Elsevier

Dyes and Pigments

Volume 120, September 2015, Pages 340-346
Dyes and Pigments

A simple zinc-porphyrin-NDI dyad system generates a light energy to proton potential across a lipid membrane

https://doi.org/10.1016/j.dyepig.2015.04.040Get rights and content

Highlights

  • Creation of artificial mimic through a proton gradient across lipid membrane is described.

  • Use of a simple dyad capable of acting as an artificial mimic in lipid membrane.

  • Electron-transfer across membrane can be judged with change in intravascular pH.

  • The photocatalytic activities were studied upon UV irradiation.

  • Electron transfer between dyad was confirmed by transient absorption spectroscopy.

Abstract

We report a simple donor-acceptor dyad system capable of acting as an artificial mimic of the photosynthetic apparatus by transporting electrons across a lipid bilayer resulting in the conversion of light energy to a proton potential. The active dyad described here consists of a zinc-porphyrin as a donor and NDI as an acceptor, connected through a dithiophene spacer. Incorporation of the dyad into a lipid bilayer, followed by excitation of the zinc-porphyrin, resulted in charge separation to create a reduction potential near the inner surface and an oxidation potential near the outer surface. This led to transmembrane electron transfer where quinone was converted into hydroquinone inside the vesicle by accepting protons from the HPTS dye, creating a pH gradient. This phenomenon was supported by use of a control molecule without an appropriate spacer and electrochemical and photophysical measurements further support the existence of charge separated states and formation of stable radicals.

Introduction

In a natural photosynthetic reaction centre, light energy is converted into chemical energy by a series of electron transfer steps across a lipid bilayer [1]. Sunlight is absorbed by light-harvesting antenna fragments such as pigments, chlorophylls and carotenoids and subsequently transferred between chromophores through an energy cascade ultimately reaching a reaction centre [2]. The transmembrane electron transfer occurs in the reaction centre within the protein environment to avoid back reactions [3]. Such machinery of life was developed biologically in the long-term evolutionary process. A wish to understand these mechanisms has motivated chemists to design systems within a lipid bilayer membrane with similar properties to provide a practical model of the working molecular apparatus i.e. an artificial solar energy reaction centre [2], [3], [4], [5], [6], [7], [8], [9], [10]. So far, most of the research on artificial solar energy conversion has focused on mimicking various aspects of natural systems, and a reasonable understanding of the various components necessary for construction of an artificial photosynthetic reaction centre has been developed. To mimic the natural system, the main challenge is assembling these components in a spatially organised manner to harvest light energy into chemical energy [11]. There are currently three strategies which have been employed. One is based on constructing donor-acceptor systems in which various components are linked covalently through chemical bonds [12], [13], [14], [15], [16], [17], [18], [19]. The second uses artificial systems for the ordering of molecules in particular dyes (i.e. tubules with diameters of about 1 nm and macroscopic lengths or molecular monolayers of macroscopic areas with a thickness and interlayer distance of about 2 nm) [20], which are similar to the natural system. The third approach is to directly use lipid membrane scaffolds for incorporating and organising the necessary components, and to create a photoinduced light energy to proton potential across the lipid membrane [1], [8], [9], [10]. However, the construction of such complex, multifunctional architectures are difficult to use in practical applications due to the complexity of the scaffold, and involve lengthy multistep synthetic procedures.

We report the assembly of an artificial photosynthetic centre employing a donor-acceptor dyad, which creates a photoinduced light energy to proton potential across a lipid bilayer. Our model is based on a simple design consisting of an electron donor (zinc-porphyrin) and acceptor (naphthalene diimide: NDI). The model requires the asymmetric insertion of the molecular dyad, which has been designed to support sufficient charge-separation lifetimes, for conversion of light into a proton potential across the lipid bilayer membrane by an appropriate charge transfer sequence. From the design perspective, we wanted to establish donating and accepting dyes with an end to end distance of about 35 Å, which led to the preparation of dyad 1 (see Fig. 1).

