Controllable Phycobilin Modification: An Alternative Photoacclimation Response in Cryptophyte Algae

Spangler, Leah C.; Yu, Mina; Jeffrey, Philip D.; Scholes, Gregory D.

doi:10.1021/acscentsci.1c01209

Title: Controllable Phycobilin Modification: An Alternative Photoacclimation Response in Cryptophyte Algae

Journal Article · 08 February 2022 · ACS Central Science

DOI: https://doi.org/10.1021/acscentsci.1c01209 · OSTI ID:1982013

Spangler, Leah C. ^[1]; Yu, Mina ^[1]; Jeffrey, Philip D. ^[1];

^[1]

Princeton University, NJ (United States)

Cryptophyte algae are well-known for their ability to survive under low light conditions using their auxiliary light harvesting antennas, phycobiliproteins. Mainly acting to absorb light where chlorophyll cannot (500-650 nm), phycobiliproteins also play an instrumental role in helping cryptophyte algae respond to changes in light intensity through the process of photoacclimation. Until recently, photoacclimation in cryptophyte algae was only observed as a change in the cellular concentration of phycobiliproteins; however, an additional photoacclimation response was recently discovered that causes shifts in the phycobiliprotein absorbance peaks following growth under red, blue, or green light. Here, we reproduce this newly identified photoacclimation response in two species of cryptophyte algae and elucidate the origin of the response on the protein level. We compare isolated native and photoacclimated phycobiliproteins for these two species using spectroscopy and mass spectrometry, and we report the X-ray structures of each phycobiliprotein and the corresponding photoacclimated complex. We find that neither the protein sequences nor the protein structures are modified by photoacclimation. We conclude that cryptophyte algae change one chromophore in the phycobiliprotein β subunits in response to changes in the spectral quality of light. Ultrafast pump-probe spectroscopy shows that the energy transfer is weakly affected by photoacclimation.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States); Princeton University, NJ (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); Canadian Institute for Advanced Research (CIFAR)

Grant/Contract Number:: SC0012704

OSTI ID:: 1982013

Journal Information:: ACS Central Science, Journal Name: ACS Central Science Journal Issue: 3 Vol. 8; ISSN 2374-7943

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (40)

