Infrared Signatures of Phycobilins within the Phycocyanin 645 Complex

Roy, Partha Pratim; Leonardo, Cristina; Orcutt, Kaydren; Oberg, Catrina; Scholes, Gregory D.; Fleming, Graham R.

doi:10.1021/acs.jpcb.3c01352

Title: Infrared Signatures of Phycobilins within the Phycocyanin 645 Complex

Journal Article · 16 May 2023 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI: https://doi.org/10.1021/acs.jpcb.3c01352 · OSTI ID:1973899

^[1]; Leonardo, Cristina ^[1];

^[1]; Oberg, Catrina ^[2];

^[2];

^[3]

University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Princeton University, NJ (United States)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Kavli Energy Nanoscience Institute at Berkeley, Berkeley, CA (United States)

Aquatic photosynthetic organisms evolved to use a variety of light frequencies to perform photosynthesis. Phycobiliprotein phycocyanin 645 (PC645) is a light-harvesting complex in cryptophyte algae able to transfer the absorbed green solar light to other antennas with over 99% efficiency. The infrared signatures of the phycobilin pigments embedded in PC645 are difficult to access and could provide useful information to understand the mechanism behind the high efficiency of energy transfer in PC645. We use visible-pump IR-probe and two-dimensional electronic vibrational spectroscopy to study the dynamical evolution and assign the fingerprint mid-infrared signatures to each pigment in PC645. Here, we report the pigment-specific vibrational markers that enable us to track the spatial flow of excitation energy between the phycobilin pigment pairs. We speculate that two high-frequency modes (1588 and 1596 cm^–1) are involved in the vibronic coupling leading to fast (< ps) and direct energy transfer from the highest to lowest exciton, bypassing the intermediate excitons.

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Research Organization:: University of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0020437; FWP 449A

OSTI ID:: 1973899

Alternate ID(s):: OSTI ID: 1975198

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Vol. 127, Issue 20; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (42)

