J. 93, 2038–2047 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Ege, C., Ratajczak, M. K., Majewski, J., Kjaer, K. & Lee, K. Y. C. Evidence for lipid/cholesterol ordering in model lipid membranes. Biophys. J. 91, L01–L03 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Johnson, D. L. & Martin, L. L. Controlling protein orientation at interfaces using histidine tags: an alternative to Ni/NTA. J. Am. Chem. Soc. 127, 2018–2019 (2005).

    Article  CAS  PubMed  Google Scholar 

  177. Rusling, J. F. & Nassar, A. E. F. Enhanced electron transfer for myoglobin in surfactant films on electrodes. J. Am. Chem. Soc. 115, 11891–11897 (1993).

    Article  CAS  Google Scholar 

  178. Fleming, B. D. et al. Redox properties of cytochrome P450BM3 measured by direct methods. Eur. J. Biochem. 270, 4082–4088 (2003).

    Article  CAS  PubMed  Google Scholar 

  179. Göpel, W. & Heiduschka, P. Interface analysis in biosensor design. Biosens. Bioelectron. 10, 853–883 (1995).

    Article  PubMed  Google Scholar 

  180. Laftsoglou, T. & Jeuken, L. J. C. Supramolecular electrode assemblies for bioelectrochemistry. Chem. Commun. 53, 3801–3809 (2017).

    Article  CAS  Google Scholar 

  181. Jeuken, L. J. C. Electrodes for integral membrane enzymes. Nat. Prod. Rep. 26, 1234–1240 (2009).

    Article  CAS  PubMed  Google Scholar 

  182. Torchut, E., Bourdillon, C. & Laval, J.-M. Reconstitution of functional electron transfer between membrane biological elements in a two-dimensional lipidic structure at the electrode interface. Biosens. Bioelectron. 9, 719–723 (1994).

    Article  CAS  PubMed  Google Scholar 

  183. Marchal, D., Pantigny, J., Laval, J. M., Moiroux, J. & Bourdillon, C. Rate constants in two dimensions of electron transfer between pyruvate oxidase, a membrane enzyme, and ubiquinone (coenzyme Q8), its water-insoluble electron carrier. Biochemistry 40, 1248–1256 (2001).

    Article  CAS  PubMed  Google Scholar 

  184. Burgess, J. D., Rhoten, M. C. & Hawkridge, F. M. Cytochrome c oxidase immobilized in stable supported lipid bilayer membranes. Langmuir 14, 2467–2475 (1998).

    Article  CAS  Google Scholar 

  185. Hemmatian, Z. et al. Electronic control of H+ current in a bioprotonic device with gramicidin A and alamethicin. Nat. Commun. 7, 12981 (2016). This work illustrates the integration of complex transmembrane ion channels into HBMs for the construction of functional bioprotonic devices.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Kozuch, J., Steinem, C., Hildebrandt, P. & Millo, D. Combined electrochemistry and surface-enhanced infrared absorption spectroscopy of gramicidin A incorporated into tethered bilayer lipid membranes. Angew. Chem. Int. Ed. 51, 8114–8117 (2012). This work demonstrates the use of advanced surface spectroscopic techniques for the in situ structural and functional characterization of HBMs with membrane-bound peptides.

    Article  CAS  Google Scholar 

  187. Langecker, M., Arnaut, V., List, J. & Simmel, F. C. DNA nanostructures interacting with lipid bilayer membranes. Acc. Chem. Res. 47, 1807–1815 (2014).

    Article  CAS  PubMed  Google Scholar 

  188. Radu, V., Frielingsdorf, S., Evans, S. D., Lenz, O. & Jeuken, L. J. C. Enhanced oxygen-tolerance of the full heterotrimeric membrane-bound [NiFe]-hydrogenase of Ralstonia eutropha. J. Am. Chem. Soc. 136, 8512–8515 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Pollheimer, P. et al. Reversible biofunctionalization of surfaces with a switchable mutant of avidin. Bioconjug. Chem. 24, 1656–1668 (2013).

    Article  CAS  PubMed  Google Scholar 

  190. Janiak, M. J., Small, D. M. & Shipley, G. G. Temperature and compositional dependence of the structure of hydrated dimyristoyl lecithin. J. Biol. Chem. 254, 6068–6078 (1979).

    Article  CAS  PubMed  Google Scholar 

  191. Gudmand, M. et al. Influence of lipid heterogeneity and phase behavior on phospholipase A2 action at the single molecule level. Biophys. J. 98, 1873–1882 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Moraille, P. & Badia, A. Enzymatic lithography of phospholipid bilayer films by stereoselective hydrolysis. J. Am. Chem. Soc. 127, 6546–6547 (2005).

    Article  CAS  PubMed  Google Scholar 

  193. Liu, J. & Conboy, J. C. Phase transition of a single lipid bilayer measured by sum-frequency vibrational spectroscopy. J. Am. Chem. Soc. 126, 8894–8895 (2004).

    Article  CAS  PubMed  Google Scholar 

  194. Yang, J. & Appleyard, J. The main phase transition of mica-supported phosphatidylcholine membranes. J. Phys. Chem. B 104, 8097–8100 (2000).

    Article  CAS  Google Scholar 

  195. Feng, Z. V., Spurlin, T. A. & Gewirth, A. A. Direct visualization of asymmetric behavior in supported lipid bilayers at the gel–fluid phase transition. Biophys. J. 88, 2154–2164 (2005).

