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. Harry H. Low & Jan Löwe, 2006. "A bacterial dynamin-like protein," Nature, Nature, vol. 444(7120), pages 766-769, December.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    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. Ye Yuan & Lei Chen & Kexu Song & Miaomiao Cheng & Ling Fang & Lingfei Kong & Lanlan Yu & Ruonan Wang & Zhendong Fu & Minmin Sun & Qian Wang & Chengjun Cui & Haojue Wang & Jiuyang He & Xiaonan Wang & Y, 2024. "Stable peptide-assembled nanozyme mimicking dual antifungal actions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Chih-Wei Chen & Chi Su & Chang-Yu Huang & Xuan-Rong Huang & Xiaojing Cuili & Tung Chao & Chun-Hsiang Fan & Cheng-Wei Ting & Yi-Wei Tsai & Kai-Chien Yang & Ti-Yen Yeh & Sung-Tsang Hsieh & Yi-Ju Chen & , 2024. "NME3 is a gatekeeper for DRP1-dependent mitophagy in hypoxia," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Wonchul Shin & Ben Zucker & Nidhi Kundu & Sung Hoon Lee & Bo Shi & Chung Yu Chan & Xiaoli Guo & Jonathan T. Harrison & Jaymie Moore Turechek & Jenny E. Hinshaw & Michael M. Kozlov & Ling-Gang Wu, 2022. "Molecular mechanics underlying flat-to-round membrane budding in live secretory cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Ivica Odorčić & Mohamed Belal Hamed & Sam Lismont & Lucía Chávez-Gutiérrez & Rouslan G. Efremov, 2024. "Apo and Aβ46-bound γ-secretase structures provide insights into amyloid-β processing by the APH-1B isoform," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Léon Faure & Bastien Mollet & Wolfram Liebermeister & Jean-Loup Faulon, 2023. "A neural-mechanistic hybrid approach improving the predictive power of genome-scale metabolic models," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Tian Zhu & Merry H. Ma, 2022. "Deriving the Optimal Strategy for the Two Dice Pig Game via Reinforcement Learning," Stats, MDPI, vol. 5(3), pages 1-14, August.
    9. Stella Vitt & Simone Prinz & Martin Eisinger & Ulrich Ermler & Wolfgang Buckel, 2022. "Purification and structural characterization of the Na+-translocating ferredoxin: NAD+ reductase (Rnf) complex of Clostridium tetanomorphum," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    10. 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.
    11. Riya Shah & Thomas C. Panagiotou & Gregory B. Cole & Trevor F. Moraes & Brigitte D. Lavoie & Christopher A. McCulloch & Andrew Wilde, 2024. "The DIAPH3 linker specifies a β-actin network that maintains RhoA and Myosin-II at the cytokinetic furrow," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Yashan Yang & Qianqian Shao & Mingcheng Guo & Lin Han & Xinyue Zhao & Aohan Wang & Xiangyun Li & Bo Wang & Ji-An Pan & Zhenguo Chen & Andrei Fokine & Lei Sun & Qianglin Fang, 2024. "Capsid structure of bacteriophage ΦKZ provides insights into assembly and stabilization of jumbo phages," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    13. 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.
    14. Bret M. Boyd & Ian James & Kevin P. Johnson & Robert B. Weiss & Sarah E. Bush & Dale H. Clayton & Colin Dale, 2024. "Stochasticity, determinism, and contingency shape genome evolution of endosymbiotic bacteria," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    16. 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.
    17. 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.
    18. 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.
    19. Ahrum Son & Hyunsoo Kim & Jolene K. Diedrich & Casimir Bamberger & Daniel B. McClatchy & Stuart A. Lipton & John R. Yates, 2024. "Using in vivo intact structure for system-wide quantitative analysis of changes in proteins," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    20. Justin N. Vaughn & Sandra E. Branham & Brian Abernathy & Amanda M. Hulse-Kemp & Adam R. Rivers & Amnon Levi & William P. Wechter, 2022. "Graph-based pangenomics maximizes genotyping density and reveals structural impacts on fungal resistance in melon," Nature Communications, Nature, vol. 13(1), pages 1-14, 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.