Molecular diversity and evolution of far-red light-acclimated photosystem I

Gisriel, Christopher J.; Bryant, Donald A.; Brudvig, Gary W.; Cardona, Tanai

doi:10.3389/fpls.2023.1289199

Molecular diversity and evolution of far-red light-acclimated photosystem I

Journal Article · Sun Nov 19 00:00:00 EST 2023 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2023.1289199· OSTI ID:2339814

Gisriel, Christopher J. ^[1]; Bryant, Donald A. ^[2]; Brudvig, Gary W. ^[3]; Cardona, Tanai ^[4]

Yale University, New Haven, CT (United States); Yale University; Yale University
Pennsylvania State University, University Park, PA (United States)
Yale University, New Haven, CT (United States)
Imperial College London (United Kingdom); Queen Mary University of London (United Kingdom)

The need to acclimate to different environmental conditions is central to the evolution of cyanobacteria. Far-red light (FRL) photoacclimation, or FaRLiP, is an acclimation mechanism that enables certain cyanobacteria to use FRL to drive photosynthesis. During this process, a well-defined gene cluster is upregulated, resulting in changes to the photosystems that allow them to absorb FRL to perform photochemistry. Because FaRLiP is widespread, and because it exemplifies cyanobacterial adaptation mechanisms in nature, it is of interest to understand its molecular evolution. Here, we performed a phylogenetic analysis of the photosystem I subunits encoded in the FaRLiP gene cluster and analyzed the available structural data to predict ancestral characteristics of FRL-absorbing photosystem I. The analysis suggests that FRL-specific photosystem I subunits arose relatively late during the evolution of cyanobacteria when compared with some of the FRL-specific subunits of photosystem II, and that the order Nodosilineales, which include strains like Halomicronema hongdechloris and Synechococcus sp. PCC 7335, could have obtained FaRLiP via horizontal gene transfer. We show that the ancestral form of FRL-absorbing photosystem I contained three chlorophyll f-binding sites in the PsaB2 subunit, and a rotated chlorophyll a molecule in the A0B site of the electron transfer chain. Along with our previous study of photosystem II expressed during FaRLiP, these studies describe the molecular evolution of the photosystem complexes encoded by the FaRLiP gene cluster.

View Accepted Manuscript (DOE)

Research Organization:: Yale University, New Haven, CT (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-05ER15646

OSTI ID:: 2339814

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 14; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

