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Giant fish-killing water bug reveals ancient and dynamic venom evolution in Heteroptera

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Abstract

True Bugs (Insecta: Heteroptera) produce venom or saliva with diverse bioactivities depending on their feeding strategies. However, little is known about the molecular evolution of the venom toxins underlying these biological activities. We examined venom of the giant fish-killing water bug Lethocerus distinctifemur (Insecta: Belostomatidae) using infrared spectroscopy, transcriptomics, and proteomics. We report 132 venom proteins including putative enzymes, cytolytic toxins, and antimicrobial peptides. Over 73% (96 proteins) showed homology to venom proteins from assassin bugs (Reduviidae), including 21% (28 proteins from seven families) not known from other sources. These data suggest that numerous protein families were recruited into venom and diversified rapidly following the switch from phytophagy to predation by ancestral heteropterans, and then were retained over > 200 my of evolution. In contrast, trophic switches to blood-feeding (e.g. in Triatominae and Cimicidae) or reversions to plant-feeding (e.g., in Pentatomomorpha) were accompanied by rapid changes in the composition of venom/saliva, including the loss of many protein families.

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Acknowledgements

We thank the Australian Insect Farm for acquiring insects, Alun Jones for assistance with proteomics experiments, Idriss Blakey for assistance with FTIR spectroscopy, Christiane Weirauch for discussions of phylogeny, and Eivind Undheim for assistance with animals and sequencing costs. This work was supported by a University of Queensland Postdoctoral Fellowship to A.A.W. and a Principal Research Fellowship to G.F.K. from the Australian National Health and Medical Research Council. Sequences discovered in this project were deposited to GenBank with identifiers of MF683255–MF683386.

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Authors and Affiliations

  1. Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD, 4072, Australia

    Andrew A. Walker & Glenn F. King

  2. Instituto de Biotecnología, Universidad Nacional Autónoma de México, 61500, Cuernavaca, Morelos, Mexico

    Maria José Hernández-Vargas & Gerardo Corzo

  3. Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD, 4072, Australia

    Bryan G. Fry

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  1. Andrew A. Walker
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  2. Maria José Hernández-Vargas
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  3. Gerardo Corzo
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  4. Bryan G. Fry
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Correspondence to Andrew A. Walker or Glenn F. King.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Dataset S1

: Identification and annotation of Lethocerus distinctifemur venom proteins (XLSX 207 kb)

Supplementary Dataset S2

: Most abundant transcripts in each compartment of Lethocerus distinctifemur venom glands (XLSX 90 kb)

Supplementary Fig. S1

: Alignment of amino acid sequences of family 2 venom proteins, redulysins and trialysins (PDF 77 kb)

Supplementary Table S1:

Abundant venom proteins detected by LC–MS/MS (PDF 36 kb)

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Walker, A.A., Hernández-Vargas, M.J., Corzo, G. et al. Giant fish-killing water bug reveals ancient and dynamic venom evolution in Heteroptera. Cell. Mol. Life Sci. 75, 3215–3229 (2018). https://doi.org/10.1007/s00018-018-2768-1

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