Skip to main content

Advertisement

SpringerLink
Log in

Amphiphilic, hydrophilic, or hydrophobic synthetic bacteriochlorins in biohybrid light-harvesting architectures: consideration of molecular designs

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Biohybrid light-harvesting architectures can be constructed that employ native-like bacterial photosynthetic antenna peptides as a scaffold to which synthetic chromophores are attached to augment overall spectral coverage. Synthetic bacteriochlorins are attractive to enhance capture of solar radiation in the photon-rich near-infrared spectral region. The effect of the polarity of the bacteriochlorin substituents on the antenna self-assembly process was explored by the preparation of a bacteriochlorin–peptide conjugate using a synthetic amphiphilic bacteriochlorin (B1) to complement prior studies using hydrophilic (B2, four carboxylic acids) or hydrophobic (B3) bacteriochlorins. The amphiphilic bioconjugatable bacteriochlorin B1 with a polar ammonium-terminated tail was synthesized by sequential Pd-mediated reactions of a 3,13-dibromo-5-methoxybacteriochlorin. Each bacteriochlorin bears a maleimido-terminated tether for attachment to a cysteine-containing analog of the Rhodobacter sphaeroides antenna β-peptide to give conjugates β-B1, β-B2, and β-B3. Given the hydrophobic nature of the β-peptide, the polarity of B1 and B2 facilitated purification of the respective conjugate compared to the hydrophobic B3. Bacteriochlorophyll a (BChl a) associates with each conjugate in aqueous micellar media to form a dyad containing two β-peptides, two covalently attached synthetic bacteriochlorins, and a datively bonded BChl-a pair, albeit to a limited extent for β-B2. The reversible assembly/disassembly of dyad (β-B2/BChl)2 was examined in aqueous detergent (octyl glucoside) solution by temperature variation (15–35 °C). The energy-transfer efficiency from the synthetic bacteriochlorin to the BChl-a dimer was found to be 0.85 for (β-B1/BChl)2, 0.40 for (β-B2/BChl)2, and 0.85 for (β-B3/BChl)2. Thus, in terms of handling, assembly and energy-transfer efficiency taken together, the amphiphilic design examined herein is more attractive than the prior hydrophilic or hydrophobic designs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

BChl a :

Bacteriochlorophyll a

CMC:

Critical micelle concentration

DMF:

N,N-Dimethylformamide

DCC:

N,N-Dicyclohexylcarbodiimide

ESI-MS:

Electrospray ionization mass spectrometry

FWHM:

Full width at half maximum

LH1:

Light-harvesting antenna 1 from photosynthetic bacteria

LH2:

Light-harvesting antenna 2 from photosynthetic bacteria

MALDI-MS:

Matrix-assisted laser-desorption ionization mass spectrometry

octG:

n-Octyl β-D-glucoside

THF:

Tetrahydrofuran

References

  • Aggarwal A, Thompson S, Singh S, Newton B, Moore A, Gao R, Gu X, Mukherjee S, Drain CM (2014) Photophysics of glycosylated derivatives of a chlorin, isobacteriochlorin, and bacteriochlorin for photodynamic theragnostics: discovery of a two-photon-absorbing photosensitizer. Photochem Photobiol 90:419–430

    Article  CAS  PubMed  Google Scholar 

  • Alexander VM, Sano K, Yu Z, Nakajima T, Choyke PL, Ptaszek M, Kobayashi H (2012) Galactosyl human serum albumin-NMP1 conjugate: a near infrared (NIR)-activatable fluorescence imaging agent to detect peritoneal ovarian cancer metastases. Bioconjug Chem 23:1671–1679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aratani N, Osuka A (2010) Synthetic strategies toward multiporphyrinic arrays. In: Kadish KM, Smith KM, Guilard R (eds) Handbook of porphyrin science, vol 1. World Scientific Publishing Co., Singapore, pp 1–132

    Chapter  Google Scholar 

  • Aravindu K, Mass O, Vairaprakash P, Springer JW, Yang E, Niedzwiedzki DM, Bocian DF, Holten D, Lindsey JS (2013) Amphiphilic chlorins and bacteriochlorins in micellar environments. Molecular design, de novo synthesis, and photophysical properties. Chem Sci 4:3459–3477

