IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37746-9.html
   My bibliography  Save this article

SynDLP is a dynamin-like protein of Synechocystis sp. PCC 6803 with eukaryotic features

Author

Listed:
  • Lucas Gewehr

    (Johannes Gutenberg University Mainz)

  • Benedikt Junglas

    (Ernst Ruska-Centre for Microscopy and Spectroscopy with Electrons (ER-C-3): Structural Biology
    Institute for Biological Information Processing (IBI-6): Cellular Structural Biology)

  • Ruven Jilly

    (Johannes Gutenberg University Mainz)

  • Johannes Franz

    (Max Planck Institute for Polymer Research)

  • Wenyu Eva Zhu

    (Johannes Gutenberg University Mainz)

  • Tobias Weidner

    (Department of Chemistry, Aarhus University)

  • Mischa Bonn

    (Max Planck Institute for Polymer Research)

  • Carsten Sachse

    (Ernst Ruska-Centre for Microscopy and Spectroscopy with Electrons (ER-C-3): Structural Biology
    Institute for Biological Information Processing (IBI-6): Cellular Structural Biology
    Heinrich Heine University)

  • Dirk Schneider

    (Johannes Gutenberg University Mainz
    Johannes Gutenberg University Mainz)

Abstract

Dynamin-like proteins are membrane remodeling GTPases with well-understood functions in eukaryotic cells. However, bacterial dynamin-like proteins are still poorly investigated. SynDLP, the dynamin-like protein of the cyanobacterium Synechocystis sp. PCC 6803, forms ordered oligomers in solution. The 3.7 Å resolution cryo-EM structure of SynDLP oligomers reveals the presence of oligomeric stalk interfaces typical for eukaryotic dynamin-like proteins. The bundle signaling element domain shows distinct features, such as an intramolecular disulfide bridge that affects the GTPase activity, or an expanded intermolecular interface with the GTPase domain. In addition to typical GD-GD contacts, such atypical GTPase domain interfaces might be a GTPase activity regulating tool in oligomerized SynDLP. Furthermore, we show that SynDLP interacts with and intercalates into membranes containing negatively charged thylakoid membrane lipids independent of nucleotides. The structural characteristics of SynDLP oligomers suggest it to be the closest known bacterial ancestor of eukaryotic dynamin.

