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A promiscuous mechanism to phase separate eukaryotic carbon fixation in the green lineage
Open accessPreprint — published as 10.1038/s41477-024-01812-x · Paper page
Abstract
CO 2 fixation is commonly limited by inefficiency of the CO 2 -fixing enzyme Rubisco. Eukaryotic algae concentrate and fix CO 2 in phase-separated condensates called pyrenoids, which complete up to one-third of global CO 2 fixation. Condensation of Rubisco in pyrenoids is dependent on interaction with disordered linker proteins that show little conservation between species. We developed a sequence-independent bioinformatic pipeline to identify linker proteins in green algae. We report the linker from Chlorella and demonstrate that it binds a conserved site on the Rubisco large subunit. We show the Chlorella linker phase separates Chlamydomonas Rubisco and that despite their separation by ∼800 million years of evolution, the Chlorella linker can support the formation of a functional pyrenoid in Chlamydomonas . This cross-species reactivity extends to plants, with the Chlorella linker able to drive condensation of some native plant Rubiscos in vitro and in planta . Our results represent an exciting frontier for pyrenoid engineering in plants, which is modelled to increase crop yields.
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Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
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Research works printed but not linked: 69
- 10.1126/science.281.5374.237 · DOI · Paper page
- 10.1021/bi2002289 · DOI · Paper page
- Shih, P. M. et al. Biochemical characterization of predicted Precambrian RuBisCO. Nat. Commun. 7, 10382 (2016). · DOI
- 2024, Rubisco is evolving for improved catalytic efficiency and CO2 assimilation in plants, Proc. Natl. Acad. Sci. U. S. A, 121, e2321050121, 10.1073/pnas.2321050121 · DOI
- 10.1073/pnas.0600605103 · DOI
- 2021, Targeted knockdown of ribulose-1, 5-bisphosphate carboxylase-oxygenase in rice mesophyll cells, J. Plant Physiol, 260, 153395, 10.1016/j.jplph.2021.153395 · DOI
- 1991, Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS : II. Flux-control coefficients for photosynthesis in varying light, CO2, and air humidity. Planta, 183, 555
- Fichtner, K. et al. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS. Planta 190, (1993). · DOI
- 1984, Rate-limiting factors in leaf photosynthesis, I. Carbon fluxes in the calvin cycle. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 767, 432
- 10.1007/BF00194276 · DOI
- 10.1007/BF00386231 · DOI · Paper page
- 2013, Rubisco: still the most abundant protein of Earth?, The New phytologist, 198, 1, 10.1111/nph.12197 · DOI
- 10.1111/pce.12425 · DOI
- 10.1073/pnas.1816654116 · DOI
- 10.1073/pnas.1522866113 · DOI
- 2021, Pyrenoids: CO2-fixing phase separated liquid organelles, Biochim. Biophys. Acta Mol. Cell Res, 118949, 1868
- 2023, A linker protein from a red-type pyrenoid phase separates with Rubisco via oligomerizing sticker motifs, Proc. Natl. Acad. Sci. U. S. A, 120, e2304833120, 10.1073/pnas.2304833120 · DOI
- 10.1093/plphys/kiac373 · DOI
- 2022, Modelling the pyrenoid-based CO2-concentrating mechanism provides insights into its operating principles and a roadmap for its engineering into crops, Nat Plants, 8, 583, 10.1038/s41477-022-01153-7 · DOI
- 10.1073/pnas.1909706116 · DOI
- 10.1073/pnas.1904587116 · DOI
- 10.1093/jxb/erz275 · DOI
- 10.1038/s41467-020-20132-0 · DOI
- 2024, SAGA1 and SAGA2 promote starch formation around proto-pyrenoids in Arabidopsis chloroplasts, Proc. Natl. Acad. Sci. U. S. A, 121, e2311013121, 10.1073/pnas.2311013121 · DOI
- 10.1073/pnas.1207719109 · DOI
- 10.1016/j.cell.2017.08.008 · DOI
- 2018, Genomic characterization reveals significant divergence within Chlorella sorokiniana (Chlorellales, Trebouxiophyceae). Algal Research, 35, 449, 10.1016/j.algal.2018.09.012 · DOI
- 10.1073/pnas.1910060117 · DOI
- Guo, W. , et al. In-situ high-resolution 3D imaging combined with proteomics and metabolomics reveals enlargement of subcellular architecture and enhancement of photosynthesis pathways in nuclear-irradiated Chlorella pyrenoidosa . Chem. Eng. J. 430, 133037 (2022). · DOI
- 10.1038/s41467-018-07624-w · DOI
- 10.1101/gad.331520.119 · DOI
- He, S. et al. The structural basis of Rubisco phase separation in the pyrenoid. Nature Plants 1–11 (2020). · DOI
