An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)

Spiders use venom to subdue their prey, but little is known about the diversity of venoms in different spider families. Given the limited data available for orb-weaver spiders (Araneidae), we selected the wasp spider <i>Argiope bruennichi</i> for detailed analysis. Our strategy combined...

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Main Authors: Tim Lüddecke, Björn M. von Reumont, Frank Förster, André Billion, Thomas Timm, Günter Lochnit, Andreas Vilcinskas, Sarah Lemke
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/10/7/978
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author Tim Lüddecke
Björn M. von Reumont
Frank Förster
André Billion
Thomas Timm
Günter Lochnit
Andreas Vilcinskas
Sarah Lemke
author_facet Tim Lüddecke
Björn M. von Reumont
Frank Förster
André Billion
Thomas Timm
Günter Lochnit
Andreas Vilcinskas
Sarah Lemke
author_sort Tim Lüddecke
collection DOAJ
description Spiders use venom to subdue their prey, but little is known about the diversity of venoms in different spider families. Given the limited data available for orb-weaver spiders (Araneidae), we selected the wasp spider <i>Argiope bruennichi</i> for detailed analysis. Our strategy combined a transcriptomics pipeline based on multiple assemblies with a dual proteomics workflow involving parallel mass spectrometry techniques and electrophoretic profiling. We found that the remarkably simple venom of <i>A. bruennichi</i> has an atypical composition compared to other spider venoms, prominently featuring members of the cysteine-rich secretory protein, antigen 5 and pathogenesis-related protein 1 (CAP) superfamily and other, mostly high-molecular-weight proteins. We also detected a subset of potentially novel toxins similar to neuropeptides. We discuss the potential function of these proteins in the context of the unique hunting behavior of wasp spiders, which rely mostly on silk to trap their prey. We propose that the simplicity of the venom evolved to solve an economic dilemma between two competing yet metabolically expensive weapon systems. This study emphasizes the importance of cutting-edge methods to encompass the lineages of smaller venomous species that have yet to be characterized in detail, allowing us to understand the biology of their venom systems and to mine this prolific resource for translational research.
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spelling doaj.art-a8ccbcf384174213a8a7bb4ca69522d62023-11-20T05:27:14ZengMDPI AGBiomolecules2218-273X2020-06-0110797810.3390/biom10070978An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)Tim Lüddecke0Björn M. von Reumont1Frank Förster2André Billion3Thomas Timm4Günter Lochnit5Andreas Vilcinskas6Sarah Lemke7Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Gießen, GermanyLOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, GermanyInstitute for Bioinformatics and Systems Biology, Justus-Liebig-University of Gießen, Heinrich-Buff-Ring 58, 35392 Gießen, GermanyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Gießen, GermanyInstitute of Biochemistry, Justus-Liebig-University of Gießen, Friedrichstr. 24, 35392 Gießen, GermanyInstitute of Biochemistry, Justus-Liebig-University of Gießen, Friedrichstr. 24, 35392 Gießen, GermanyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Gießen, GermanyLOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, GermanySpiders use venom to subdue their prey, but little is known about the diversity of venoms in different spider families. Given the limited data available for orb-weaver spiders (Araneidae), we selected the wasp spider <i>Argiope bruennichi</i> for detailed analysis. Our strategy combined a transcriptomics pipeline based on multiple assemblies with a dual proteomics workflow involving parallel mass spectrometry techniques and electrophoretic profiling. We found that the remarkably simple venom of <i>A. bruennichi</i> has an atypical composition compared to other spider venoms, prominently featuring members of the cysteine-rich secretory protein, antigen 5 and pathogenesis-related protein 1 (CAP) superfamily and other, mostly high-molecular-weight proteins. We also detected a subset of potentially novel toxins similar to neuropeptides. We discuss the potential function of these proteins in the context of the unique hunting behavior of wasp spiders, which rely mostly on silk to trap their prey. We propose that the simplicity of the venom evolved to solve an economic dilemma between two competing yet metabolically expensive weapon systems. This study emphasizes the importance of cutting-edge methods to encompass the lineages of smaller venomous species that have yet to be characterized in detail, allowing us to understand the biology of their venom systems and to mine this prolific resource for translational research.https://www.mdpi.com/2218-273X/10/7/978venomics<i>Argiope bruennichi</i>CAP superfamilyICKneuropeptideshunting behavior
spellingShingle Tim Lüddecke
Björn M. von Reumont
Frank Förster
André Billion
Thomas Timm
Günter Lochnit
Andreas Vilcinskas
Sarah Lemke
An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
Biomolecules
venomics
<i>Argiope bruennichi</i>
CAP superfamily
ICK
neuropeptides
hunting behavior
title An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
title_full An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
title_fullStr An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
title_full_unstemmed An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
title_short An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (<i>Argiope bruennichi</i>)
title_sort economic dilemma between molecular weapon systems may explain an arachno atypical venom in wasp spiders i argiope bruennichi i
topic venomics
<i>Argiope bruennichi</i>
CAP superfamily
ICK
neuropeptides
hunting behavior
url https://www.mdpi.com/2218-273X/10/7/978
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