Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins

Autores
Dreon, Marcos Sebastian; Frassa, Maria Victoria; Ceolin, Marcelo Raul; Ituarte, Santiago; Qiu, Jian Wen; Sun, Jin; Fernández, Patricia Elena; Heras, Horacio
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Although most eggs are intensely predated, the aerial egg clutches from the aquatic snail Pomacea canaliculata have only one reported predator due to unparalleled biochemical defenses. These include two storage-proteins: ovorubin that provides a conspicuous (presumably warning) coloration and has antinutritive and antidigestive properties, and PcPV2 a neurotoxin with lethal effect on rodents. We sequenced PcPV2 and studied whether it was able to withstand the gastrointestinal environment and reach circulation of a potential predator. Capacity to resist digestion was assayed using small-angle X-ray scattering (SAXS), fluorescence spectroscopy and simulated gastrointestinal proteolysis. PcPV2 oligomer is antinutritive, withstanding proteinase digestion and displaying structural stability between pH 4.0-10.0. cDNA sequencing and protein domain search showed that its two subunits share homology with membrane attack complex/perforin (MACPF)-like toxins and tachylectin-like lectins, a previously unknown structure that resembles plant Type-2 ribosome-inactivating proteins and bacterial botulinum toxins. The protomer has therefore a novel AB toxin combination of a MACPF-like chain linked by disulfide bonds to a lectin-like chain, indicating a delivery system for the former. This was further supported by observing PcPV2 binding to glycocalix of enterocytes in vivo and in culture, and by its hemaggutinating, but not hemolytic activity, which suggested an interaction with surface oligosaccharides. PcPV2 is able to get into predator's body as evidenced in rats and mice by the presence of circulating antibodies in response to sublethal oral doses. To our knowledge, a lectin-pore-forming toxin has not been reported before, providing the first evidence of a neurotoxic lectin in animals, and a novel function for ancient and widely distributed proteins. The acquisition of this unique neurotoxic/antinutritive/storage protein may confer the eggs a survival advantage, opening new perspectives in the study of the evolution of animal defensive strategies.
Fil: Dreon, Marcos Sebastian. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina
Fil: Frassa, Maria Victoria. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; Argentina
Fil: Ceolin, Marcelo Raul. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; Argentina
Fil: Ituarte, Santiago. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina
Fil: Qiu, Jian Wen. Hong Kong Baptist University. Department of Biology; China
Fil: Sun, Jin. Hong Kong Baptist University. Department of Biology; China
Fil: Fernández, Patricia Elena. Universidad Nacional de la Plata. Facultad de Ciencias Veterinarias. Cátedra de Patología General Veterinaria; Argentina
Fil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Naturales y Museo; Argentina
Materia
Egg Protein
Macpf
Lectin
Perforin
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/2962
Acceder
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spelling Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack ToxinsDreon, Marcos SebastianFrassa, Maria VictoriaCeolin, Marcelo RaulItuarte, SantiagoQiu, Jian WenSun, JinFernández, Patricia ElenaHeras, HoracioEgg ProteinMacpfLectinPerforinhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1https://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Although most eggs are intensely predated, the aerial egg clutches from the aquatic snail Pomacea canaliculata have only one reported predator due to unparalleled biochemical defenses. These include two storage-proteins: ovorubin that provides a conspicuous (presumably warning) coloration and has antinutritive and antidigestive properties, and PcPV2 a neurotoxin with lethal effect on rodents. We sequenced PcPV2 and studied whether it was able to withstand the gastrointestinal environment and reach circulation of a potential predator. Capacity to resist digestion was assayed using small-angle X-ray scattering (SAXS), fluorescence spectroscopy and simulated gastrointestinal proteolysis. PcPV2 oligomer is antinutritive, withstanding proteinase digestion and displaying structural stability between pH 4.0-10.0. cDNA sequencing and protein domain search showed that its two subunits share homology with membrane attack complex/perforin (MACPF)-like toxins and tachylectin-like lectins, a previously unknown structure that resembles plant Type-2 ribosome-inactivating proteins and bacterial botulinum toxins. The protomer has therefore a novel AB toxin combination of a MACPF-like chain linked by disulfide bonds to a lectin-like chain, indicating a delivery system for the former. This was further supported by observing PcPV2 binding to glycocalix of enterocytes in vivo and in culture, and by its hemaggutinating, but not hemolytic activity, which suggested an interaction with surface oligosaccharides. PcPV2 is able to get into predator's body as evidenced in rats and mice by the presence of circulating antibodies in response to sublethal oral doses. To our knowledge, a lectin-pore-forming toxin has not been reported before, providing the first evidence of a neurotoxic lectin in animals, and a novel function for ancient and widely distributed proteins. The acquisition of this unique neurotoxic/antinutritive/storage protein may confer the eggs a survival advantage, opening new perspectives in the study of the evolution of animal defensive strategies.Fil: Dreon, Marcos Sebastian. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; ArgentinaFil: Frassa, Maria Victoria. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; ArgentinaFil: Ceolin, Marcelo Raul. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; ArgentinaFil: Ituarte, Santiago. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; ArgentinaFil: Qiu, Jian Wen. Hong Kong Baptist University. Department of Biology; ChinaFil: Sun, Jin. Hong Kong Baptist University. Department of Biology; ChinaFil: Fernández, Patricia Elena. Universidad Nacional de la Plata. Facultad de Ciencias Veterinarias. Cátedra de Patología General Veterinaria; ArgentinaFil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Naturales y Museo; ArgentinaPublic Library of Science2013-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/2962Dreon, Marcos Sebastian; Frassa, Maria Victoria; Ceolin, Marcelo Raul; Ituarte, Santiago; Qiu, Jian Wen; et al.; Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins; Public Library of Science; Plos One; 8; 5; 5-2013; e637821932-6203enginfo:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0063782info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0063782info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:27:05Zoai:ri.conicet.gov.ar:11336/2962instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 14:27:05.998CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
title Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
spellingShingle Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
Dreon, Marcos Sebastian
Egg Protein
Macpf
Lectin
Perforin
title_short Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
title_full Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
title_fullStr Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
title_full_unstemmed Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
title_sort Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins
dc.creator.none.fl_str_mv Dreon, Marcos Sebastian
Frassa, Maria Victoria
Ceolin, Marcelo Raul
Ituarte, Santiago
Qiu, Jian Wen
Sun, Jin
Fernández, Patricia Elena
Heras, Horacio
author Dreon, Marcos Sebastian
author_facet Dreon, Marcos Sebastian
Frassa, Maria Victoria
Ceolin, Marcelo Raul
Ituarte, Santiago
Qiu, Jian Wen
Sun, Jin
Fernández, Patricia Elena
Heras, Horacio
author_role author
author2 Frassa, Maria Victoria
Ceolin, Marcelo Raul
Ituarte, Santiago
Qiu, Jian Wen
Sun, Jin
Fernández, Patricia Elena
Heras, Horacio
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Egg Protein
Macpf
Lectin
Perforin
topic Egg Protein
Macpf
Lectin
Perforin
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Although most eggs are intensely predated, the aerial egg clutches from the aquatic snail Pomacea canaliculata have only one reported predator due to unparalleled biochemical defenses. These include two storage-proteins: ovorubin that provides a conspicuous (presumably warning) coloration and has antinutritive and antidigestive properties, and PcPV2 a neurotoxin with lethal effect on rodents. We sequenced PcPV2 and studied whether it was able to withstand the gastrointestinal environment and reach circulation of a potential predator. Capacity to resist digestion was assayed using small-angle X-ray scattering (SAXS), fluorescence spectroscopy and simulated gastrointestinal proteolysis. PcPV2 oligomer is antinutritive, withstanding proteinase digestion and displaying structural stability between pH 4.0-10.0. cDNA sequencing and protein domain search showed that its two subunits share homology with membrane attack complex/perforin (MACPF)-like toxins and tachylectin-like lectins, a previously unknown structure that resembles plant Type-2 ribosome-inactivating proteins and bacterial botulinum toxins. The protomer has therefore a novel AB toxin combination of a MACPF-like chain linked by disulfide bonds to a lectin-like chain, indicating a delivery system for the former. This was further supported by observing PcPV2 binding to glycocalix of enterocytes in vivo and in culture, and by its hemaggutinating, but not hemolytic activity, which suggested an interaction with surface oligosaccharides. PcPV2 is able to get into predator's body as evidenced in rats and mice by the presence of circulating antibodies in response to sublethal oral doses. To our knowledge, a lectin-pore-forming toxin has not been reported before, providing the first evidence of a neurotoxic lectin in animals, and a novel function for ancient and widely distributed proteins. The acquisition of this unique neurotoxic/antinutritive/storage protein may confer the eggs a survival advantage, opening new perspectives in the study of the evolution of animal defensive strategies.