    Article  CAS  Google Scholar 

  • Billsten HH, Herek JL, Garcia-Asua G, Hashøj L, Polívka T, Hunter CN, Sundström V (2002) Dynamics of energy transfer from lycopene to bacteriochlorophyll in genetically-modified LH2 complexes of Rhodobacter sphaeroides. Biochemistry 41:4127–4136

    Article  CAS  Google Scholar 

  • Brückner C, Samankumara L, Ogikubo J (2012) Syntheses of bacteriochlorins and isobacteriochlorins. In: Kadish KM, Smith KM, Guilard R (eds) Handbook of porphyrin science, vol 17. World Scientific, Singapore, pp 1–112

    Google Scholar 

  • Chang MC, Callahan PM, Parkes-Loach PS, Cotton TM, Loach PA (1990) Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit. Biochemistry 29:421–429

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Li G, Pandey RK (2004) Synthesis of bacteriochlorins and their potential utility in photodynamic therapy (PDT). Curr Org Chem 8:1105–1134

    Article  CAS  Google Scholar 

  • Chen C-Y, Sun E, Fan D, Taniguchi M, McDowell BE, Yang E, Diers DF, Bocian D, Holten D, Lindsey JS (2012) Synthesis and photophysical properties of metallobacteriochlorins. Inorg Chem 51:9443–9464

    Article  CAS  PubMed  Google Scholar 

  • Connolly JS, Samuel EB, Janzen AF (1982) Effects of solvent on the fluorescence properties of bacteriochlorophyll a. Photochem Photobiol 36:565–574

    Article  CAS  Google Scholar 

  • da Graça Miguel M, Eidelman O, Ollivon M, Walter A (1989) Temperature dependence of the vesicle–micelle transition of egg phosphatidyl choline and octyl glucoside. Biochemistry 28:8921–8928

    Article  PubMed  Google Scholar 

  • Dąbrowski JM, Urbanska K, Arnaut LG, Pereira MM, Abreu AR, Simões S, Stochel G (2011) Biodistribution and photodynamic efficacy of a water-soluble, stable, halogenated bacteriochlorin against melanoma. ChemMedChem 6:465–475

    Article  PubMed  Google Scholar 

  • Du H, Fuh RCA, Li J, Corkan LA, Lindsey JS (1998) PhotochemCAD. A computer-aided design and research tool in photochemistry and photobiology. Photochem Photobiol 68:141–142

    CAS  Google Scholar 

  • Galezowski M, Gryko DT (2007) Recent advances in the synthesis of hydroporphyrins. Curr Org Chem 11:1310–1338

    Article  CAS  Google Scholar 

  • Grin MA, Mironov AF, Shtil AA (2008) Bacteriochlorophyll a and its derivatives: chemistry and perspectives for cancer therapy. Anti-Cancer Agents Med Chem 8:683–697

    Article  CAS  Google Scholar 

  • Harada T, Sano K, Sato K, Watanabe R, Yu Z, Hanaoka H, Nakajima T, Choyke PL, Ptaszek M, Kobayashi H (2014) Activatable organic near-infrared fluorescent probes based on a bacteriochlorin platform: synthesis and multicolor in vivo imaging with a single excitation wavelength. Bioconjug Chem 25:362–369

    Article  CAS  PubMed  Google Scholar 

  • Harris MA, Parkes-Loach PS, Springer JW, Jiang J, Martin EC, Qian P, Jiao J, Niedzwiedzki DM, Kirmaier C, Olsen JD, Bocian DF, Holten D, Hunter CN, Lindsey JS, Loach PA (2013) Integration of multiple chromophores with native photosynthetic antennas to enhance solar energy capture and delivery. Chem Sci 4:3924–3933

    Article  CAS  Google Scholar 

  • Harris MA, Jiang J, Niedzwiedzki DM, Jiao J, Taniguchi M, Kirmaier C, Loach PA, Bocian DF, Lindsey JS, Holten D, Parkes-Loach PS (2014) Versatile design of biohybrid light-harvesting architectures to tune location, density and spectral coverage of attached synthetic chromophores for enhanced energy capture. Photosynth Res 121:25–48

  • Harvey PD (2003) Recent advances in free and metalated multiporphyrin assemblies and arrays; a photophysical behavior and energy transfer perspective. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook, vol 18. Academic Press, San Diego, pp 63–250

    Chapter  Google Scholar 

  • Harvey PD, Stern C, Guilard R (2011) Bio-inspired molecular devices based on systems found in photosynthetic bacteria. In: Kadish KM, Smith KM, Guilard R (eds) Handbook of porphyrin science, vol 11. World Scientific Publishing Co., Singapore, pp 1–179