- 2020, Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation, Nat. Struct. Mol. Biol, 27, 281, 10.1038/s41594-020-0387-7 · DOI
- 10.1038/s41586-019-0880-5 · DOI
- 10.1038/ncomms9843 · DOI
- Kellogg, E. & Juliano, N . The structure and function of RuBisCO and their implications for systematic studies. Am. J. Bot. 84, 413 (1997). · DOI
- 10.1111/nph.16577 · DOI
- 10.1073/pnas.1210993109 · DOI
- 10.1038/nsmb.2171 · DOI
- 10.1006/jmbi.2000.3724 · DOI
- 2024, Algal chloroplast pyrenoids: Evidence for convergent evolution, Proceedings of the National Academy of Sciences of the United States of America, 121, e2402546121
- GrandPre, T. et al. Impact of Linker Length on Biomolecular Condensate Formation. PRX Life 1, 023013 (2023). · DOI
- Payne-Dwyer, A ., et al. Predicting Rubisco:Linker Condensation from Titration in the Dilute Phase. arXiv [cond-mat.soft] (2023). · DOI
- Choi, J.-M. & Pappu, R. V . The Stickers and Spacers Framework for Describing Phase Behavior of Multivalent Intrinsically Disordered Proteins. Biophys. J. 118, 492a (2020). · DOI
- 10.1111/nph.14414 · DOI
- Meyer, M. T. et al. Assembly of the algal CO2-fixing organelle, the pyrenoid, is guided by a Rubisco-binding motif. Sci Adv 6, (2020). · DOI
- 10.1111/j.1365-313X.2011.04537.x · DOI
- 10.1093/nar/gky384 · DOI
- 10.1101/2022.06.06.494887 · DOI
- Newman, A. M. & Cooper, J. B . XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8, 382 (2007). · DOI
- 10.1038/S41592-022-01488-1 · DOI · Paper page
- Barratt, L. J. , Reynolds, I. J. , Franco Ortega, S. & Harper, A. L . Transcriptomic and co-expression network analyses on diverse wheat landraces identifies candidate master regulators of the response to early drought. Front. Plant Sci. 14, 1212559 (2023). · DOI
- 2020, DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput, Nat. Methods, 17, 41, 10.1038/s41592-019-0638-x · DOI
- Almagro Armenteros , J. J ., et al. Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance 2, (2019). · DOI
- 10.1021/sb4001504 · DOI
- 10.1104/pp.17.00554 · DOI
- 10.1093/protein/14.12.993 · DOI
- 10.1016/j.jsb.2012.09.006 · DOI · Paper page
- Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. Elife 7, (2018). · DOI
- 10.1016/j.jsb.2015.08.008 · DOI
- 10.1107/S205225251801463X · DOI
- 10.1002/jcc.20084 · DOI
- 2010, Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr, 66, 486, 10.1107/S0907444910007493 · DOI · Paper page
- 10.1107/S0907444909052925 · DOI · Paper page
- 10.1107/S0907444909042073 · DOI · Paper page
- 10.1002/PRO.3943 · DOI
- 10.1002/prot.20449 · DOI
- Yamano, T. & Fukuzawa, H . Transformation of the Model Microalga Chlamydomonas reinhardtii Without Cell-Wall Removal. in Electroporation Protocols: Microorganism, Mammalian System, and Nanodevice (eds. Li, S., Chang, L. & Teissie, J.) 155–161 (Springer US, New York, NY, 2020). · DOI
- 10.1093/molbev/mst010 · DOI · Paper page
Metadata
- Authors
- Barrett, J., Naduthodi, M. I. S., Mao, Y., Dégut, C., Musiał, S., Salter, A., Leake, M. C., Plevin, M. J., McCormick, A. J., Blaza, J. N., & Mackinder, L. C. M.
- Affiliations
- University of York (GB)
- University of Edinburgh (GB)
- Corresponding author
- Mackinder, Luke C.M.
- ORCID
- Venue
- Nature Plants
- Publisher
- openRxiv
- Published
- 2024-04-11
- Volume
- 10
- Issue
- 11
- Pages
- 1801-1813
- ISSN
- 2055-026X (ISSN-L)
- PMC
- PMC11570498
- OpenAlex
- W4403253348
- Cited by
- 37
- References
- 1
- Citations by year
- 2026: 20 · 2025: 11 · 2024: 6
- FWCI
- 5.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Nature Plants (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Bill and Melinda Gates Foundation (INV-054558)
- Wellcome Trust (206161, Z/17/Z, 206161/Z/17/Z)
- UK Research and Innovation (MR/T040742/1)
- Research Councils UK (MR/T040742/1, EP/W024063/1)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (019.221EN.010)
- Darwin Trust of Edinburgh
- Directorate for Biological Sciences
- Engineering and Physical Sciences Research Council (EP/W024063/1)
- Biotechnology and Biological Sciences Research Council (BB/S015337/1, BB/M0111511a, BB/S015337/11, BB/Y000323/1, BB/T007222/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Keywords
- pyrenoid, Rubisco, phase separation, linker proteins, CO2 fixation, Chlorella, Chlamydomonas, green algae, Rubisco large subunit, protein condensates, crop yield, CO2-concentrating mechanism
- MeSH terms
- Carbon Dioxide, Chlamydomonas, Chlorella, Ribulose-Bisphosphate Carboxylase, Carbon Cycle
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