Article pubs.acs.org/JPCB
Self-Assembled Light-Harvesting System from Chromophores in Lipid Vesicles Tuba Sahin,† Michelle A. Harris,‡ Pothiappan Vairaprakash,† Dariusz M. Niedzwiedzki,§ Vijaya Subramanian,∥ Andrew P. Shreve,*,∥ David F. Bocian,*,⊥ Dewey Holten,*,‡ and Jonathan S. Lindsey*,† †
Department of Chemistry, North Carolina State University, Raleigh, North Carolina 27695-8204, United States Department of Chemistry, Washington University, St. Louis, Missouri 63130-4889, United States § Photosynthetic Antenna Research Center, Washington University, St. Louis, Missouri 63130-4889, United States ∥ Center for Biomedical Engineering and Department of Chemical and Biological Engineering, University of New Mexico, Albuquerque, New Mexico 87131-0001, United States ⊥ Department of Chemistry, University of California, Riverside, California 92521-0403, United States ‡
S Supporting Information *
ABSTRACT: Lipid vesicles are used as the organizational structure of self-assembled light-harvesting systems. Following analysis of 17 chromophores, six were selected for inclusion in vesicle-based antennas. The complementary absorption features of the chromophores span the near-ultraviolet, visible, and near-infrared region. Although the overall concentration of the pigments is low (∼1 μM for quantitative spectroscopic studies) in a cuvette, the lipid-vesicle system affords high concentration (≥10 mM) in the bilayer for efficient energy flow from donor to acceptor. Energy transfer was characterized in 13 representative binary mixtures using static techniques (fluorescence−excitation versus absorptance spectra, quenching of donor fluorescence, modeling emission spectra of a mixture versus components) and time-resolved spectroscopy (fluorescence, ultrafast absorption). Binary donor−acceptor systems that employ a boron-dipyrrin donor (S0 ↔ S1 absorption/ emission in the blue-green) and a chlorin or bacteriochlorin acceptor (S0 ↔ S1 absorption/emission in the red or near-infrared) have an average excitation-energy-transfer efficiency (ΦEET) of ∼50%. Binary systems with a chlorin donor and a chlorin or bacteriochlorin acceptor have ΦEET ∼ 85%. The differences in ΦEET generally track the donor-fluorescence/acceptor-absorption spectral overlap within a dipole−dipole coupling (Förster) mechanism. Substantial deviation from single-exponential decay of the excited donor (due to the dispersion of donor−acceptor distances) is expected and observed. The time profiles and resulting ΦEET are modeled on the basis of (Förster) energy transfer between chromophores relatively densely packed in a twodimensional compartment. Initial studies of two ternary and one quaternary combination of chromophores show the enhanced spectral coverage and energy-transfer efficacy expected on the basis of the binary systems. Collectively, this approach may provide one of the simplest designs for self-assembled light-harvesting systems that afford broad solar collection and efficient energy transfer.
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INTRODUCTION Photosynthesis, the ultimate source of energy for almost all life, begins by absorption of light in antenna systems.1 The antenna are highly organized three-dimensional systems of pigments that absorb light and funnel the excitation energy to the reaction centers.2,3 The antenna systems chiefly rely on (bacterio)chlorophylls although accessory pigments such as carotenoids are also employed.3 Regardless, most if not all such antenna systems have regions of the solar spectrum where their absorption is relatively weak. The lack of complete absorption of incident sunlight is not thought to constrain growth, however, because photosynthetic organisms are typically not light-limited. © XXXX American Chemical Society
In ideal artificial photosynthetic systems, however, overall performance would be light-limited. Thus, one of the objectives in artificial photosynthesis is to create panchromatic lightharvesting systems wherein photons across the spectral region from the near-ultraviolet (NUV) through the visible and into the near-infrared (NIR) are captured for effective utilization. In this regard, the artificial antenna systems differ from the native systems. Diverse approaches have been pursued to create synthetic light-harvesting systems. A widespread practice relies Received: May 20, 2015 Revised: July 7, 2015
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DOI: 10.1021/acs.jpcb.5b04841 J. Phys. Chem. B XXXX, XXX, XXX−XXX
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The Journal of Physical Chemistry B
Figure 1. Structures of the chromophores screened.