The photophysics of cryptophyte light-harvesting Doust, Alexander B.; Wilk, Krystyna E.; Curmi, Paul M. G. Journal of Photochemistry and Photobiology A: Chemistry, Vol. 184, Issue 1-2 https://doi.org/10.1016/j.jphotochem.2006.06.006	journal	November 2006
Glotaran : A Java -Based Graphical User Interface for the R Package TIMP Snellenburg, Joris J.; Laptenok, Sergey P.; Seger, Ralf Journal of Statistical Software, Vol. 49, Issue 3 https://doi.org/10.18637/jss.v049.i03	journal	January 2012
Disentangling Electronic and Vibrational Coherence in the Phycocyanin-645 Light-Harvesting Complex Richards, G. H.; Wilk, K. E.; Curmi, P. M. G. The Journal of Physical Chemistry Letters, Vol. 5, Issue 1 https://doi.org/10.1021/jz402217j	journal	December 2013
Physical Basis for Long-Lived Electronic Coherence in Photosynthetic Light-Harvesting Systems Pachón, Leonardo A.; Brumer, Paul The Journal of Physical Chemistry Letters, Vol. 2, Issue 21 https://doi.org/10.1021/jz201189p	journal	October 2011
Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature Collini, Elisabetta; Wong, Cathy Y.; Wilk, Krystyna E. Nature, Vol. 463, Issue 7281 https://doi.org/10.1038/nature08811	journal	February 2010
From antenna to reaction center: Pathways of ultrafast energy and charge transfer in photosystem II Yang, Shiun-Jr; Arsenault, Eric A.; Orcutt, Kaydren Proceedings of the National Academy of Sciences, Vol. 119, Issue 42 https://doi.org/10.1073/pnas.2208033119	journal	October 2022
Infrared spectroscopy of proteins Barth, Andreas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 9 https://doi.org/10.1016/j.bbabio.2007.06.004	journal	September 2007
Broad-Band Pump–Probe Spectroscopy Quantifies Ultrafast Solvation Dynamics of Proteins and Molecules Jumper, Chanelle C.; Arpin, Paul C.; Turner, Daniel B. The Journal of Physical Chemistry Letters, Vol. 7, Issue 22 https://doi.org/10.1021/acs.jpclett.6b02237	journal	November 2016
Spectroscopic Studies of Cryptophyte Light Harvesting Proteins: Vibrations and Coherent Oscillations Arpin, Paul C.; Turner, Daniel B.; McClure, Scott D. The Journal of Physical Chemistry B, Vol. 119, Issue 31 https://doi.org/10.1021/acs.jpcb.5b04704	journal	July 2015
Solar light harvesting by energy transfer: from ecology to coherence Scholes, Gregory D.; Mirkovic, Tihana; Turner, Daniel B. Energy & Environmental Science, Vol. 5, Issue 11 https://doi.org/10.1039/c2ee23013e	journal	January 2012
Flow of Excitation Energy in the Cryptophyte Light-Harvesting Antenna Phycocyanin 645 Marin, Alessandro; Doust, Alexander B.; Scholes, Gregory D. Biophysical Journal, Vol. 101, Issue 4 https://doi.org/10.1016/j.bpj.2011.07.012	journal	August 2011
Theoretical Study of Coherent Excitation Energy Transfer in Cryptophyte Phycocyanin 645 at Physiological Temperature Huo, Pengfei; Coker, David F. The Journal of Physical Chemistry Letters, Vol. 2, Issue 7 https://doi.org/10.1021/jz200301j	journal	March 2011
Two-dimensional electronic–vibrational spectroscopy: Exploring the interplay of electrons and nuclei in excited state molecular dynamics Arsenault, Eric A.; Bhattacharyya, Pallavi; Yoneda, Yusuke The Journal of Chemical Physics, Vol. 155, Issue 2 https://doi.org/10.1063/5.0053042	journal	July 2021
Two-dimensional Fourier transform electronic spectroscopy with a pulse-shaper Myers, J. A.; Lewis, K. L. M.; Tekavec, P. F. Springer Series in Chemical Physics https://doi.org/10.1007/978-3-540-95946-5_310	book	January 2009
The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae Kolli, Avinash; O’Reilly, Edward J.; Scholes, Gregory D. The Journal of Chemical Physics, Vol. 137, Issue 17 https://doi.org/10.1063/1.4764100	journal	November 2012
Solvent Mediated Excited State Proton Transfer in Indigo Carmine Roy, Partha Pratim; Shee, James; Arsenault, Eric A. The Journal of Physical Chemistry Letters, Vol. 11, Issue 10 https://doi.org/10.1021/acs.jpclett.0c00946	journal	May 2020
Excited state coherent dynamics in light-harvesting complexes from photosynthetic marine algae Richards, G. H.; Wilk, K. E.; Curmi, P. M. G. Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 45, Issue 15 https://doi.org/10.1088/0953-4075/45/15/154015	journal	July 2012
Fourier transform near-infrared resonance Raman spectroscopic study of the α-subunit of phycoerythrocyanin and phycocyanin from the cyanobacteriumMastigocladus laminosus Kneip, Christa; Parbel, Axel; Foerstendorf, Harald Journal of Raman Spectroscopy, Vol. 29, Issue 10-11 https://doi.org/10.1002/(sici)1097-4555(199810/11)29:10/11<939::aid-jrs320>3.0.co;2-x	journal	October 1998
Vibrational and Nonadiabatic Coherence in 2D Electronic Spectroscopy, the Jahn–Teller Effect, and Energy Transfer Jonas, David M. Annual Review of Physical Chemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev-physchem-052516-050602	journal	April 2018
Two-Dimensional Electronic–Vibrational Spectroscopy of Coupled Molecular Complexes: A Near-Analytical Approach Bhattacharyya, Pallavi; Fleming, Graham R. The Journal of Physical Chemistry Letters, Vol. 10, Issue 9 https://doi.org/10.1021/acs.jpclett.9b00588	journal	April 2019
The initial charge separation step in oxygenic photosynthesis Yoneda, Yusuke; Arsenault, Eric A.; Yang, Shiun-Jr Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29983-1	journal	April 2022
