Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis

Park, Soomin; Steen, Collin J.; Lyska, Dagmar; Fischer, Alexandra L.; Endelman, Benjamin; Iwai, Masakazu; Niyogi, Krishna K.; Fleming, Graham R.

doi:10.1073/pnas.1819011116

Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis

Journal Article · Sun Feb 10 23:00:00 EST 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1819011116· OSTI ID:1542372

^[1]; ^[1]; Lyska, Dagmar ^[1]; Fischer, Alexandra L. ^[1]; Endelman, Benjamin ^[1]; ^[1]; ^[1]; ^[1]

Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Nonphotochemical quenching (NPQ) is a proxy for photoprotective thermal dissipation processes that regulate photosynthetic light harvesting. The identification of NPQ mechanisms and their molecular or physiological triggering factors under in vivo conditions is a matter of controversy. In this work, to view chlorophyll (Chl)–zeaxanthin (Zea) excitation energy transfer (EET) and charge transfer (CT) as possible NPQ mechanisms, we performed transient absorption (TA) spectroscopy on live cells of the microalga Nannochloropsis oceanica. We gained evidence for the operation of both EET and CT quenching by observing spectral features associated with the Zea S₁and Zea^•+excited-state absorption (ESA) signals, respectively, after Chl excitation. Knockout mutants for genes encoding either violaxanthin de-epoxidase or LHCX1 proteins exhibited strongly inhibited NPQ capabilities and lacked detectable Zea S₁ and Zea^•+ ESA signals in vivo, which strongly suggests that the accumulation of Zea and active LHCX1 is essential for both EET and CT quenching inN. oceanica.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1542372

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 9 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

References (57)