Section snippets

Material and measurements

Naphthalenetetracarboxy dianhydride, octylamine, acetic acid (AcOH), pyrrole, benzaldehyde, boron trifluoride etherate (BF3·O(Et)2), 2,3-Dichloro-5,6-dicyano-1,4-benzoquinone (DDQ), bromine (Br2), dimethyl formamide (DMF), toluene, chloroform (CHCl3), chloroform-d (CDCl3), methanol (MeOH), dichloromethane (DCM), and zinc acetate (Zn(OAc)2·2H2O) were purchased from Aldrich and 3,5-bis(octyloxy)benzaldehyde (Ark Pharm, Inc. USA), and egg yolk phosphatidylcholine (EYPC) (Avanti polar lipids) were

Molecular design and working principle

Dyad (1) spans the lipid membrane, and is capable of fast photoinduced charge separation through initial excitation of the zinc-porphyrin donor outside the lipid bilayer, to shuttle the electron to the internal quinone. Molecular dyad 1 (Fig. 1) was prepared by linking a synthetic triarylporphyrin (por) to the naphthalene diimide (NDI) moiety with a dithiophene spacer (see Supplementary Information). Dyad 1 bears three key features consistent with other specific methodologies for studying

Conclusions

We have demonstrated the synthesis of simple donor-acceptor dyads bearing a zinc-porphyrin donor and a core-substituted naphthalene diimide acceptor with (1) and without (2) dithiophene spacer. The length of the rigid-dyad scaffold of 1 perfectly matches with (35 Å) the thickness of lipid bilayer membranes. The photosynthetic activity was measured in egg yolk phosphatidylcholine large unilamellar vesicles (EYPC-LUVs). The inside of these vesicles were loaded with sulphanato naphthaquione (Q)

Acknowledgements

SVB. (RMIT) acknowledges financial support from the Australian Research Council, Australia under a Future Fellowship Scheme (FT110100152). LAJ thanks RMIT University for receipt of a Vice Chancellors (Industry) fellowship. K.O. acknowledges the Grant-in-Aids for Scientific Research (Nos. 23750014, 26620154, 26288037) from MEXT, Japan. SVB (IICT) is grateful for financial support from the SERB (DST) SB/S1/IC-09/2014, New Delhi, India.

References (30)

  • P.R. Mussini et al.

    Modulating the electronic properties of asymmetric push–pull and symmetric Zn(II)-diarylporphyrinates with para substituted phenylethynyl moieties in 5,15 meso positions: a combined electrochemical and spectroscopic investigation

    Electrochim Acta

    (2012)
  • W.E. Ford et al.

    Photosensitized electron transport across lipid vesicle walls: quantum yield dependence on sensitizer concentration

    Proc Natl Acad Sci

    (1979)
  • R.V. Bensasson et al.

    Mimicry of antenna and photo-protective carotenoid functions by a synthetic carotenoporphyrin

    Nature

    (1981)
  • A.L. Moore et al.

    Photoprotection by carotenoids during photosynthesis: motional dependence of intramolecular energy transfer

    Science

    (1982)
  • M.R. Wasielewski et al.

    Ultrafast carotenoid to pheophorbide energy transfer in a biomimetic model for antenna function in photosynthesis

    Nature

    (1986)
  • C.M. Drain et al.

    Photogating of ionic currents across a lipid bilayer

    Proc Natl Acad Sci

    (1989)
  • D. Gust et al.

    Mimicking photosynthesis

    Science

    (1989)
  • C.M. Drain

    Self-organization of self-assembled photonic materials into functional devices: photo-switched conductors

    Proc Natl Acad Sci

    (2002)
  • D. Gust et al.

    Molecular mimicry of photosynthetic energy and electron tyransfer

    Acc Chem Res

    (1993)
  • G. Steinberg-Yfrach et al.

    Conversion of light energy to proton potential in liposomes by artificial photosynthetic reaction centers

    Nature

    (1997)
  • S. Bhosale et al.

    Photoproduction of proton gradients with π-stacked fluorophore scaffolds in lipid bilayers

    Science

    (2006)
  • A. Yella et al.

    Porphyrin-sensitized solar cells with cobalt (II/III)–based redox electrolyte exceed 12 percent efficiency

    Science

    (2011)
  • D. Gust et al.

    Efficient multistep photoinitiated electron transfer in a molecular pentad

    Science

    (1990)
  • D. Kuciauskas et al.

    An artificial photosynthetic antenna-reaction center complex

    J Am Chem Soc

    (1999)
  • R.W. Wagner et al.

    Soluble synthetic multiporphyrin arrays. 1. modular design and synthesis

    J Am Chem Soc

    (1996)
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