A fresh look at the evolution and diversification of photochemical reaction centers Cardona, Tanai Photosynthesis Research, Vol. 126, Issue 1 https://doi.org/10.1007/s11120-014-0065-x	journal	December 2014
Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002 Shen, Gaozhong; Canniffe, Daniel P.; Ho, Ming-Yang Photosynthesis Research, Vol. 140, Issue 1 https://doi.org/10.1007/s11120-018-00610-9	journal	January 2019
Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered Photosystem I complexes Kurashov, Vasily; Ho, Ming-Yang; Shen, Gaozhong Photosynthesis Research, Vol. 141, Issue 2 https://doi.org/10.1007/s11120-019-00616-x	journal	February 2019
Far-red light allophycocyanin subunits play a role in chlorophyll d accumulation in far-red light Bryant, Donald A.; Shen, Gaozhong; Turner, Gavin M. Photosynthesis Research, Vol. 143, Issue 1 https://doi.org/10.1007/s11120-019-00689-8	journal	November 2019
Characterization of cyanobacterial allophycocyanins absorbing far-red light Soulier, Nathan; Laremore, Tatiana N.; Bryant, Donald A. Photosynthesis Research, Vol. 145, Issue 3 https://doi.org/10.1007/s11120-020-00775-2	journal	July 2020
The structural basis of far-red light absorbance by allophycocyanins Soulier, Nathan; Bryant, Donald A. Photosynthesis Research, Vol. 147, Issue 1 https://doi.org/10.1007/s11120-020-00787-y	journal	October 2020
Modeling Photosystem I with the alternative reaction center protein PsaB2 in the nitrogen fixing cyanobacterium Nostoc punctiforme Magnuson, Ann; Krassen, Henning; Stensjö, Karin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 9 https://doi.org/10.1016/j.bbabio.2011.05.004	journal	September 2011
Charge separation in Photosystem II: A comparative and evolutionary overview Cardona, Tanai; Sedoud, Arezki; Cox, Nicholas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1 https://doi.org/10.1016/j.bbabio.2011.07.012	journal	January 2012
Thylakoid membrane function in heterocysts Magnuson, Ann; Cardona, Tanai Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 3 https://doi.org/10.1016/j.bbabio.2015.10.016	journal	March 2016
Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis Malavath, Tirupathi; Caspy, Ido; Netzer-El, Sigal Y. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 9 https://doi.org/10.1016/j.bbabio.2018.02.002	journal	September 2018
Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: Evidence that the A–1 cofactor is chlorophyll f Hastings, Gary; Makita, Hiroki; Agarwala, Neva Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 6 https://doi.org/10.1016/j.bbabio.2019.04.002	journal	June 2019
Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light Ho, Ming-Yang; Niedzwiedzki, Dariusz M.; MacGregor-Chatwin, Craig Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 4 https://doi.org/10.1016/j.bbabio.2019.148064	journal	April 2020
Evidence that chlorophyll f functions solely as an antenna pigment in far-red-light photosystem I from Fischerella thermalis PCC 7521 Cherepanov, Dmitry A.; Shelaev, Ivan V.; Gostev, Fedor E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 5-6 https://doi.org/10.1016/j.bbabio.2020.148184	journal	June 2020
The primary donor of far-red photosystem II: ChlD1 or PD2? Judd, Martyna; Morton, Jennifer; Nürnberg, Dennis Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 10 https://doi.org/10.1016/j.bbabio.2020.148248	journal	October 2020
Mass spectrometry and spectroscopic characterization of a tetrameric photosystem I supercomplex from Leptolyngbya ohadii, a desiccation-tolerant cyanobacterium Niedzwiedzki, Dariusz M.; Magdaong, Nikki Cecil M.; Su, Xinyang Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1864, Issue 2 https://doi.org/10.1016/j.bbabio.2023.148955	journal	April 2023
Quantitative assessment of chlorophyll types in cryo-EM maps of photosystem I acclimated to far-red light Gisriel, Christopher J.; Huang, Hao-Li; Reiss, Krystle M. BBA Advances, Vol. 1 https://doi.org/10.1016/j.bbadva.2021.100019	journal	January 2021
Breaking the Red Limit: Efficient Trapping of Long-Wavelength Excitations in Chlorophyll-f-Containing Photosystem I Tros, Martijn; Mascoli, Vincenzo; Shen, Gaozhong Chem, Vol. 7, Issue 1 https://doi.org/10.1016/j.chempr.2020.10.024	journal	January 2021
Unique constitution of photosystem I with a novel subunit in the cyanobacterium Gloeobacter violaceus PCC 7421 Inoue, Hidetoshi; Tsuchiya, Tohru; Satoh, Soichirou FEBS Letters, Vol. 578, Issue 3 https://doi.org/10.1016/j.febslet.2004.11.013	journal	November 2004
Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation Gisriel, Christopher J.; Flesher, David A.; Shen, Gaozhong Journal of Biological Chemistry, Vol. 298, Issue 1 https://doi.org/10.1016/j.jbc.2021.101408	journal	January 2022
Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red light reveals the functions of chlorophylls d and f Gisriel, Christopher J.; Shen, Gaozhong; Ho, Ming-Yang Journal of Biological Chemistry, Vol. 298, Issue 1 https://doi.org/10.1016/j.jbc.2021.101424	journal	January 2022
Structure of a dimeric photosystem II complex from a cyanobacterium acclimated to far-red light Gisriel, Christopher J.; Shen, Gaozhong; Flesher, David A. Journal of Biological Chemistry, Vol. 299, Issue 1 https://doi.org/10.1016/j.jbc.2022.102815	journal	January 2023
Light regulation of pigment and photosystem biosynthesis in cyanobacteria Ho, Ming-Yang; Soulier, Nathan T.; Canniffe, Daniel P. Current Opinion in Plant Biology, Vol. 37 https://doi.org/10.1016/j.pbi.2017.03.006	journal	June 2017
Metabolic Adaptations in a H ₂ Producing Heterocyst-Forming Cyanobacterium: Potentials and Implications for Biological Engineering Ekman, Martin; Ow, Saw Yen; Holmqvist, Marie Journal of Proteome Research, Vol. 10, Issue 4 https://doi.org/10.1021/pr101055v	journal	April 2011
Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution Jordan, Patrick; Fromme, Petra; Witt, Horst Tobias Nature, Vol. 411, Issue 6840 https://doi.org/10.1038/35082000	journal	June 2001
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation Chen, Meng-Yun; Teng, Wen-Kai; Zhao, Liang The ISME Journal, Vol. 15, Issue 1 https://doi.org/10.1038/s41396-020-00775-z	journal	September 2020
Global distribution of a chlorophyll f cyanobacterial marker Antonaru, Laura A.; Cardona, Tanai; Larkum, Anthony W. D. The ISME Journal, Vol. 14, Issue 9 https://doi.org/10.1038/s41396-020-0670-y	journal	May 2020
Structural basis for the adaptation and function of chlorophyll f in photosystem I Kato, Koji; Shinoda, Toshiyuki; Nagao, Ryo Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-13898-5	journal	January 2020
Timing the evolution of antioxidant enzymes in cyanobacteria Boden, Joanne S.; Konhauser, Kurt O.; Robbins, Leslie J. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-24396-y	journal	August 2021
Chlorophyll f synthesis by a super-rogue photosystem II complex Trinugroho, Joko P.; Bečková, Martina; Shao, Shengxi Nature Plants, Vol. 6, Issue 3 https://doi.org/10.1038/s41477-020-0616-4	journal	March 2020
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Origin of marine planktonic cyanobacteria Sánchez-Baracaldo, Patricia Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17418	journal	December 2015
Femtosecond infrared spectroscopy of chlorophyll f-containing photosystem I Zamzam, Noura; Kaucikas, Marius; Nürnberg, Dennis J. Physical Chemistry Chemical Physics, Vol. 21, Issue 3 https://doi.org/10.1039/C8CP05627G	journal	January 2019
Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing Shih, P. M.; Wu, D.; Latifi, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058 https://doi.org/10.1073/pnas.1217107110	journal	December 2012
Femtosecond visible transient absorption spectroscopy of chlorophyll- f -containing photosystem II Zamzam, Noura; Rakowski, Rafal; Kaucikas, Marius Proceedings of the National Academy of Sciences, Vol. 117, Issue 37 https://doi.org/10.1073/pnas.2006016117	journal	August 2020
Complete Genome Structure of Gloeobacter violaceus PCC 7421, a Cyanobacterium that Lacks Thylakoids Nakamura, Y. DNA Research, Vol. 10, Issue 4 https://doi.org/10.1093/dnares/10.4.137	journal	January 2003
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era Minh, Bui Quang; Schmidt, Heiko A.; Chernomor, Olga Molecular Biology and Evolution, Vol. 37, Issue 5 https://doi.org/10.1093/molbev/msaa015	journal	February 2020
Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria Cardona, Tanai; Murray, James W.; Rutherford, A. William Molecular Biology and Evolution, Vol. 32, Issue 5 https://doi.org/10.1093/molbev/msv024	journal	February 2015
JPred4: a protein secondary structure prediction server Drozdetskiy, Alexey; Cole, Christian; Procter, James Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv332	journal	April 2015
Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria Pardo-De la Hoz, Carlos J.; Magain, Nicolas; Piatkowski, Bryan Systematic Biology, Vol. 72, Issue 3 https://doi.org/10.1093/sysbio/syad008	journal	February 2023
Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks Huson, Daniel H.; Scornavacca, Celine Systematic Biology, Vol. 61, Issue 6 https://doi.org/10.1093/sysbio/sys062	journal	September 2012
Thinking twice about the evolution of photosynthesis Cardona, Tanai Open Biology, Vol. 9, Issue 3 https://doi.org/10.1098/rsob.180246	journal	March 2019
The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages Fournier, G. P.; Moore, K. R.; Rangel, L. T. Proceedings of the Royal Society B: Biological Sciences, Vol. 288, Issue 1959 https://doi.org/10.1098/rspb.2021.0675	journal	September 2021
Impact of energy limitations on function and resilience in long-wavelength Photosystem II Viola, Stefania; Roseby, William; Santabarabara, Stefano eLife https://doi.org/10.1101/2022.04.05.486971	preprint	April 2022
Adaptive and acclimative responses of cyanobacteria to far-red light: Responses of cyanobacteria to far-red light Gan, Fei; Bryant, Donald A. Environmental Microbiology, Vol. 17, Issue 10 https://doi.org/10.1111/1462-2920.12992	journal	August 2015
An updated classification of cyanobacterial orders and families based on phylogenomic and polyphasic analysis Strunecký, Otakar; Ivanova, Anna Pavlovna; Mareš, Jan Journal of Phycology, Vol. 59, Issue 1 https://doi.org/10.1111/jpy.13304	journal	January 2023
The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis Gisriel, Christopher; Shen, Gaozhong; Kurashov, Vasily Science Advances, Vol. 6, Issue 6 https://doi.org/10.1126/sciadv.aay6415	journal	February 2020
Changes in supramolecular organization of cyanobacterial thylakoid membrane complexes in response to far-red light photoacclimation MacGregor-Chatwin, Craig; Nürnberg, Dennis J.; Jackson, Philip J. Science Advances, Vol. 8, Issue 6 https://doi.org/10.1126/sciadv.abj4437	journal	February 2022
Helical allophycocyanin nanotubes absorb far-red light in a thermophilic cyanobacterium Gisriel, Christopher J.; Elias, Eduard; Shen, Gaozhong Science Advances, Vol. 9, Issue 12 https://doi.org/10.1126/sciadv.adg0251	journal	March 2023
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
Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II Ho, M. -Y.; Shen, G.; Canniffe, D. P. Science, Vol. 353, Issue 6302 https://doi.org/10.1126/science.aaf9178	journal	July 2016
Photochemistry beyond the red limit in chlorophyll f–containing photosystems Nürnberg, Dennis J.; Morton, Jennifer; Santabarbara, Stefano Science, Vol. 360, Issue 6394 https://doi.org/10.1126/science.aar8313	journal	June 2018
The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat Olsen, Millie T.; Nowack, Shane; Wood, Jason M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00604	journal	June 2015
The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light Nowack, Shane; Olsen, Millie T.; Schaible, George A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00626	journal	June 2015
Global Transcriptional Profiling of the Cyanobacterium Chlorogloeopsis fritschii PCC 9212 in Far-Red Light: Insights Into the Regulation of Chlorophyll d Synthesis Ho, Ming-Yang; Bryant, Donald A. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00465	journal	March 2019
Identification of far-red light acclimation in an endolithic Chroococcidiopsis strain and associated genomic features: Implications for oxygenic photosynthesis on exoplanets Billi, Daniela; Napoli, Alessandro; Mosca, Claudia Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.933404	journal	August 2022
Occurrence of Far-Red Light Photoacclimation (FaRLiP) in Diverse Cyanobacteria Gan, Fei; Shen, Gaozhong; Bryant, Donald Life, Vol. 5, Issue 1 https://doi.org/10.3390/life5010004	journal	December 2014
Molecular Evolution of Far-Red Light-Acclimated Photosystem II Gisriel, Christopher J.; Cardona, Tanai; Bryant, Donald A. Microorganisms, Vol. 10, Issue 7 https://doi.org/10.3390/microorganisms10071270	journal	June 2022
Structural basis for the absence of low-energy chlorophylls in a photosystem I trimer from Gloeobacter violaceus Kato, Koji; Hamaguchi, Tasuku; Nagao, Ryo eLife, Vol. 11 https://doi.org/10.7554/eLife.73990	journal	April 2022

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