    Google Scholar 

  • Hunter CN, Bergström H, van Grondelle R, Sundström V (1990) Energy-transfer dynamics in three light-harvesting mutants of Rhodobacter sphaeroides: a picosecond spectroscopic study. Biochemistry 29:3203–3207

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Vairaprakash P, Reddy KR, Sahin T, Pavan MP, Lubian E, Lindsey JS (2014) Hydrophilic tetracarboxy bacteriochlorins for photonics applications. Org Biomol Chem 12:86–103

    Article  PubMed  Google Scholar 

  • Kim HJ, Lindsey JS (2005) De novo synthesis of stable tetrahydroporphyrinic macrocycles: bacteriochlorins and a tetradehydrocorrin. J Org Chem 70:5475–5486

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Akiyama M, Kano H, Kise H (2006) An overview of chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Springer, Dordrecht, pp 79–94

    Chapter  Google Scholar 

  • Koepke J, Hu X, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:581–597

    Article  CAS  PubMed  Google Scholar 

  • Kozyrev A, Ethirajan M, Chen P, Ohkubo K, Robinson BC, Barkigia KM, Fukuzumi S, Kadish KM, Pandey RK (2012) Synthesis, photophysical and electrochemistry of near-IR absorbing bacteriochlorins related to bacteriochlorophyll a. J Org Chem 77:10260–10271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krayer M, Ptaszek M, Kim HJ, Meneely KR, Fan D, Secor K, Lindsey JS (2010) Expanded scope of synthetic bacteriochlorins via improved acid catalysis conditions and diverse dihydrodipyrrin-acetals. J Org Chem 75:1016–1039

    Article  CAS  PubMed  Google Scholar 

  • Law CJ, Chen J, Parkes-Loach PS, Loach PA (2003) Interaction of bacteriochlorophyll with the LH1 and PufX polypeptides of photosynthetic bacteria: use of chemically synthesized analogs and covalently attached fluorescent probes. Photosynth Res 75:193–210

    Article  CAS  PubMed  Google Scholar 

  • Lindsey JS, Mass O, Chen CY (2011) Tapping the near-infrared spectral region with bacteriochlorin arrays. New J Chem 35:511–516

    Article  CAS  Google Scholar 

  • Loach PA, Parkes-Loach PS (1995) Structure-function relationships in core light-harvesting complexes (LH1) as determined by characterization of the structural subunit and by reconstitution experiments. In: Blankenship RE, Madigan MT, Bauer CE (eds) Advances in photosynthesis: anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 437–471

    Google Scholar 

  • Loach PA, Parkes-Loach PS (2009) Structure-function relationships in bacterial light-harvesting complexes investigated by reconstitution techniques. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The purple phototropic bacteria. Springer, Dordrecht, pp 181–198

    Chapter  Google Scholar 

  • Loach PA, Parkes-Loach PS, Davis CM, Heller BA (1994) Probing protein structural requirements for formation of the core light-harvesting complex of photosynthetic bacteria using hybrid reconstitution methodology. Photosynth Res 40:231–245

    Article  CAS  PubMed  Google Scholar 

  • Mauzerall D (1973) Why chlorophyll? Ann NY Acad Sci 206:483–494

    Article  CAS  PubMed  Google Scholar 

  • Mauzerall D (1992) Light, iron, Sam Granick and the origin of life. Photosynth Res 33:163–170

    Article  CAS  PubMed  Google Scholar 

  • McCarthy JR, Bhaumik J, Merbouh N, Weissleder R (2009) High-yielding syntheses of hydrophilic conjugatable chlorins and bacteriochlorins. Org Biomol Chem 7:3430–3436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meadows KA, Iida K, Kazuichi T, Recchia PA, Heller BA, Antonio B, Nango M, Loach PA (1995) Enzymatic and chemical cleavage of the core light-harvesting polypeptides of photosynthetic bacteria: determination of the minimal polypeptide size and structure required for subunit and light-harvesting complex formation. Biochemistry 34:1559–1574

    Article  CAS  PubMed  Google Scholar 

  • Meadows KA, Parkes-Loach PS, Kehoe JW, Loach PA (1998) Reconstitution of light-harvesting complexes of photosynthetic bacteria using chemically synthesized polypeptides. 1. Minimal requirements for subunit formation. Biochemistry 37:3411–3417