Fil: Dreon, Marcos Sebastian. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina
Fil: Frassa, Maria Victoria. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; Argentina
Fil: Ceolin, Marcelo Raul. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico la Plata. Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas; Argentina
Fil: Ituarte, Santiago. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina
Fil: Qiu, Jian Wen. Hong Kong Baptist University. Department of Biology; China
Fil: Sun, Jin. Hong Kong Baptist University. Department of Biology; China
Fil: Fernández, Patricia Elena. Universidad Nacional de la Plata. Facultad de Ciencias Veterinarias. Cátedra de Patología General Veterinaria; Argentina
Fil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Bioquímicas de La Plata; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Naturales y Museo; Argentina
description Although most eggs are intensely predated, the aerial egg clutches from the aquatic snail Pomacea canaliculata have only one reported predator due to unparalleled biochemical defenses. These include two storage-proteins: ovorubin that provides a conspicuous (presumably warning) coloration and has antinutritive and antidigestive properties, and PcPV2 a neurotoxin with lethal effect on rodents. We sequenced PcPV2 and studied whether it was able to withstand the gastrointestinal environment and reach circulation of a potential predator. Capacity to resist digestion was assayed using small-angle X-ray scattering (SAXS), fluorescence spectroscopy and simulated gastrointestinal proteolysis. PcPV2 oligomer is antinutritive, withstanding proteinase digestion and displaying structural stability between pH 4.0-10.0. cDNA sequencing and protein domain search showed that its two subunits share homology with membrane attack complex/perforin (MACPF)-like toxins and tachylectin-like lectins, a previously unknown structure that resembles plant Type-2 ribosome-inactivating proteins and bacterial botulinum toxins. The protomer has therefore a novel AB toxin combination of a MACPF-like chain linked by disulfide bonds to a lectin-like chain, indicating a delivery system for the former. This was further supported by observing PcPV2 binding to glycocalix of enterocytes in vivo and in culture, and by its hemaggutinating, but not hemolytic activity, which suggested an interaction with surface oligosaccharides. PcPV2 is able to get into predator's body as evidenced in rats and mice by the presence of circulating antibodies in response to sublethal oral doses. To our knowledge, a lectin-pore-forming toxin has not been reported before, providing the first evidence of a neurotoxic lectin in animals, and a novel function for ancient and widely distributed proteins. The acquisition of this unique neurotoxic/antinutritive/storage protein may confer the eggs a survival advantage, opening new perspectives in the study of the evolution of animal defensive strategies.
publishDate 2013
dc.date.none.fl_str_mv 2013-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/2962
Dreon, Marcos Sebastian; Frassa, Maria Victoria; Ceolin, Marcelo Raul; Ituarte, Santiago; Qiu, Jian Wen; et al.; Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins; Public Library of Science; Plos One; 8; 5; 5-2013; e63782
1932-6203
url http://hdl.handle.net/11336/2962
identifier_str_mv Dreon, Marcos Sebastian; Frassa, Maria Victoria; Ceolin, Marcelo Raul; Ituarte, Santiago; Qiu, Jian Wen; et al.; Novel Animal Defenses against Predation: A Snail Egg Neurotoxin Combining Lectin and Pore-Forming Chains That Resembles Plant Defense and Bacteria Attack Toxins; Public Library of Science; Plos One; 8; 5; 5-2013; e63782
1932-6203
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0063782
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0063782
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.22299

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