The deep-rooted origin of disulfide-rich spider venom toxins

  1. Naeem Yusuf Shaikh
  2. Kartik Sunagar  Is a corresponding author
  1. Indian Institute of Science Bangalore, India

Abstract

Spider venoms are a complex concoction of enzymes, polyamines, inorganic salts and disulfide-rich peptides (DRPs). Although DRPs are widely distributed and abundant, their evolutionary origin has remained elusive. This knowledge gap stems from the extensive molecular divergence of DRPs and a lack of sequence and structural data from diverse lineages. By evaluating DRPs under a comprehensive phylogenetic, structural and evolutionary framework, we have not only identified 78 novel spider toxin superfamilies but also provided the first evidence for their common origin. We trace the origin of these toxin superfamilies to a primordial knot - which we name 'Adi Shakti', after the creator of the Universe according to Hindu mythology - 375 MYA in the common ancestor of Araneomorphae and Mygalomorphae. As the lineages under evaluation constitute nearly 60% of extant spiders, our findings provide fascinating insights into the early evolution and diversification of the spider venom arsenal. Reliance on a single molecular toxin scaffold by nearly all spiders is in complete contrast to most other venomous animals that have recruited into their venoms diverse toxins with independent origins. By comparatively evaluating the molecular evolutionary histories of araneomorph and mygalomorph spider venom toxins, we highlight their contrasting evolutionary diversification rates. Our results also suggest that venom deployment (e.g., prey capture or self-defense) influences evolutionary diversification of DRP toxin superfamilies.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 2, 3, 4 and 5.

Article and author information

Author details

  1. Naeem Yusuf Shaikh

    Evolutionary Venomics Lab, Indian Institute of Science Bangalore, Bengaluru, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9903-8484
  2. Kartik Sunagar

    Evolutionary Venomics Lab, Indian Institute of Science Bangalore, Bengaluru, India
    For correspondence
    ksunagar@iisc.ac.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0998-1581

Funding

The Wellcome Trust DBT India Alliance (IA/I/19/2/504647)

  • Kartik Sunagar

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ariel Chipman, The Hebrew University of Jerusalem, Israel

Version history

  1. Received: September 28, 2022
  2. Preprint posted: October 7, 2022 (view preprint)
  3. Accepted: February 8, 2023
  4. Accepted Manuscript published: February 9, 2023 (version 1)
  5. Version of Record published: March 15, 2023 (version 2)

Copyright

© 2023, Shaikh & Sunagar

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Naeem Yusuf Shaikh
  2. Kartik Sunagar
(2023)
The deep-rooted origin of disulfide-rich spider venom toxins
eLife 12:e83761.
https://doi.org/10.7554/eLife.83761

Share this article

https://doi.org/10.7554/eLife.83761

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