IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40550-0.html
   My bibliography  Save this article

Domain loss enabled evolution of novel functions in the snake three-finger toxin gene superfamily

Author

Listed:
  • Ivan Koludarov

    (TUM (Technical University of Munich) Department of Informatics, Bioinformatics & Computational Biology—i12)

  • Tobias Senoner

    (TUM (Technical University of Munich) Department of Informatics, Bioinformatics & Computational Biology—i12)

  • Timothy N. W. Jackson

    (University of Melbourne)

  • Daniel Dashevsky

    (Commonwealth Scientific & Industrial Research Organisation)

  • Michael Heinzinger

    (TUM (Technical University of Munich) Department of Informatics, Bioinformatics & Computational Biology—i12)

  • Steven D. Aird

    (7744-23 Hotaka Ariake)

  • Burkhard Rost

    (TUM (Technical University of Munich) Department of Informatics, Bioinformatics & Computational Biology—i12
    Institute for Advanced Study (TUM-IAS)
    TUM School of Life Sciences Weihenstephan (WZW))

Abstract

Three-finger toxins (3FTXs) are a functionally diverse family of toxins, apparently unique to venoms of caenophidian snakes. Although the ancestral function of 3FTXs is antagonism of nicotinic acetylcholine receptors, redundancy conferred by the accumulation of duplicate genes has facilitated extensive neofunctionalization, such that derived members of the family interact with a range of targets. 3FTXs are members of the LY6/UPAR family, but their non-toxin ancestor remains unknown. Combining traditional phylogenetic approaches, manual synteny analysis, and machine learning techniques (including AlphaFold2 and ProtT5), we have reconstructed a detailed evolutionary history of 3FTXs. We identify their immediate ancestor as a non-secretory LY6, unique to squamate reptiles, and propose that changes in molecular ecology resulting from loss of a membrane-anchoring domain and changes in gene expression, paved the way for the evolution of one of the most important families of snake toxins.

Suggested Citation

  • Ivan Koludarov & Tobias Senoner & Timothy N. W. Jackson & Daniel Dashevsky & Michael Heinzinger & Steven D. Aird & Burkhard Rost, 2023. "Domain loss enabled evolution of novel functions in the snake three-finger toxin gene superfamily," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40550-0
    DOI: 10.1038/s41467-023-40550-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40550-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40550-0?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. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Nicholas R. Casewell & Gavin A. Huttley & Wolfgang Wüster, 2012. "Dynamic evolution of venom proteins in squamate reptiles," Nature Communications, Nature, vol. 3(1), pages 1-10, January.
    3. Martin Steinegger & Johannes Söding, 2018. "Clustering huge protein sequence sets in linear time," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    4. 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.
    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. David Moi & Shunsuke Nishio & Xiaohui Li & Clari Valansi & Mauricio Langleib & Nicolas G. Brukman & Kateryna Flyak & Christophe Dessimoz & Daniele de Sanctis & Kathryn Tunyasuvunakool & John Jumper & , 2022. "Discovery of archaeal fusexins homologous to eukaryotic HAP2/GCS1 gamete fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Jeffrey A. Ruffolo & Lee-Shin Chu & Sai Pooja Mahajan & Jeffrey J. Gray, 2023. "Fast, accurate antibody structure prediction from deep learning on massive set of natural antibodies," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Julia Koehler Leman & Pawel Szczerbiak & P. Douglas Renfrew & Vladimir Gligorijevic & Daniel Berenberg & Tommi Vatanen & Bryn C. Taylor & Chris Chandler & Stefan Janssen & Andras Pataki & Nick Carrier, 2023. "Sequence-structure-function relationships in the microbial protein universe," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Junhui Peng & Li Zhao, 2024. "The origin and structural evolution of de novo genes in Drosophila," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. 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.
    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. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. Eliza S. Nieweglowska & Axel F. Brilot & Melissa Méndez-Moran & Claire Kokontis & Minkyung Baek & Junrui Li & Yifan Cheng & David Baker & Joseph Bondy-Denomy & David A. Agard, 2023. "The ϕPA3 phage nucleus is enclosed by a self-assembling 2D crystalline lattice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. Sash Lopaticki & Robyn McConville & Alan John & Niall Geoghegan & Shihab Deen Mohamed & Lisa Verzier & Ryan W. J. Steel & Cindy Evelyn & Matthew T. O’Neill & Niccolay Madiedo Soler & Nichollas E. Scot, 2022. "Tryptophan C-mannosylation is critical for Plasmodium falciparum transmission," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Radoslaw Pluta & Eric Aragón & Nicholas A. Prescott & Lidia Ruiz & Rebeca A. Mees & Blazej Baginski & Julia R. Flood & Pau Martin-Malpartida & Joan Massagué & Yael David & Maria J. Macias, 2022. "Molecular basis for DNA recognition by the maternal pioneer transcription factor FoxH1," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Xinheng He & Lifen Zhao & Yinping Tian & Rui Li & Qinyu Chu & Zhiyong Gu & Mingyue Zheng & Yusong Wang & Shaoning Li & Hualiang Jiang & Yi Jiang & Liuqing Wen & Dingyan Wang & Xi Cheng, 2024. "Highly accurate carbohydrate-binding site prediction with DeepGlycanSite," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    18. 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.
    19. 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.
    20. 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.

    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_s41467-023-40550-0. 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.