Ultrafast Dynamics of Carotenoid Excited States — From Solution to Natural and Artificial Systems Polivka, Tomas; Sundstroem, Villy ChemInform, Vol. 35, Issue 24 https://doi.org/10.1002/chin.200424298	journal	June 2004
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria Demmig-Adams, Barbara; Garab, Gyozo; Adams III, William Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-9032-1	book	January 2014
Electrochromism: a useful probe to study algal photosynthesis Bailleul, Benjamin; Cardol, Pierre; Breyton, Cécile Photosynthesis Research, Vol. 106, Issue 1-2 https://doi.org/10.1007/s11120-010-9579-z	journal	July 2010
The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting Holleboom, Christoph-Peter; Walla, Peter J. Photosynthesis Research, Vol. 119, Issue 1-2 https://doi.org/10.1007/s11120-013-9815-4	journal	April 2013
Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica Litvín, Radek; Bína, David; Herbstová, Miroslava Photosynthesis Research, Vol. 130, Issue 1-3 https://doi.org/10.1007/s11120-016-0234-1	journal	February 2016
Evidence of the supercomplex organization of photosystem II and light-harvesting complexes in Nannochloropsis granulata Umetani, Ikumi; Kunugi, Motoshi; Yokono, Makio Photosynthesis Research, Vol. 136, Issue 1 https://doi.org/10.1007/s11120-017-0438-z	journal	August 2017
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3 https://doi.org/10.1016/S0005-2728(89)80347-0	journal	August 1989
Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence Young, A. J.; Frank, H. A. Journal of Photochemistry and Photobiology B: Biology, Vol. 36, Issue 1 https://doi.org/10.1016/S1011-1344(96)07397-6	journal	October 1996
Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis Nilkens, Manuela; Kress, Eugen; Lambrev, Petar Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 4 https://doi.org/10.1016/j.bbabio.2010.01.001	journal	April 2010
Photoprotective sites in the violaxanthin–chlorophyll a binding Protein (VCP) from Nannochloropsis gaditana Carbonera, Donatella; Agostini, Alessandro; Di Valentin, Marilena Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 8 https://doi.org/10.1016/j.bbabio.2014.03.014	journal	August 2014
Efficient light-harvesting using non-carbonyl carotenoids: Energy transfer dynamics in the VCP complex from Nannochloropsis oceanica Keşan, Gürkan; Litvín, Radek; Bína, David Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 4 https://doi.org/10.1016/j.bbabio.2015.12.011	journal	April 2016
Photoprotection strategies of the alga Nannochloropsis gaditana Chukhutsina, Volha U.; Fristedt, Rikard; Morosinotto, Tomas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 7 https://doi.org/10.1016/j.bbabio.2017.05.003	journal	July 2017
Acclimation of Nannochloropsis gaditana to different illumination regimes: Effects on lipids accumulation Simionato, Diana; Sforza, Eleonora; Corteggiani Carpinelli, Elisa Bioresource Technology, Vol. 102, Issue 10 https://doi.org/10.1016/j.biortech.2011.02.100	journal	May 2011
Biodiesel from microalgae Chisti, Yusuf Biotechnology Advances, Vol. 25, Issue 3, p. 294-306 https://doi.org/10.1016/j.biotechadv.2007.02.001	journal	May 2007
A transthylakoid proton gradient and inhibitors induce a non-photochemical fluorescence quenching in unicellular algae Nannochloropsis sp. Cao, Shaona; Zhang, Xiaowen; Xu, Dong FEBS Letters, Vol. 587, Issue 9 https://doi.org/10.1016/j.febslet.2012.12.031	journal	March 2013
Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes Park, Soomin; Fischer, Alexandra L.; Li, Zhirong The Journal of Physical Chemistry Letters, Vol. 8, Issue 22 https://doi.org/10.1021/acs.jpclett.7b02486	journal	November 2017
Molecular Origin of Photoprotection in Cyanobacteria Probed by Watermarked Femtosecond Stimulated Raman Spectroscopy Hontani, Yusaku; Kloz, Miroslav; Polívka, Tomáš The Journal of Physical Chemistry Letters, Vol. 9, Issue 7 https://doi.org/10.1021/acs.jpclett.8b00663	journal	March 2018
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems Polívka, Tomáš; Sundström, Villy Chemical Reviews, Vol. 104, Issue 4 https://doi.org/10.1021/cr020674n	journal	April 2004
Carotenoid Photoprotection in Artificial Photosynthetic Antennas Kloz, Miroslav; Pillai, Smitha; Kodis, Gerdenis Journal of the American Chemical Society, Vol. 133, Issue 18 https://doi.org/10.1021/ja1103553	journal	May 2011
Chlorophyll-Carotenoid Excitation Energy Transfer in High-Light-Exposed Thylakoid Membranes Investigated by Snapshot Transient Absorption Spectroscopy Park, Soomin; Fischer, Alexandra L.; Steen, Collin J. Journal of the American Chemical Society, Vol. 140, Issue 38 https://doi.org/10.1021/jacs.8b04844	journal	September 2018
Understanding the Energy Transfer Function of LHCII, the Major Light-Harvesting Complex of Green Plants ^† van Amerongen, Herbert; van Grondelle, Rienk The Journal of Physical Chemistry B, Vol. 105, Issue 3 https://doi.org/10.1021/jp0028406	journal	January 2001
Excited-State Kinetics of the Carotenoid S ₁ State in LHC II and Two-Photon Excitation Spectra of Lutein and β-Carotene in Solution: Efficient Car S ₁ →Chl Electronic Energy Transfer via Hot S ₁ States? ^† Walla, Peter J.; Linden, Patricia A.; Ohta, Kaoru The Journal of Physical Chemistry A, Vol. 106, Issue 10 https://doi.org/10.1021/jp011495x	journal	March 2002
Charge-Transfer State as a Possible Signature of a Zeaxanthin−Chlorophyll Dimer in the Non-photochemical Quenching Process in Green Plants Dreuw, Andreas; Fleming, Graham R.; Head-Gordon, Martin The Journal of Physical Chemistry B, Vol. 107, Issue 27 https://doi.org/10.1021/jp034562r	journal	July 2003
Excited-State Processes in the Carotenoid Zeaxanthin after Excess Energy Excitation Billsten, Helena Hörvin; Pan, Jingxi; Sinha, Subrata The Journal of Physical Chemistry A, Vol. 109, Issue 31 https://doi.org/10.1021/jp052227s	journal	August 2005
Correlation of Car S ₁ → Chl with Chl → Car S ₁ Energy Transfer Supports the Excitonic Model in Quenched Light Harvesting Complex II Liao, Pen-Nan; Holleboom, Christoph-Peter; Wilk, Laura The Journal of Physical Chemistry B, Vol. 114, Issue 47 https://doi.org/10.1021/jp1034163	journal	December 2010
A pigment-binding protein essential for regulation of photosynthetic light harvesting Li, Xiao-Ping; Björkman, Olle; Shih, Connie Nature, Vol. 403, Issue 6768 https://doi.org/10.1038/35000131	journal	January 2000
Identification of a mechanism of photoprotective energy dissipation in higher plants Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06262	journal	November 2007
An ancient light-harvesting protein is critical for the regulation of algal photosynthesis Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth Nature, Vol. 462, Issue 7272 https://doi.org/10.1038/nature08587	journal	November 2009