Phase-cycling schemes for pump–probe beam geometry two-dimensional electronic spectroscopy Zhang, Zhengyang; Wells, Kym Lewis; Hyland, Edward William James Chemical Physics Letters, Vol. 550 https://doi.org/10.1016/j.cplett.2012.08.037	journal	October 2012
Controllable Phycobilin Modification: An Alternative Photoacclimation Response in Cryptophyte Algae Spangler, Leah C.; Yu, Mina; Jeffrey, Philip D. ACS Central Science, Vol. 8, Issue 3 https://doi.org/10.1021/acscentsci.1c01209	journal	February 2022
FTIR spectroscopic characterization of protein structure in aqueous and non-aqueous media Haris, Parvez I.; Severcan, Feride Journal of Molecular Catalysis B: Enzymatic, Vol. 7, Issue 1-4 https://doi.org/10.1016/S1381-1177(99)00030-2	journal	September 1999
High Magnetic Field Detunes Vibronic Resonances in Photosynthetic Light Harvesting Maiuri, Margherita; Oviedo, Maria B.; Dean, Jacob C. The Journal of Physical Chemistry Letters, Vol. 9, Issue 18 https://doi.org/10.1021/acs.jpclett.8b02748	journal	September 2018
Cryptomonad biliproteins ? an evolutionary perspective Glazer, Alexander N.; Wedemayer, Gary J. Photosynthesis Research, Vol. 46, Issue 1-2 https://doi.org/10.1007/BF00020420	journal	November 1995
Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms Mirkovic, Tihana; Ostroumov, Evgeny E.; Anna, Jessica M. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00002	journal	March 2016
A picosecond time-resolved fluorescence study on the biliprotein, phycocyanin 645 Malak, Henryk; MacColl, Robert Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1059, Issue 2 https://doi.org/10.1016/S0005-2728(05)80201-4	journal	August 1991
Two-dimensional electronic vibrational spectroscopy and ultrafast excitonic and vibronic photosynthetic energy transfer Wu, Eric C.; Arsenault, Eric A.; Bhattacharyya, Pallavi Faraday Discussions, Vol. 216 https://doi.org/10.1039/c8fd00190a	journal	January 2019
Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins Harrop, Stephen J.; Wilk, Krystyna E.; Dinshaw, Rayomond Proceedings of the National Academy of Sciences, Vol. 111, Issue 26 https://doi.org/10.1073/pnas.1402538111	journal	June 2014
Measuring correlated electronic and vibrational spectral dynamics using line shapes in two-dimensional electronic-vibrational spectroscopy Lewis, Nicholas H. C.; Dong, Hui; Oliver, Thomas A. A. The Journal of Chemical Physics, Vol. 142, Issue 17 https://doi.org/10.1063/1.4919686	journal	May 2015
Local protein solvation drives direct down-conversion in phycobiliprotein PC645 via incoherent vibronic transport Blau, Samuel M.; Bennett, Doran I. G.; Kreisbeck, Christoph Proceedings of the National Academy of Sciences, Vol. 115, Issue 15 https://doi.org/10.1073/pnas.1800370115	journal	March 2018
Vibronic Enhancement of Algae Light Harvesting Dean, Jacob C.; Mirkovic, Tihana; Toa, Zi S. D. Chem, Vol. 1, Issue 6 https://doi.org/10.1016/j.chempr.2016.11.002	journal	December 2016
Photosynthetic light harvesting: excitons and coherence Fassioli, Francesca; Dinshaw, Rayomond; Arpin, Paul C. Journal of The Royal Society Interface, Vol. 11, Issue 92 https://doi.org/10.1098/rsif.2013.0901	journal	March 2014
Ultrafast proton release reaction and primary photochemistry of phycocyanobilin in solution observed with fs-time-resolved mid-IR and UV/Vis spectroscopy Theiß, Maximilian; Grupe, Merten; Lamparter, Tilman Photochemical & Photobiological Sciences, Vol. 20, Issue 6 https://doi.org/10.1007/s43630-021-00045-7	journal	May 2021
Correlating the motion of electrons and nuclei with two-dimensional electronic-vibrational spectroscopy Oliver, T. A. A.; Lewis, N. H. C.; Fleming, G. R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 28 https://doi.org/10.1073/pnas.1409207111	journal	June 2014
The colorful world of cryptophyte phycobiliproteins Richardson, Tammi L. Journal of Plankton Research, Vol. 44, Issue 6 https://doi.org/10.1093/plankt/fbac048	journal	September 2022
Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: Crystal structure of a cryptophyte phycoerythrin at 1.63-A resolution Wilk, K. E.; Harrop, S. J.; Jankova, L. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.8901	journal	August 1999
Global and target analysis of time-resolved spectra van Stokkum, Ivo H. M.; Larsen, Delmar S.; van Grondelle, Rienk Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1657, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.04.011	journal	July 2004
Revealing structural involvement of chromophores in algal light harvesting complexes using symmetry-adapted perturbation theory Toa, Zi S. D.; Dean, Jacob C.; Scholes, Gregory D. Journal of Photochemistry and Photobiology B: Biology, Vol. 190 https://doi.org/10.1016/j.jphotobiol.2018.11.007	journal	January 2019
Probing the Photoreaction Mechanism of Phytochrome through Analysis of Resonance Raman Vibrational Spectra of Recombinant Analogues Andel, Frank; Murphy, John T.; Haas, Jeff A. Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1021/bi991688z	journal	February 2000
The phycocyanin-chlorophyll-protein complexes isolated from Chroomonas placoidea Chen, Min; Li, Qin; Wang, Yuxuan Journal of Oceanology and Limnology, Vol. 40, Issue 2 https://doi.org/10.1007/s00343-021-0451-0	journal	December 2021

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