Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models
The evolution of an aquatic lifestyle from land dwelling venomous elapids is a radical ecological modification, bringing about many evolutionary changes from morphology to diet. Diet is an important ecological facet which can play a key role in regulating functional traits such as venom composition...
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| Format: | Article |
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MDPI AG
2020-10-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/19/7377 |
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| author | Richard J. Harris Nicholas J. Youngman Christina N. Zdenek Tam M. Huynh Amanda Nouwens Wayne C. Hodgson David Harrich Nathan Dunstan José A. Portes-Junior Bryan G. Fry |
| author_facet | Richard J. Harris Nicholas J. Youngman Christina N. Zdenek Tam M. Huynh Amanda Nouwens Wayne C. Hodgson David Harrich Nathan Dunstan José A. Portes-Junior Bryan G. Fry |
| author_sort | Richard J. Harris |
| collection | DOAJ |
| description | The evolution of an aquatic lifestyle from land dwelling venomous elapids is a radical ecological modification, bringing about many evolutionary changes from morphology to diet. Diet is an important ecological facet which can play a key role in regulating functional traits such as venom composition and prey-specific targeting of venom. In addition to predating upon novel prey (e.g., fish, fish eggs and invertebrates), the venoms of aquatic elapids also face the challenge of increased prey-escape potential in the aquatic environment. Thus, despite the independent radiation into an aquatic niche on four separate occasions, the venoms of aquatic elapids are evolving under convergent selection pressures. Utilising a biolayer interferometry binding assay, this study set out to elucidate whether crude venoms from representative aquatic elapids were target-specific to the orthosteric site of postsynaptic nicotinic acetylcholine receptor mimotopes of fish compared to other terrestrial prey types. Representatives of the four aquatic lineages were: aquatic coral snakes representative was <i>Micrurus surinamensis</i>;, sea kraits representative was <i>Laticauda colubrina;</i> sea snakes representatives were two <i>Aipysurus</i> spp. and eight <i>Hydrophis</i> spp; and water cobras representative was <i>Naja annulata</i>. No prey-specific differences in crude venom binding were observed from any species tested, except for <i>Aipysurus laevis,</i> which showed slight evidence of prey-potency differences. For <i>Hydrophis caerulescens</i>, <i>H. peronii</i>, <i>H. schistosus</i> and <i>M. surinamensis</i>, there was a lack of binding to the orthosteric site of any target lineage. Subsequent testing on the in vitro chick-biventer cervicis muscle preparation suggested that, while the venoms of these species bound postsynaptically, they bound to allosteric sites rather than orthosteric. Allosteric binding is potentially a weaker but faster-acting form of neurotoxicity and we hypothesise that the switch to allosteric binding is likely due to selection pressures related to prey-escape potential. This research has potentially opened up the possibility of a new functional class of toxins which have never been assessed previously while shedding light on the selection pressures shaping venom evolution. |
| first_indexed | 2024-03-10T15:48:24Z |
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| id | doaj.art-0dd5ec779e8149e9ab1cf4749e2dd32a |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T15:48:24Z |
| publishDate | 2020-10-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-0dd5ec779e8149e9ab1cf4749e2dd32a2023-11-20T16:12:38ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-10-012119737710.3390/ijms21197377Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey ModelsRichard J. Harris0Nicholas J. Youngman1Christina N. Zdenek2Tam M. Huynh3Amanda Nouwens4Wayne C. Hodgson5David Harrich6Nathan Dunstan7José A. Portes-Junior8Bryan G. Fry9Toxin Evolution Lab, University of Queensland, Biological Sciences, St. Lucia, QLD 4072, AustraliaToxin Evolution Lab, University of Queensland, Biological Sciences, St. Lucia, QLD 4072, AustraliaToxin Evolution Lab, University of Queensland, Biological Sciences, St. Lucia, QLD 4072, AustraliaDepartment of Pharmacology, Biomedicine Discovery Institute, Monash University, Clayton, VIC 3800, AustraliaSchool of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, QLD 4072, AustraliaDepartment of Pharmacology, Biomedicine Discovery Institute, Monash University, Clayton, VIC 3800, AustraliaQIMR Berghofer, Royal Brisbane Hospital, Herston, QLD 4029, AustraliaVenom Supplies, Tanunda, SA 5352, AustraliaLaboratório de Coleções Zoológicas, Instituto Butantan, São Paulo 05503-900, BrazilToxin Evolution Lab, University of Queensland, Biological Sciences, St. Lucia, QLD 4072, AustraliaThe evolution of an aquatic lifestyle from land dwelling venomous elapids is a radical ecological modification, bringing about many evolutionary changes from morphology to diet. Diet is an important ecological facet which can play a key role in regulating functional traits such as venom composition and prey-specific targeting of venom. In addition to predating upon novel prey (e.g., fish, fish eggs and invertebrates), the venoms of aquatic elapids also face the challenge of increased prey-escape potential in the aquatic environment. Thus, despite the independent radiation into an aquatic niche on four separate occasions, the venoms of aquatic elapids are evolving under convergent selection pressures. Utilising a biolayer interferometry binding assay, this study set out to elucidate whether crude venoms from representative aquatic elapids were target-specific to the orthosteric site of postsynaptic nicotinic acetylcholine receptor mimotopes of fish compared to other terrestrial prey types. Representatives of the four aquatic lineages were: aquatic coral snakes representative was <i>Micrurus surinamensis</i>;, sea kraits representative was <i>Laticauda colubrina;</i> sea snakes representatives were two <i>Aipysurus</i> spp. and eight <i>Hydrophis</i> spp; and water cobras representative was <i>Naja annulata</i>. No prey-specific differences in crude venom binding were observed from any species tested, except for <i>Aipysurus laevis,</i> which showed slight evidence of prey-potency differences. For <i>Hydrophis caerulescens</i>, <i>H. peronii</i>, <i>H. schistosus</i> and <i>M. surinamensis</i>, there was a lack of binding to the orthosteric site of any target lineage. Subsequent testing on the in vitro chick-biventer cervicis muscle preparation suggested that, while the venoms of these species bound postsynaptically, they bound to allosteric sites rather than orthosteric. Allosteric binding is potentially a weaker but faster-acting form of neurotoxicity and we hypothesise that the switch to allosteric binding is likely due to selection pressures related to prey-escape potential. This research has potentially opened up the possibility of a new functional class of toxins which have never been assessed previously while shedding light on the selection pressures shaping venom evolution.https://www.mdpi.com/1422-0067/21/19/7377Elapidaevenomneurotoxicitynicotinic acetylcholine receptorsorthostericallosteric |
| spellingShingle | Richard J. Harris Nicholas J. Youngman Christina N. Zdenek Tam M. Huynh Amanda Nouwens Wayne C. Hodgson David Harrich Nathan Dunstan José A. Portes-Junior Bryan G. Fry Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models International Journal of Molecular Sciences Elapidae venom neurotoxicity nicotinic acetylcholine receptors orthosteric allosteric |
| title | Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models |
| title_full | Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models |
| title_fullStr | Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models |
| title_full_unstemmed | Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models |
| title_short | Assessing the Binding of Venoms from Aquatic Elapids to the Nicotinic Acetylcholine Receptor Orthosteric Site of Different Prey Models |
| title_sort | assessing the binding of venoms from aquatic elapids to the nicotinic acetylcholine receptor orthosteric site of different prey models |
| topic | Elapidae venom neurotoxicity nicotinic acetylcholine receptors orthosteric allosteric |
| url | https://www.mdpi.com/1422-0067/21/19/7377 |
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