Red‑on‑Yellow Queen: Bio‑Layer Interferometry Reveals Functional Diversity Within Micrurus Venoms and Toxin Resistance in Prey Species

Daniel Dashevsky; Richard Harris; Christina N Zdenek; Melissa Benard-Valle; Alejandro  Alagón; José A.  A Portes‑Junior; Anita  M Tanaka‑Azevedo; Kathleen  F Grego; Sávio  S Sant’Anna; Nathaniel Frank; Bryan G Fry

doi:10.1007/s00239-024-10176-x

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Red‑on‑Yellow Queen: Bio‑Layer Interferometry Reveals Functional Diversity Within Micrurus Venoms and Toxin Resistance in Prey Species

Journal article

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Red‑on‑Yellow Queen: Bio‑Layer Interferometry Reveals Functional Diversity Within Micrurus Venoms and Toxin Resistance in Prey Species

Daniel Dashevsky, Richard Harris, Christina N Zdenek, Melissa Benard-Valle, Alejandro Alagón, José A. A Portes‑Junior, Anita M Tanaka‑Azevedo, Kathleen F Grego, Sávio S Sant’Anna, Nathaniel Frank, …

Journal of Molecular Evolution, Vol.92(3), pp.317-328

2024

DOI: https://doi.org/10.1007/s00239-024-10176-x

PMID: 38814340

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Abstract

Three-finger toxin

Mimotope

Arms race

Coral snake

Elapid

Snakes in the family Elapidae largely produce venoms rich in three-finger toxins (3FTx) that bind to the α 1 subunit of nicotinic acetylcholine receptors (nAChRs), impeding ion channel activity. These neurotoxins immobilize the prey by disrupting muscle contraction. Coral snakes of the genus Micrurus are specialist predators who produce many 3FTx, making them an interesting system for examining the coevolution of these toxins and their targets in prey animals. We used a bio-layer interferometry technique to measure the binding interaction between 15 Micrurus venoms and 12 taxon-specific mimotopes designed to resemble the orthosteric binding region of the muscular nAChR subunit. We found that Micrurus venoms vary greatly in their potency on this assay and that this variation follows phylogenetic patterns rather than previously reported patterns of venom composition. The long-tailed Micrurus tend to have greater binding to nAChR orthosteric sites than their short-tailed relatives and we conclude this is the likely ancestral state. The repeated loss of this activity may be due to the evolution of 3FTx that bind to other regions of the nAChR. We also observed variations in the potency of the venoms depending on the taxon of the target mimotope. Rather than a pattern of prey-specificity, we found that mimotopes modeled after snake nAChRs are less susceptible to Micrurus venoms and that this resistance is partly due to a characteristic tryptophan→serine mutation within the orthosteric site in all snake mimotopes. This resistance may be part of a Red Queen arms race between coral snakes and their prey.

Details

Title: Red‑on‑Yellow Queen: Bio‑Layer Interferometry Reveals Functional Diversity Within Micrurus Venoms and Toxin Resistance in Prey Species
Authors: Daniel Dashevsky (Corresponding Author) - Australian National Insect Collection
Richard Harris (Author) - The University of Queensland
Christina N Zdenek - The University of Queensland
Melissa Benard-Valle (Author) - Technical University of Denmark
Alejandro Alagón (Author) - Universidad Nacional Autónoma de México
José A. A Portes‑Junior (Author) - Instituto Butantan
Anita M Tanaka‑Azevedo (Author) - Instituto Butantan
Kathleen F Grego (Author) - Instituto Butantan
Sávio S Sant’Anna (Author) - Instituto Butantan
Nathaniel Frank (Author) - Oshkosh
Bryan G Fry (Author) - The University of Queensland
Publication details: Journal of Molecular Evolution, Vol.92(3), pp.317-328
Publisher: Springer New York LLC
Date published: 2024
DOI: 10.1007/s00239-024-10176-x
ISSN: 1432-1432; 0022-2844
PMID: 38814340
Copyright note: © The Author(s) 2024. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Grants: Functional evolution and therapeutic potential of snake venom coagulotoxins, DP190100304, Australian Research Council (Australia, Canberra) - ARC
Grant note: DD was funded by a UQ Centennial Scholarship from The University of Queensland, a Research Training Program scholarship from the Australian Government Department of Education and Training, and a CSIRO Early Research Career Postdoctoral Fellowship from the Commonwealth Science & Industry Research Organisation. AA was funded by Pronaii 303045 (CONAHCYT, Mexico). JAPJ was funded by the Fundação de Amparo á Pesquisa do Estado de São Paulo under the grant 2018/25749-8.
Organisation Unit: Centre for Bioinnovation
Language: English
Record Identifier: 991177843202621
Output Type: Journal article

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Web Of Science research areas: Biochemistry & Molecular Biology; Evolutionary Biology; Genetics & Heredity

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