    Article  CAS  PubMed  Google Scholar 

  • Minehan TG, Kishi Y (1999) Total synthesis of the proposed structure of (+)-tolyporphin A O, O-diacetate. Angew Chem Int Ed 38:923–925

    Article  CAS  Google Scholar 

  • Pandit A, Visschers RW, van Stokkum IHM, Kraayenhof R, van Grondelle R (2001) Oligomerization of light-harvesting 1 antenna peptides of Rhodospirillum rubrum. Biochemistry 40:12913–12924

    Article  CAS  PubMed  Google Scholar 

  • Pandit A, Ma H, van Stokkum IHM, Gruebele M, van Grondelle R (2002) Time-resolved dissociation of the light-harvesting 1 complex of Rhodospirillum rubrum, studied by infrared laser temperature jump. Biochemistry 41:15115–15120

    Article  CAS  PubMed  Google Scholar 

  • Parkes-Loach PS, Sprinkle JR, Loach PA (1988) Reconstitution of the B873 light-harvesting complex of Rhodospirillum rubrum from the separately isolated α- and β-polypeptides and bacteriochlorophyll a. Biochemistry 27:2718–2727

    Article  CAS  PubMed  Google Scholar 

  • Pereira NAM, Fonseca SM, Serra AC, Pinho e Melo TMVD, Burrows HD (2011) [8π + 2π] Cycloaddition of meso-tetra- and 5,15-diarylporphyrins: synthesis and photophysical characterization of stable chlorins and bacteriochlorins. Eur J Org Chem 3970–3979

  • Pflock T, Dezi M, Venturoli G, Cogdell RJ, Köhler J, Oellerich S (2008) Comparison of the fluorescence kinetics of detergent-solubilized and membrane-reconstituted LH2 complexes from Rps. acidophila and Rb. sphaeroides. Photosynth Res 95:291–298

    Article  CAS  PubMed  Google Scholar 

  • Reddy KR, Jiang J, Krayer M, Harris MA, Springer JW, Yang E, Jiao J, Niedzwiedzki DM, Pandithavidana D, Parkes-Loach PS, Kirmaier C, Loach PA, Bocian DF, Holten D, Lindsey JS (2013) Palette of lipophilic bioconjugatable bacteriochlorins for construction of biohybrid light-harvesting architectures. Chem Sci 4:2036–2053

    Article  CAS  Google Scholar 

  • Ruzié C, Krayer M, Balasubramanian T, Lindsey JS (2008) Tailoring a bacteriochlorin building block with cationic, amphipathic, or lipophilic substituents. J Org Chem 73:5806–5820

    Article  PubMed  Google Scholar 

  • Samankumara LP, Wells S, Zeller M, Acuña AM, Röder B, Brückner C (2012) Expanded bacteriochlorins. Angew Chem Int Ed 51:5757–5760

    Article  CAS  Google Scholar 

  • Schubert A, Stenstam A, Beenken WJD, Herek JL, Cogdell R, Pullerits T, Sundström V (2004) In vitro self-assembly of the light harvesting pigment-protein LH2 revealed by ultrafast spectroscopy and electron microscopy. Biophys J 86:2363–2373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva AMG, Tomé AC, Neves MGPMS, Silva AMS, Cavaleiro JAS (2005) 1,3-Dipolar cycloaddition reactions of porphyrins with azomethine ylides. J Org Chem 70:2306–2314

    Article  CAS  PubMed  Google Scholar 

  • Singh S, Aggarwal A, Thompson S, Tomé JPC, Zhu X, Samaroo D, Vinodu M, Gao R, Drain CM (2010) Synthesis and photophysical properties of thioglycosylated chlorins, isobacteriochlorins, and bacteriochlorins for bioimaging and diagnostics. Bioconjug Chem 21:2136–2146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Springer JW, Parkes-Loach PS, Reddy KR, Krayer M, Jiao J, Lee GM, Niedzwiedzki DM, Harris MA, Kirmaier C, Bocian DF, Lindsey JS, Holten D, Loach PA (2012) Biohybrid photosynthetic antenna complexes for enhanced light-harvesting. J Am Chem Soc 134:4589–4599

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan N, Haney CA, Lindsey JS, Zhang W, Chait BT (1999) Investigation of MALDI-TOF mass spectrometry of diverse synthetic metalloporphyrins, phthalocyanines, and multiporphyrin arrays. J Porphyrins Phthalocyanines 3:283–291