    Article  CAS  PubMed  Google Scholar 

  196. Hønger, T., Jørgensen, K., Biltonen, R. L. & Mouritsen, O. G. Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity. Biochemistry 35, 9003–9006 (1996).

    Article  PubMed  Google Scholar 

  197. Ray, S., Scott, J. L. & Tatulian, S. A. Effects of lipid phase transition and membrane surface charge on the interfacial activation of phospholipase A2. Biochemistry 46, 13089–13100 (2007).

    Article  CAS  PubMed  Google Scholar 

  198. Wu, H. et al. Enzyme-catalyzed hydrolysis of the supported phospholipid bilayers studied by atomic force microscopy. Biochim. Biophys. Acta 1828, 642–651 (2013).

    Article  CAS  PubMed  Google Scholar 

  199. Dufrêne, Y. F. & Lee, G. U. Advances in the characterization of supported lipid films with the atomic force microscope. Biochim. Biophys. Acta 1509, 14–41 (2000).

    Article  PubMed  Google Scholar 

  200. Leidy, C. et al. Membrane restructuring by phospholipase A2 is regulated by the presence of lipid domains. Biophys. J. 101, 90–99 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. El Kirat, K., Morandat, S. & Dufrêne, Y. F. Nanoscale analysis of supported lipid bilayers using atomic force microscopy. Biochim. Biophys. Acta 1798, 750–765 (2010).

    Article  CAS  PubMed  Google Scholar 

  202. Nagle, J. F. & Tristram-Nagle, S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159–195 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Leidy, C., Kaasgaard, T., Crowe, J. H., Mouritsen, O. G. & Jørgensen, K. Ripples and the formation of anisotropic lipid domains: imaging two-component supported double bilayers by atomic force microscopy. Biophys. J. 83, 2625–2633 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Leidy, C., Mouritsen, O. G., Jørgensen, K. & Peters, G. H. Evolution of a rippled membrane during phospholipase A2 hydrolysis studied by time-resolved AFM. Biophys. J. 87, 408–418 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Wang, W. & Tse, E. C. M. Proton removal kinetics that govern the hydrogen peroxide oxidation activity of heterogeneous bioinorganic platforms. Inorg. Chem. 60, 6900–6910 (2021).

    Article  CAS  PubMed  Google Scholar 

  206. Basu Ball, W., Neff, J. K. & Gohil, V. M. The role of nonbilayer phospholipids in mitochondrial structure and function. FEBS Lett. 592, 1273–1290 (2018).

    Article  CAS  PubMed  Google Scholar 

  207. Vanni, S., Hirose, H., Barelli, H., Antonny, B. & Gautier, R. A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment. Nat. Commun. 5, 4916 (2014).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

E.C.M.T. thanks the Hong Kong (HK) Research Grants Council (RGC) for funding the HBM research programme via an Early Career Scheme (RGC grant 27301120) and the National Natural Science Foundation of China for providing a Young Scientists Fund (NSFC 22002132) to support research efforts on heterogeneous energy catalysis. The authors thank the CAS−RGC Joint Laboratory Funding Scheme (RGC grant JLFS/P-704/18) for supporting the HKU−CAS Joint Laboratory on New Materials. The authors acknowledge financial support from the Innovation and Technology Commission (ITC) for funding the “Laboratory for Synthetic Chemistry and Chemical Biology” via the Health@InnoHK programme. H.-L.W. thanks MOST (the Ministry of Science and Technology), Taiwan and the Center of Atomic Initiative for New Materials, National Taiwan University, from the Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education in Taiwan (108L9008). The contributions of C.J.B. and R.P.G. are based upon work supported by the National Science Foundation CAREER Award under grant number CHE-2046105.

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Authors and Affiliations

  1. Department of Chemistry, University of Hong Kong, Hong Kong SAR, China

    Tian Zeng, Ying Li & Edmund C. M. Tse

  2. Department of Chemistry, University of Nevada, Reno, NV, USA

    Rajendra P. Gautam & Christopher J. Barile

  3. Catalyst Tec Limited, Auckland, New Zealand

    Danny H. Ko & Ali Hosseini

  4. Center for Condensed Matter Sciences, National Taiwan University, Taipei, Taiwan

    Heng-Liang Wu

  5. Center of Atomic Initiative for New Materials, National Taiwan University, Taipei, Taiwan

    Heng-Liang Wu

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  1. Tian Zeng
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All authors contributed equally to the preparation of this manuscript.

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Glossary

Agglomeration

A process in which nanoparticles aggregate into a larger mass that is loosely packed by physical and chemical forces.

Flip-flop diffusion

A process where a bilayer-bound molecule moves from one lipid leaflet to another leaflet.

Laviron analysis

A mathematical method of determining the electron transfer rate constant of redox-active species adsorbed on an electrode by varying the scan rate in cyclic voltammetry.

Michaelis constant

(Km). Measures the affinity between the transporter and its substrate. Km is defined as the substrate concentration that is transported at half the maximum velocity.

Quartz crystal microbalance

Records the change in frequency of a quartz crystal resonator to measure the mass variation per unit area for determining the surface affinity of molecules in liquid.

Marangoni convection

A physical phenomenon driven by the surface tension gradient on the surface of a thin liquid layer.

Mica

A freshly cleaved mica plate can be used in AFM studies owing to its surface flatness at the atomic level.

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Zeng, T., Gautam, R.P., Ko, D.H. et al. Hybrid bilayer membranes as platforms for biomimicry and catalysis. Nat Rev Chem 6, 862–880 (2022). https://doi.org/10.1038/s41570-022-00433-2

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