Cooperative Subunit Refolding of a Light‐Harvesting Protein through a Self‐Chaperone Mechanism Laos, Alistair J.; Dean, Jacob C.; Toa, Zi S. D. Angewandte Chemie, Vol. 129, Issue 29 https://doi.org/10.1002/ange.201607921	journal	February 2017
Spectral Variability in Phycocyanin Cryptophyte Antenna Complexes is Controlled by Changes in the α‐Polypeptide Chains Corbella, Marina; Cupellini, Lorenzo; Lipparini, Filippo ChemPhotoChem, Vol. 3, Issue 9 https://doi.org/10.1002/cptc.201900045	journal	May 2019
Light-Harvesting Antennas in Photosynthesis Green, Beverley R.; Parson, William W. Advances in Photosynthesis and Respiration https://doi.org/10.1007/978-94-017-2087-8	book	January 2003
Cryptomonad biliproteins: Bilin types and locations Wedemayer, Gary J.; Kidd, Daniel G.; Glazer, Alexander N. Photosynthesis Research, Vol. 48, Issue 1-2 https://doi.org/10.1007/BF00041006	journal	May 1996
Freeze fracture immunocytochemistry of light-harvesting pigment complexes in a cryptophyte Vesk, M.; Dwarte, D.; Fowler, S. Protoplasma, Vol. 170, Issue 3-4 https://doi.org/10.1007/BF01378791	journal	September 1992
Phycobiliprotein diffusion in chloroplasts of cryptophyte Rhodomonas CS24 Mirkovic, Tihana; Wilk, Krystyna E.; Curmi, Paul M. G. Photosynthesis Research, Vol. 100, Issue 1 https://doi.org/10.1007/s11120-009-9412-8	journal	February 2009
Phycobilisome: architecture of a light-harvesting supercomplex Watanabe, Mai; Ikeuchi, Masahiko Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9905-3	journal	October 2013
Proteomic analysis of the phycobiliprotein antenna of the cryptophyte alga Guillardia theta cultured under different light intensities Kieselbach, Thomas; Cheregi, Otilia; Green, Beverley R. Photosynthesis Research, Vol. 135, Issue 1-3 https://doi.org/10.1007/s11120-017-0400-0	journal	May 2017
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
Vibronic Wavepackets and Energy Transfer in Cryptophyte Light-Harvesting Complexes Jumper, Chanelle C.; van Stokkum, Ivo H. M.; Mirkovic, Tihana The Journal of Physical Chemistry B, Vol. 122, Issue 24 https://doi.org/10.1021/acs.jpcb.8b02629	journal	May 2018
Photosynthetic Light-Harvesting Is Tuned by the Heterogeneous Polarizable Environment of the Protein Curutchet, Carles; Kongsted, Jacob; Muñoz-Losa, Aurora Journal of the American Chemical Society, Vol. 133, Issue 9 https://doi.org/10.1021/ja110053y	journal	March 2011
Mediation of Ultrafast Light-Harvesting by a Central Dimer in Phycoerythrin 545 Studied by Transient Absorption and Global Analysis Doust, Alexander B.; van Stokkum, Ivo H. M.; Larsen, Delmar S. The Journal of Physical Chemistry B, Vol. 109, Issue 29 https://doi.org/10.1021/jp051173j	journal	July 2005
How Energy Funnels from the Phycoerythrin Antenna Complex to Photosystem I and Photosystem II in Cryptophyte Rhodomonas CS24 Cells van der Weij-De Wit, Chantal D.; Doust, Alexander B.; van Stokkum, Ivo H. M. The Journal of Physical Chemistry B, Vol. 110, Issue 49 https://doi.org/10.1021/jp061546w	journal	November 2006
Energy Flow in the Cryptophyte PE545 Antenna Is Directed by Bilin Pigment Conformation Curutchet, Carles; Novoderezhkin, Vladimir I.; Kongsted, Jacob The Journal of Physical Chemistry B, Vol. 117, Issue 16 https://doi.org/10.1021/jp305033d	journal	October 2012
Coherent Oscillations in the PC577 Cryptophyte Antenna Occur in the Excited Electronic State McClure, Scott D.; Turner, Daniel B.; Arpin, Paul C. The Journal of Physical Chemistry B, Vol. 118, Issue 5 https://doi.org/10.1021/jp411924c	journal	January 2014
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
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
Chromatic adaptation and the evolution of light color sensing in cyanobacteria Kehoe, D. M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 20 https://doi.org/10.1073/pnas.1004510107	journal	May 2010
Phycoerythrin-specific bilin lyase-isomerase controls blue-green chromatic acclimation in marine Synechococcus Shukla, A.; Biswas, A.; Blot, N. Proceedings of the National Academy of Sciences, Vol. 109, Issue 49 https://doi.org/10.1073/pnas.1211777109	journal	November 2012
Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus Flombaum, P.; Gallegos, J. L.; Gordillo, R. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 24 https://doi.org/10.1073/pnas.1307701110	journal	May 2013