    Article  CAS  Google Scholar 

  • Sutton JM, Clarke OJ, Fernandez N, Boyle RW (2002) Porphyrin, chlorin, and bacteriochlorin isothiocyanates: useful reagents for the synthesis of photoactive bioconjugates. Bioconjug Chem 13:249–263

    Article  CAS  PubMed  Google Scholar 

  • Todd JB, Recchia PA, Parkes-Loach PS, Olsen JD, Fowler GJS, McGlynn P, Hunter NC, Loach PA (1999) Minimal requirements for in vitro reconstitution of the structural subunit of light-harvesting complexes of photosynthetic bacteria. Photosynth Res 62:85–98

    Article  CAS  Google Scholar 

  • Tomé AC, Neves MGPMS, Cavaleiro JAS (2009) Porphyrins and other pyrrolic macrocycles in cycloaddition reactions. J Porphyrins Phthalocyanines 13:408–414

    Article  Google Scholar 

  • Wagner RW, Lindsey JS (1996a) Boron-dipyrromethene dyes for incorporation in synthetic multi-pigment light-harvesting arrays. Pure Appl Chem 68:1373–1380

    Article  CAS  Google Scholar 

  • Wagner RW, Lindsey JS (1996) Boron-dipyrromethene dyes for incorporation in synthetic multi-pigment light-harvesting arrays. Pure Appl Chem 70:1 (Corrigendum)

  • Wang W, Kishi Y (1999) Synthesis and structure of tolyporphin A O, O-diacetate. Org Lett 1:1129–1132

    Article  CAS  PubMed  Google Scholar 

  • Wolf-Klein H, Kohl C, Müllen K, Paulsen H (2002) Biomimetic model of a plant photosystem consisting of a recombinant light-harvesting complex and a terrylene dye. Angew Chem Int Ed 41:3378–3380

    Article  CAS  Google Scholar 

  • Yang E, Kirmaier C, Krayer M, Taniguchi M, Kim HJ, Diers JR, Bocian DF, Lindsey JS, Holten D (2011) Photophysical properties and electronic structure of stable, tunable synthetic bacteriochlorins: extending the features of native photosynthetic pigments. J Phys Chem B 115:10801–10816

    Article  CAS  PubMed  Google Scholar 

  • Yu Z, Ptaszek M (2012) Multifunctional bacteriochlorins from selective palladium-coupling reactions. Org Lett 14:3708–3711

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was carried out as part of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Award No. DE-SC0001035. Mass spectra were obtained at the Mass Spectrometry Laboratory for Biotechnology at North Carolina State University. Partial funding for the facility was obtained from the North Carolina Biotechnology Center and the National Science Foundation.

Author information

Authors and Affiliations

  1. Department of Chemistry, North Carolina State University, Raleigh, NC, 27695-8204, USA

    Jianbing Jiang, Kanumuri Ramesh Reddy, M. Phani Pavan, Elisa Lubian & Jonathan S. Lindsey

  2. Department of Chemistry, Washington University, St. Louis, MO, 63130-4889, USA

    Michelle A. Harris, Christine Kirmaier & Dewey Holten

  3. Department of Chemistry, University of California, Riverside, CA, 92521-0403, USA

    Jieying Jiao & David F. Bocian

  4. Department of Molecular Biosciences, Northwestern University, Evanston, IL, 60208-3500, USA

    Pamela S. Parkes-Loach & Paul A. Loach

  5. Photosynthetic Antenna Research Center, Washington University, St. Louis, MO, 63130-4889, USA

    Dariusz M. Niedzwiedzki

Authors
  1. Jianbing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kanumuri Ramesh Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Phani Pavan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisa Lubian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michelle A. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jieying Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dariusz M. Niedzwiedzki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christine Kirmaier
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pamela S. Parkes-Loach
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Paul A. Loach
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. David F. Bocian
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Dewey Holten
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jonathan S. Lindsey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan S. Lindsey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 260 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, J., Reddy, K.R., Pavan, M.P. et al. Amphiphilic, hydrophilic, or hydrophobic synthetic bacteriochlorins in biohybrid light-harvesting architectures: consideration of molecular designs. Photosynth Res 122, 187–202 (2014). https://doi.org/10.1007/s11120-014-0021-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-014-0021-9

Keywords

Search

Navigation