coverage depending on the properties of the individual pigments. An approach that is intermediate between the full covalent architecture and the chlorosome self-assembly approaches relies on incorporating synthetic chromophores with photosynthetic light-harvesting peptides. In this hybrid approach, the attachment of accessory chromophores to a photosynthetic peptide (e.g., the β-peptide of the bacterial light-harvesting-1 complex) at judiciously chosen sites results in formation of an antenna oligomer. The oligomer resembles the native bacterial antenna system, but exhibits increased light-harvesting capabilities due to absorption by the appended chromophores and subsequent energy funneling to the native bacteriochlorophylls.15 The synthetic, native, or hybrid light-harvesting architectures all have a high degree of 3-dimensional organization. As a counterpoint to this feature, we wondered whether a panchromatic light-harvesting system could be created by the self-assembly of chromophores in a lipid membrane. The
on synthetic chemistry to construct covalently linked molecular architectures composed of light-absorbing pigments and an accompanying scaffold. Numerous elegant architectures composed of sizable numbers of pigments with 3-dimensional control of interpigment distances and orientations have been created,4−9 yet the approach is constrained by the extensive synthesis required. An alternative approach to that of the full covalent architecture relies on self-assembly, as in mimicry of the chlorosomes of green photosynthetic bacteria. Chlorosomes are large cigar-shaped antenna complexes in which the lightabsorbing pigments are organized in self-assembled structures with relatively small contributions from proteins.10 To mimic such systems, large assemblies of chromophores are generated from pigments by using direct pigment−pigment interactions.3,11−14 This approach requires relatively less synthesis but may not afford large assemblies and broad-band spectral B
DOI: 10.1021/acs.jpcb.5b04841 J. Phys. Chem. B XXXX, XXX, XXX−XXX
Article
The Journal of Physical Chemistry B
4.2 and 1.7 Hz, 2H); MALDI-MS obsd 268.9; ESI-MS obsd 270.10029, calcd 270.10086 [(M + H)+, M = C14H10BF2N3]. 8-(N-Methylpyridinium-4-yl)-4,4-difluoro-4-bora-3a,4adiaza-s-indacene (Py-BDPY). A solution of 8-(4-pyridyl)-4,4difluoro-4-bora-3a,4a-diaza-s-indacene (22 mg, 0.082 mmol) in CHCl3 (4 mL) was treated with iodomethane (0.20 mL, 3.2 mmol). The reaction mixture was stirred at room temperature for 24 h. The volatiles were evaporated under a stream of argon in the hood. The resulting crude solid was treated with anhydrous diethyl ether followed by immersion in a benchtop sonication bath. The resulting suspension was centrifuged. The supernatant was removed leaving the title compound as a solid (5.0 mg, 14%, assuming an iodide counterion): 1H NMR (400 MHz, DMSO-d6) δ 4.45 (s, 3H), 6.77 (dd, J = 4.2 and 1.2 Hz, 2H), 7.06 (d, J = 4.2 Hz, 2H), 8.31 (s, 2H), 8.46 (d, J = 6.6 Hz, 2H), 9.21 (d, J = 6.6 Hz, 2H); MALDI-MS obsd 284.1; ESI-MS obsd 284.11607, calcd 284.11651 [(M − I) + , M = C15H13BF2IN3]. Vesicles. Large, unilamellar vesicles of L-α-phosphatidylcholine were prepared by extrusion, and have a mean diameter of ∼120 nm (σ ∼ 15 nm) measured by dynamic light-scattering.27 The resulting stock vesicle suspension was 65 mM [lipid] in 0.1 M potassium phosphate buffer (pH 7). Chromophore Incorporation in Vesicles. Each experiment was conducted in a 1 cm path length cuvette containing 2 mL of 0.054 mM [lipid] vesicle suspension in 0.1 M potassium phosphate buffer (pH 7). This corresponds to 108 nmol (6.5 × 1016 molecules) of lipid in the solution. Each chromophore was prepared as an ethanol stock solution (∼0.020−0.122 mM). An aliquot (∼10−60 μL) of the ethanolic solution of each chromophore was injected into the lipid-vesicle suspension at room temperature. Depending on the system, this amount corresponds to 0.5, 0.7, or 1.2 nmol of each chromophore; for most of the studies for which a ΦEET value is reported, the amount of each chromophore (donor and acceptor) is 1.2 nmol. Absorption, fluorescence, and fluorescence−excitation spectra were first performed for the chromophore alone, and then in a binary system as an energy-transfer donor or acceptor. The molar absorptivities (ε, M−1 cm−1) of the chromophores at the S0 → S1 maximum (the Qy for chlorins and bacteriochlorins) used for calculating concentrations were drawn from the literature where known or adopted on the basis of values for analogues. The values employed are as follows: MsBDPY (50 000, by analogy with meso-arylborondipyrrins24), Chl-BA and Chl-Py (40 000, by analogy with similar chlorins28−30), PPa (45 000),31 BChl-BA and BChl-Py (100 000, by analogy with diverse bacteriochlorins32). A lower value of 40 000 M−1 cm−1 for BChl-Py has been employed in other studies.23 Later analysis of the absorption spectrum of BChl-Py in comparison with those for a range of bacteriochlorins indicated that ε = 80 000 M−1 cm−1 is more appropriate22 and reflects the broader Qy band relative to the norm (e.g., BChl-BA) but with similar integrated intensity. The value of 80 000 M−1 cm−1 for BChl-Py was used below for other analysis (e.g., energy-transfer using Förster theory). Concentration of Chromophores. The assembly of chromophores into the lipid membrane of the vesicle results in a high effective concentration of chromophores inside the bilayer, yet the total chromophore concentration is quite low (typically