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
Self-regulating genomic island encoding tandem regulators confers chromatic acclimation to marine Synechococcus Sanfilippo, Joseph E.; Nguyen, Adam A.; Karty, Jonathan A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 21 https://doi.org/10.1073/pnas.1600625113	journal	May 2016
Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria Grébert, Théophile; Doré, Hugo; Partensky, Frédéric Proceedings of the National Academy of Sciences, Vol. 115, Issue 9 https://doi.org/10.1073/pnas.1717069115	journal	February 2018
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
Insights into the Biosynthesis and Assembly of Cryptophycean Phycobiliproteins Overkamp, Kristina E.; Gasper, Raphael; Kock, Klaus Journal of Biological Chemistry, Vol. 289, Issue 39 https://doi.org/10.1074/jbc.M114.591131	journal	September 2014
Localization of phycoerythrin at the lumenal surface of the thylakoid membrane in Rhodomonas lens. Ludwig, M.; Gibbs, S. P. Journal of Cell Biology, Vol. 108, Issue 3 https://doi.org/10.1083/jcb.108.3.875	journal	March 1989
The Timescale of Phenotypic Plasticity and Its Impact on Competition in Fluctuating Environments Stomp, Maayke; van Dijk, Mark A.; van Overzee, Harriët M. J. The American Naturalist, Vol. 172, Issue 5 https://doi.org/10.1086/591680	journal	November 2008
Emerging Perspectives on the Mechanisms, Regulation, and Distribution of Light Color Acclimation in Cyanobacteria Gutu, Andrian; Kehoe, David M. Molecular Plant, Vol. 5, Issue 1 https://doi.org/10.1093/mp/ssr054	journal	January 2012
Unique Location of the Phycobiliprotein Light-Harvesting Pigment in the Cryptophyceae Spear-bernstein, Laurel; Miller, Kenneth R. Journal of Phycology, Vol. 25, Issue 3 https://doi.org/10.1111/j.1529-8817.1989.tb00245.x	journal	September 1989
Light capture and pigment diversity in marine and freshwater cryptophytes Cunningham, Brady R.; Greenwold, Matthew J.; Lachenmyer, Eric M. Journal of Phycology, Vol. 55, Issue 3 https://doi.org/10.1111/jpy.12816	journal	December 2018
Photopigment, Absorption, and Growth Responses of Marine Cryptophytes to Varying Spectral Irradiance Heidenreich, Kristin M.; Richardson, Tammi L. Journal of Phycology, Vol. 56, Issue 2 https://doi.org/10.1111/jpy.12962	journal	February 2020
Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light Gan, F.; Zhang, S.; Rockwell, N. C. Science, Vol. 345, Issue 6202 https://doi.org/10.1126/science.1256963	journal	August 2014
Biochemical Bases of Type IV Chromatic Adaptation in Marine Synechococcus spp Everroad, Craig; Six, Christophe; Partensky, Frédéric Journal of Bacteriology, Vol. 188, Issue 9 https://doi.org/10.1128/JB.188.9.3345-3356.2006	journal	May 2006
Occurrence and nature of chromatic adaptation in cyanobacteria. Tandeau de Marsac, N. Journal of Bacteriology, Vol. 130, Issue 1 https://doi.org/10.1128/jb.130.1.82-91.1977	journal	January 1977
The phycobilisome, a light-harvesting complex responsive to environmental conditions. Grossman, A. R.; Schaefer, M. R.; Chiang, G. G. Microbiological Reviews, Vol. 57, Issue 3 https://doi.org/10.1128/mr.57.3.725-749.1993	journal	January 1993
Phycoerythrin Association with Photosystem II in the Cryptophyte Alga Rhodomonas salina Stadnichuk, I. N.; Novikova, T. M.; Miniuk, G. S. Biochemistry (Moscow), Vol. 85, Issue 6 https://doi.org/10.1134/S000629792006005X	journal	June 2020
Chromatic Acclimation in Cyanobacteria: A Diverse and Widespread Process for Optimizing Photosynthesis Sanfilippo, Joseph E.; Garczarek, Laurence; Partensky, Frédéric Annual Review of Microbiology, Vol. 73, Issue 1 https://doi.org/10.1146/annurev-micro-020518-115738	journal	September 2019
Non-Photochemical Quenching in Cryptophyte Alga Rhodomonas salina Is Located in Chlorophyll a/c Antennae Kaňa, Radek; Kotabová, Eva; Sobotka, Roman PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029700	journal	January 2012
What Happened to the Phycobilisome? Green, Beverley R. Biomolecules, Vol. 9, Issue 11 https://doi.org/10.3390/biom9110748	journal	November 2019
Carotenoids in Algae: Distributions, Biosyntheses and Functions Takaichi, Shinichi Marine Drugs, Vol. 9, Issue 6 https://doi.org/10.3390/md9061101	journal	June 2011