Suggested Citation

  • Lucas Gewehr & Benedikt Junglas & Ruven Jilly & Johannes Franz & Wenyu Eva Zhu & Tobias Weidner & Mischa Bonn & Carsten Sachse & Dirk Schneider, 2023. "SynDLP is a dynamin-like protein of Synechocystis sp. PCC 6803 with eukaryotic features," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37746-9
    DOI: 10.1038/s41467-023-37746-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37746-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37746-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Joshua S. Chappie & Sharmistha Acharya & Marilyn Leonard & Sandra L. Schmid & Fred Dyda, 2010. "G domain dimerization controls dynamin's assembly-stimulated GTPase activity," Nature, Nature, vol. 465(7297), pages 435-440, May.
    2. Manfu Wang & Xiangyang Guo & Xiuna Yang & Bing Zhang & Jie Ren & Aijun Liu & Yajun Ran & Bing Yan & Fang Chen & Luke W. Guddat & Junjie Hu & Jun Li & Zihe Rao, 2019. "Mycobacterial dynamin-like protein IniA mediates membrane fission," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Raghav Kalia & Ray Yu-Ruei Wang & Ali Yusuf & Paul V. Thomas & David A. Agard & Janet M. Shaw & Adam Frost, 2018. "Structural basis of mitochondrial receptor binding and constriction by DRP1," Nature, Nature, vol. 558(7710), pages 401-405, June.
    4. Yu-Lu Cao & Shuxia Meng & Yang Chen & Jian-Xiong Feng & Dong-Dong Gu & Bing Yu & Yu-Jie Li & Jin-Yu Yang & Shuang Liao & David C. Chan & Song Gao, 2017. "MFN1 structures reveal nucleotide-triggered dimerization critical for mitochondrial fusion," Nature, Nature, vol. 542(7641), pages 372-376, February.
    5. Song Gao & Alexander von der Malsburg & Susann Paeschke & Joachim Behlke & Otto Haller & Georg Kochs & Oliver Daumke, 2010. "Structural basis of oligomerization in the stalk region of dynamin-like MxA," Nature, Nature, vol. 465(7297), pages 502-506, May.
    6. Agnidipta Ghosh & Gerrit J. K. Praefcke & Louis Renault & Alfred Wittinghofer & Christian Herrmann, 2006. "How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP," Nature, Nature, vol. 440(7080), pages 101-104, March.
    7. Jiwei Liu & Jeffrey K. Noel & Harry H. Low, 2018. "Structural basis for membrane tethering by a bacterial dynamin-like pair," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    8. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    9. Katja Faelber & Lea Dietrich & Jeffrey K. Noel & Florian Wollweber & Anna-Katharina Pfitzner & Alexander Mühleip & Ricardo Sánchez & Misha Kudryashev & Nicolas Chiaruttini & Hauke Lilie & Jeanette Sch, 2019. "Structure and assembly of the mitochondrial membrane remodelling GTPase Mgm1," Nature, Nature, vol. 571(7765), pages 429-433, July.
    10. Harry H. Low & Jan Löwe, 2006. "A bacterial dynamin-like protein," Nature, Nature, vol. 444(7120), pages 766-769, December.
    11. Thomas F. Reubold & Katja Faelber & Nuria Plattner & York Posor & Katharina Ketel & Ute Curth & Jeanette Schlegel & Roopsee Anand & Dietmar J. Manstein & Frank Noé & Volker Haucke & Oliver Daumke & Su, 2015. "Crystal structure of the dynamin tetramer," Nature, Nature, vol. 525(7569), pages 404-408, September.
    12. Raoul Hennig & Jennifer Heidrich & Michael Saur & Lars Schmüser & Steven J. Roeters & Nadja Hellmann & Sander Woutersen & Mischa Bonn & Tobias Weidner & Jürgen Markl & Dirk Schneider, 2015. "IM30 triggers membrane fusion in cyanobacteria and chloroplasts," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    13. Tuomas Huokko & Tao Ni & Gregory F. Dykes & Deborah M. Simpson & Philip Brownridge & Fabian D. Conradi & Robert J. Beynon & Peter J. Nixon & Conrad W. Mullineaux & Peijun Zhang & Lu-Ning Liu, 2021. "Probing the biogenesis pathway and dynamics of thylakoid membranes," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    14. Leopold Kong & Kem A. Sochacki & Huaibin Wang & Shunming Fang & Bertram Canagarajah & Andrew D. Kehr & William J. Rice & Marie-Paule Strub & Justin W. Taraska & Jenny E. Hinshaw, 2018. "Cryo-EM of the dynamin polymer assembled on lipid membrane," Nature, Nature, vol. 560(7717), pages 258-262, August.
    15. Genny Orso & Diana Pendin & Song Liu & Jessica Tosetto & Tyler J. Moss & Joseph E. Faust & Massimo Micaroni & Anastasia Egorova & Andrea Martinuzzi & James A. McNew & Andrea Daga, 2010. "Erratum: Homotypic fusion of ER membranes requires the dynamin-like GTPase Atlastin," Nature, Nature, vol. 464(7290), pages 942-942, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Kristy Rochon & Brianna L. Bauer & Nathaniel A. Roethler & Yuli Buckley & Chih-Chia Su & Wei Huang & Rajesh Ramachandran & Maria S. K. Stoll & Edward W. Yu & Derek J. Taylor & Jason A. Mears, 2024. "Structural basis for regulated assembly of the mitochondrial fission GTPase Drp1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    2. Isabel Pérez-Jover & Kristy Rochon & Di Hu & Mukesh Mahajan & Pooja Madan Mohan & Isaac Santos-Pérez & Julene Ormaetxea Gisasola & Juan Manuel Martinez Galvez & Jon Agirre & Xin Qi & Jason A. Mears & , 2024. "Allosteric control of dynamin-related protein 1 through a disordered C-terminal Short Linear Motif," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative AI," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, National Bureau of Economic Research, Inc.