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection Kondo, Toru; Pinnola, Alberta; Chen, Wei Jia Nature Chemistry, Vol. 9, Issue 8 https://doi.org/10.1038/nchem.2818	journal	July 2017
Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins Staleva, Hristina; Komenda, Josef; Shukla, Mahendra K. Nature Chemical Biology, Vol. 11, Issue 4 https://doi.org/10.1038/nchembio.1755	journal	February 2015
PsbS interactions involved in the activation of energy dissipation in Arabidopsis Correa-Galvis, Viviana; Poschmann, Gereon; Melzer, Michael Nature Plants, Vol. 2, Issue 2 https://doi.org/10.1038/nplants.2015.225	journal	February 2016
The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching Sacharz, Joanna; Giovagnetti, Vasco; Ungerer, Petra Nature Plants, Vol. 3, Issue 2 https://doi.org/10.1038/nplants.2016.225	journal	January 2017
Different carotenoid conformations have distinct functions in light-harvesting regulation in plants Liguori, Nicoletta; Xu, Pengqi; van Stokkum, Ivo H. M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02239-z	journal	December 2017
Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop Głowacka, Katarzyna; Kromdijk, Johannes; Kucera, Katherine Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03231-x	journal	March 2018
Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants Balevičius, Vytautas; Fox, Kieran F.; Bricker, William P. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-13720-6	journal	October 2017
RETRACTED ARTICLE: Increased biomass productivity in green algae by tuning non-photochemical quenching Berteotti, Silvia; Ballottari, Matteo; Bassi, Roberto Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep21339	journal	February 2016
Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting Ma, Y. -Z.; Holt, N. E.; Li, X. -P. Proceedings of the National Academy of Sciences, Vol. 100, Issue 8 https://doi.org/10.1073/pnas.0736959100	journal	April 2003
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls Bode, S.; Quentmeier, C. C.; Liao, P. -N. Proceedings of the National Academy of Sciences, Vol. 106, Issue 30 https://doi.org/10.1073/pnas.0903536106	journal	July 2009
Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization Alboresi, A.; Gerotto, C.; Giacometti, G. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 24 https://doi.org/10.1073/pnas.1002873107	journal	May 2010
An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light Bailleul, B.; Rogato, A.; de Martino, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 42 https://doi.org/10.1073/pnas.1007703107	journal	October 2010
Fluorescence lifetime snapshots reveal two rapidly reversible mechanisms of photoprotection in live cells of Chlamydomonas reinhardtii Amarnath, K.; Zaks, J.; Park, S. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1205303109	journal	May 2012
A kinetic model of rapidly reversible nonphotochemical quenching Zaks, J.; Amarnath, K.; Kramer, D. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 39 https://doi.org/10.1073/pnas.1211017109	journal	August 2012
Distinct roles of the photosystem II protein PsbS and zeaxanthin in the regulation of light harvesting in plants revealed by fluorescence lifetime snapshots Sylak-Glassman, Emily J.; Malnoë, Alizée; De Re, Eleonora Proceedings of the National Academy of Sciences, Vol. 111, Issue 49 https://doi.org/10.1073/pnas.1418317111	journal	November 2014
Dissecting and modeling zeaxanthin- and lutein-dependent nonphotochemical quenching in Arabidopsis thaliana Leuenberger, Michelle; Morris, Jonathan M.; Chan, Arnold M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 33 https://doi.org/10.1073/pnas.1704502114	journal	June 2017
Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting Bennett, Doran I. G.; Fleming, Graham R.; Amarnath, Kapil Proceedings of the National Academy of Sciences, Vol. 115, Issue 41 https://doi.org/10.1073/pnas.1806597115	journal	September 2018
Zeaxanthin Radical Cation Formation in Minor Light-harvesting Complexes of Higher Plant Antenna Avenson, Thomas J.; Ahn, Tae Kyu; Zigmantas, Donatas Journal of Biological Chemistry, Vol. 283, Issue 6 https://doi.org/10.1074/jbc.M705645200	journal	November 2007
Lutein Can Act as a Switchable Charge Transfer Quencher in the CP26 Light-harvesting Complex Avenson, Thomas J.; Ahn, Tae Kyu; Niyogi, Krishna K. Journal of Biological Chemistry, Vol. 284, Issue 5 https://doi.org/10.1074/jbc.M807192200	journal	November 2008
Ascorbate Deficiency Can Limit Violaxanthin De-Epoxidase Activity in Vivo Müller-Moulé, Patricia; Conklin, Patricia L.; Niyogi, Krishna K. Plant Physiology, Vol. 128, Issue 3 https://doi.org/10.1104/pp.010924	journal	March 2002
Non-Photochemical Quenching. A Response to Excess Light Energy Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K. Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1558	journal	April 2001
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting Holt, N. E. Science, Vol. 307, Issue 5708 https://doi.org/10.1126/science.1105833	journal	January 2005
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Ahn, T. K.; Avenson, T. J.; Ballottari, M. Science, Vol. 320, Issue 5877 https://doi.org/10.1126/science.1154800	journal	May 2008
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection Kromdijk, Johannes; Głowacka, Katarzyna; Leonelli, Lauriebeth Science, Vol. 354, Issue 6314 https://doi.org/10.1126/science.aai8878	journal	November 2016
Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production Adarme-Vega, T.; Lim, David K. Y.; Timmins, Matthew Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-96	journal	January 2012
Analysis of LhcSR3, a Protein Essential for Feedback De-Excitation in the Green Alga Chlamydomonas reinhardtii Bonente, Giulia; Ballottari, Matteo; Truong, Thuy B. PLoS Biology, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pbio.1000577	journal	January 2011
Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779 Vieler, Astrid; Wu, Guangxi; Tsai, Chia-Hong PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003064	journal	November 2012
Reactive oxygen species generation and signaling in plants Tripathy, Baishnab Charan; Oelmüller, Ralf Plant Signaling & Behavior, Vol. 7, Issue 12 https://doi.org/10.4161/psb.22455	journal	December 2012
Biodiesel from Microalgae Nagarajan, R.; Jain, Aatmesh; Vora, Kamalkishore Symposium on International Automotive Technology 2017, SAE Technical Paper Series https://doi.org/10.4271/2017-26-0077	conference	January 2017

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