IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44959-z.html
   My bibliography  Save this article

An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano

Author

Listed:
  • Ravi R. Sonani

    (University of Virginia School of Medicine)

  • Lee K. Palmer

    (University of Texas Medical Branch)

  • Nathaniel C. Esteves

    (Virginia Tech)

  • Abigail A. Horton

    (Virginia Tech)

  • Amanda L. Sebastian

    (Virginia Tech)

  • Rebecca J. Kelly

    (Virginia Tech)

  • Fengbin Wang

    (University of Virginia School of Medicine
    University of Alabama at Birmingham)

  • Mark A. B. Kreutzberger

    (University of Virginia School of Medicine)

  • William K. Russell

    (University of Texas Medical Branch)

  • Petr G. Leiman

    (University of Texas Medical Branch)

  • Birgit E. Scharf

    (Virginia Tech)

  • Edward H. Egelman

    (University of Virginia School of Medicine)

Abstract

A contractile sheath and rigid tube assembly is a widespread apparatus used by bacteriophages, tailocins, and the bacterial type VI secretion system to penetrate cell membranes. In this mechanism, contraction of an external sheath powers the motion of an inner tube through the membrane. The structure, energetics, and mechanism of the machinery imply rigidity and straightness. The contractile tail of Agrobacterium tumefaciens bacteriophage Milano is flexible and bent to varying degrees, which sets it apart from other contractile tail-like systems. Here, we report structures of the Milano tail including the sheath-tube complex, baseplate, and putative receptor-binding proteins. The flexible-to-rigid transformation of the Milano tail upon contraction can be explained by unique electrostatic properties of the tail tube and sheath. All components of the Milano tail, including sheath subunits, are crosslinked by disulfides, some of which must be reduced for contraction to occur. The putative receptor-binding complex of Milano contains a tailspike, a tail fiber, and at least two small proteins that form a garland around the distal ends of the tailspikes and tail fibers. Despite being flagellotropic, Milano lacks thread-like tail filaments that can wrap around the flagellum, and is thus likely to employ a different binding mechanism.

Suggested Citation

  • Ravi R. Sonani & Lee K. Palmer & Nathaniel C. Esteves & Abigail A. Horton & Amanda L. Sebastian & Rebecca J. Kelly & Fengbin Wang & Mark A. B. Kreutzberger & William K. Russell & Petr G. Leiman & Birg, 2024. "An extensive disulfide bond network prevents tail contraction in Agrobacterium tumefaciens phage Milano," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44959-z
    DOI: 10.1038/s41467-024-44959-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44959-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44959-z?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. Shuji Kanamaru & Petr G. Leiman & Victor A. Kostyuchenko & Paul R. Chipman & Vadim V. Mesyanzhinov & Fumio Arisaka & Michael G. Rossmann, 2002. "Structure of the cell-puncturing device of bacteriophage T4," Nature, Nature, vol. 415(6871), pages 553-557, January.
    3. Zhen-Lin Chen & Jia-Ming Meng & Yong Cao & Ji-Li Yin & Run-Qian Fang & Sheng-Bo Fan & Chao Liu & Wen-Feng Zeng & Yue-He Ding & Dan Tan & Long Wu & Wen-Jing Zhou & Hao Chi & Rui-Xiang Sun & Meng-Qiu Do, 2019. "A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    4. Peng Ge & Dean Scholl & Nikolai S. Prokhorov & Jaycob Avaylon & Mikhail M. Shneider & Christopher Browning & Sergey A. Buth & Michel Plattner & Urmi Chakraborty & Ke Ding & Petr G. Leiman & Jeff F. Mi, 2020. "Action of a minimal contractile bactericidal nanomachine," Nature, Nature, vol. 580(7805), pages 658-662, April.
    5. 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. Xiaoying Cai & Yao He & Iris Yu & Anthony Imani & Dean Scholl & Jeff F. Miller & Z. Hong Zhou, 2024. "Atomic structures of a bacteriocin targeting Gram-positive bacteria," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Matthew Day & Bilal Tetik & Milena Parlak & Yasser Almeida-Hernández & Markus Räschle & Farnusch Kaschani & Heike Siegert & Anika Marko & Elsa Sanchez-Garcia & Markus Kaiser & Isabel A. Barker & Laure, 2024. "TopBP1 utilises a bipartite GINS binding mode to support genome replication," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Aleksandra Levina & Kaelin D. Fleming & John E. Burke & Thomas A. Leonard, 2022. "Activation of the essential kinase PDK1 by phosphoinositide-driven trans-autophosphorylation," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Rong-Cheng Yu & Feng Yang & Hong-Yan Zhang & Pu Hou & Kang Du & Jie Zhu & Ning Cui & Xudong Xu & Yuxing Chen & Qiong Li & Cong-Zhao Zhou, 2024. "Structure of the intact tail machine of Anabaena myophage A-1(L)," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Yichen Zhong & Hakimeh Moghaddas Sani & Bishnu P. Paudel & Jason K. K. Low & Ana P. G. Silva & Stefan Mueller & Chandrika Deshpande & Santosh Panjikar & Xavier J. Reid & Max J. Bedward & Antoine M. Oi, 2022. "The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. 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.
    20. 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.

    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:15:y:2024:i:1:d:10.1038_s41467-024-44959-z. 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.