Active transport of Ca2+ by an artificial photosynthetic membrane

Abstract

Transport of calcium ions across membranes and against a thermodynamic gradient is essential to many biological processes, including muscle contraction, the citric acid cycle, glycogen metabolism, release of neurotransmitters, vision, biological signal transduction and immune response. Synthetic systems that transport metal ions across lipid or liquid membranes are well known, and in some cases light has been used to facilitate transport. Typically, a carrier molecule located in a symmetric membrane binds the ion from aqueous solution on one side and releases it on the other. The thermodynamic driving force is provided by an ion concentration difference between the two aqueous solutions, coupling to such a gradient in an auxiliary species, or photomodulation of the carrier by an asymmetric photon flux. Here we report a different approach, in which active transport is driven not by concentration gradients, but by light-induced electron transfer in a photoactive molecule that is asymmetrically disposed across a lipid bilayer. The system comprises a synthetic, light-driven transmembrane Ca2+ pump based on a redox-sensitive, lipophilic Ca2+-binding shuttle molecule whose function is powered by an intramembrane artificial photosynthetic reaction centre. The resulting structure transports calcium ions across the bilayer of a liposome to develop both a calcium ion concentration gradient and a membrane potential, expanding Mitchell's concept of a redox loop mechanism for protons to include divalent cations. Although the quantum yield is relatively low (approximately 1 per cent), the Ca2+ electrochemical potential developed is significant.

Calcium Binding and Transport by Coenzyme Q

“…The mechanism of Ca 2þ transfer by this compound is achieved through a redox switching mechanism, principally similar to the redox-dependent proton transfer. 19 In addition to this study, we recently also showed that 2PHQ can transfer not only Ca 2þ but also Ba 2þ , Sr 2þ , and to a lower extent Mg 2þ across mimetic biomembranes. 20 The analysis of the mechanism and the stoichiometry of complex formation revealed that ion binding and transfer depend critically on the adjacent position of the two oxygen atoms in the 2PHQ molecular structure.…”

“…20 The analysis of the mechanism and the stoichiometry of complex formation revealed that ion binding and transfer depend critically on the adjacent position of the two oxygen atoms in the 2PHQ molecular structure. 19,20 Such an arrangement of neighboring oxygens is, however, not found in any naturally occurring CoQ compounds. Consequently, CoQs are known not to bind Ca 2þ and correspondingly do not transport Ca 2þ across membranes.…”

H2‐Fueled ATP Synthesis on an Electrode: Mimicking Cellular Respiration

“…Liposomes,9 where a lipid bilayer separates the inner content from the outer solution, have been used as model systems to couple light energy to different biochemical reactions. The proton gradient developed by a light‐sensitive component, either bacteriorhodopsin or an artificial photosynthetic reaction center, has been coupled to Ca 2+ active transport,10 to ATP synthesis9b or to activate bacterial pumps 11. Liposomes are fragile, however, and increased robustness is desired for in vitro applications that require coupling artificially generated electrochemical gradients to solid transducers, such as lab‐scale biosensors and biomimetic fuel cells.…”

Redox Chemistry of Ca-Transporter 2-Palmitoylhydroquinone in an Artificial Thin Organic Film Membrane

“…3 Liposomes are also suitable for membrane immobilization of lipophilic quinones. In this context, Bennett et al 10 have recently incorporated the synthetic 2-palmitoylhydroquinone (H 2 Q) in a liposome membrane to build an artificial light-driven transmembrane calcium pump. Although the redox chemistry of H 2 Q is hardly known, these authors have utilized its redox sensitivity to analyze binding of Ca 2+ .…”