    4. Anthony C. Bishop & Glorisé Torres-Montalvo & Sravya Kotaru & Kyle Mimun & A. Joshua Wand, 2023. "Robust automated backbone triple resonance NMR assignments of proteins using Bayesian-based simulated annealing," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Deyun Qiu & Jinxin V. Pei & James E. O. Rosling & Vandana Thathy & Dongdi Li & Yi Xue & John D. Tanner & Jocelyn Sietsma Penington & Yi Tong Vincent Aw & Jessica Yi Han Aw & Guoyue Xu & Abhai K. Tripa, 2022. "A G358S mutation in the Plasmodium falciparum Na+ pump PfATP4 confers clinically-relevant resistance to cipargamin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Shuo-Shuo Liu & Tian-Xia Jiang & Fan Bu & Ji-Lan Zhao & Guang-Fei Wang & Guo-Heng Yang & Jie-Yan Kong & Yun-Fan Qie & Pei Wen & Li-Bin Fan & Ning-Ning Li & Ning Gao & Xiao-Bo Qiu, 2024. "Molecular mechanisms underlying the BIRC6-mediated regulation of apoptosis and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Dick Schijven & Sourena Soheili-Nezhad & Simon E. Fisher & Clyde Francks, 2024. "Exome-wide analysis implicates rare protein-altering variants in human handedness," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. Xiaoke Yang & Mingqi Zhu & Xue Lu & Yuxin Wang & Junyu Xiao, 2024. "Architecture and activation of human muscle phosphorylase kinase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Zheng Shen & Daxiao Sun & Adriana Savastano & Sára Joana Varga & Maria-Sol Cima-Omori & Stefan Becker & Alf Honigmann & Markus Zweckstetter, 2023. "Multivalent Tau/PSD-95 interactions arrest in vitro condensates and clusters mimicking the postsynaptic density," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Evangelos Katsamakas & Oleg V. Pavlov & Ryan Saklad, 2024. "Artificial intelligence and the transformation of higher education institutions," Papers 2402.08143, arXiv.org.
    11. Efren Garcia-Maldonado & Andrew D. Huber & Sergio C. Chai & Stanley Nithianantham & Yongtao Li & Jing Wu & Shyaron Poudel & Darcie J. Miller & Jayaraman Seetharaman & Taosheng Chen, 2024. "Chemical manipulation of an activation/inhibition switch in the nuclear receptor PXR," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. Katherine A. Ray & Joshua D. Lutgens & Ramesh Bista & Jie Zhang & Ronak R. Desai & Melissa Hirsch & Takeshi Miyazawa & Antonio Cordova & Adrian T. Keatinge-Clay, 2024. "Assessing and harnessing updated polyketide synthase modules through combinatorial engineering," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    13. Fan Lu & Liang Zhu & Thomas Bromberger & Jun Yang & Qiannan Yang & Jianmin Liu & Edward F. Plow & Markus Moser & Jun Qin, 2022. "Mechanism of integrin activation by talin and its cooperation with kindlin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    14. Zengyu Shao & Jiuwei Lu & Nelli Khudaverdyan & Jikui Song, 2024. "Multi-layered heterochromatin interaction as a switch for DIM2-mediated DNA methylation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Yudong Gao & Daichi Shonai & Matthew Trn & Jieqing Zhao & Erik J. Soderblom & S. Alexandra Garcia-Moreno & Charles A. Gersbach & William C. Wetsel & Geraldine Dawson & Dmitry Velmeshev & Yong-hui Jian, 2024. "Proximity analysis of native proteomes reveals phenotypic modifiers in a mouse model of autism and related neurodevelopmental conditions," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    16. Martin F. Peter & Christian Gebhardt & Rebecca Mächtel & Gabriel G. Moya Muñoz & Janin Glaenzer & Alessandra Narducci & Gavin H. Thomas & Thorben Cordes & Gregor Hagelueken, 2022. "Cross-validation of distance measurements in proteins by PELDOR/DEER and single-molecule FRET," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    17. Lauren L. Porter & Allen K. Kim & Swechha Rimal & Loren L. Looger & Ananya Majumdar & Brett D. Mensh & Mary R. Starich & Marie-Paule Strub, 2022. "Many dissimilar NusG protein domains switch between α-helix and β-sheet folds," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. Jutta Diessl & Jens Berndtsson & Filomena Broeskamp & Lukas Habernig & Verena Kohler & Carmela Vazquez-Calvo & Arpita Nandy & Carlotta Peselj & Sofia Drobysheva & Ludovic Pelosi & F.-Nora Vögtle & Fab, 2022. "Manganese-driven CoQ deficiency," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    19. Alexander Kroll & Sahasra Ranjan & Martin K. M. Engqvist & Martin J. Lercher, 2023. "A general model to predict small molecule substrates of enzymes based on machine and deep learning," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Lisa-Marie Appel & Vedran Franke & Johannes Benedum & Irina Grishkovskaya & Xué Strobl & Anton Polyansky & Gregor Ammann & Sebastian Platzer & Andrea Neudolt & Anna Wunder & Lena Walch & Stefanie Kais, 2023. "The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37746-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.