Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior

Autores
Cadierno, María Pilar; Dreon, Marcos Sebastian; Heras, Horacio
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In contrast with vitellogenin maturation, it is unknown whether gastropod perivitellin precursors are subject to large structural changes. The gastropod reproductive tract includes an accessory organ, the albumen gland (AG), that produces and secretes perivitelline fluid. In the apple snail Pomacea canaliculata, the large, reddish-pink AG provides eggs with perivitellins that are defensive against predators. Although the AG makes a considerable contribution to apple snail biomass, field observations indicate that it is rejected by avian and mammalian predators, although the underlying reason remains unknown. By analyzing the structure-function properties of P. canaliculata perivitellin precursors, we provide insight into perivitellin maturation and its relationship with apple snail predator feeding behavior. Structural analysis using small-angle X-ray scattering, absorption and fluorescence spectroscopy, circular dichroism, electrophoresis, chromatography, and partial proteolysis showed that the size, shape, and structure of perivitellin precursors resemble those of egg mature forms. Functional analysis indicates that the precursors of the defensive perivitellins ovorubin (PcOvo) and perivitellin-2 (PcPV2) are highly stable and antinutritive, withstanding proteinase digestion and displaying structural stability of their quaternary structure under a wide pH range (4.0–10.0). Furthermore, AG extracts limit a predator’s ability to digest nutrients and are toxic to mice (median lethal concentration 96 h after administration: 5.9 mg/kg). Treated mice displayed neurologic signs similar to those produced by egg PcPV2. Results indicate that apple snails store active precursors of egg proteins inside the AG, providing evidence that gastropod perivitellin precursors do not experience the large structural processing of invertebrate vitellogenin maturation. These defensive proteins provide the apple snail AG with neurotoxic, antinutritive, and antidigestive activity, a likely explanation for the predators’ feeding behavior.
Fil: Cadierno, María Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina
Fil: Dreon, Marcos Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; Argentina
Fil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo; Argentina
Materia
PERIVITELLIN PRECURSOR
STRUCTURE-FUNCTION
DEFENSIVE PROTEIN
SNAIL KITE
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/48720
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/48720
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding BehaviorCadierno, María PilarDreon, Marcos SebastianHeras, HoracioPERIVITELLIN PRECURSORSTRUCTURE-FUNCTIONDEFENSIVE PROTEINSNAIL KITEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In contrast with vitellogenin maturation, it is unknown whether gastropod perivitellin precursors are subject to large structural changes. The gastropod reproductive tract includes an accessory organ, the albumen gland (AG), that produces and secretes perivitelline fluid. In the apple snail Pomacea canaliculata, the large, reddish-pink AG provides eggs with perivitellins that are defensive against predators. Although the AG makes a considerable contribution to apple snail biomass, field observations indicate that it is rejected by avian and mammalian predators, although the underlying reason remains unknown. By analyzing the structure-function properties of P. canaliculata perivitellin precursors, we provide insight into perivitellin maturation and its relationship with apple snail predator feeding behavior. Structural analysis using small-angle X-ray scattering, absorption and fluorescence spectroscopy, circular dichroism, electrophoresis, chromatography, and partial proteolysis showed that the size, shape, and structure of perivitellin precursors resemble those of egg mature forms. Functional analysis indicates that the precursors of the defensive perivitellins ovorubin (PcOvo) and perivitellin-2 (PcPV2) are highly stable and antinutritive, withstanding proteinase digestion and displaying structural stability of their quaternary structure under a wide pH range (4.0–10.0). Furthermore, AG extracts limit a predator’s ability to digest nutrients and are toxic to mice (median lethal concentration 96 h after administration: 5.9 mg/kg). Treated mice displayed neurologic signs similar to those produced by egg PcPV2. Results indicate that apple snails store active precursors of egg proteins inside the AG, providing evidence that gastropod perivitellin precursors do not experience the large structural processing of invertebrate vitellogenin maturation. These defensive proteins provide the apple snail AG with neurotoxic, antinutritive, and antidigestive activity, a likely explanation for the predators’ feeding behavior.Fil: Cadierno, María Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; ArgentinaFil: Dreon, Marcos Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; ArgentinaFil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo; ArgentinaUniversity of Chicago Press2017-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/48720Cadierno, María Pilar; Dreon, Marcos Sebastian; Heras, Horacio; Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior; University of Chicago Press; Physiological and Biochemical Zoology; 90; 4; 12-2017; 461-4701522-2152CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1086/691526info:eu-repo/semantics/altIdentifier/url/https://www.journals.uchicago.edu/doi/10.1086/691526info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:47:18Zoai:ri.conicet.gov.ar:11336/48720instacron: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:34982025-09-29 09:47:18.543CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
title Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
spellingShingle Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
Cadierno, María Pilar
PERIVITELLIN PRECURSOR
STRUCTURE-FUNCTION
DEFENSIVE PROTEIN
SNAIL KITE
title_short Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
title_full Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
title_fullStr Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
title_full_unstemmed Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
title_sort Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior
dc.creator.none.fl_str_mv Cadierno, María Pilar
Dreon, Marcos Sebastian
Heras, Horacio
author Cadierno, María Pilar
author_facet Cadierno, María Pilar
Dreon, Marcos Sebastian
Heras, Horacio
author_role author
author2 Dreon, Marcos Sebastian
Heras, Horacio
author2_role author
author
dc.subject.none.fl_str_mv PERIVITELLIN PRECURSOR
STRUCTURE-FUNCTION
DEFENSIVE PROTEIN
SNAIL KITE
topic PERIVITELLIN PRECURSOR
STRUCTURE-FUNCTION
DEFENSIVE PROTEIN
SNAIL KITE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In contrast with vitellogenin maturation, it is unknown whether gastropod perivitellin precursors are subject to large structural changes. The gastropod reproductive tract includes an accessory organ, the albumen gland (AG), that produces and secretes perivitelline fluid. In the apple snail Pomacea canaliculata, the large, reddish-pink AG provides eggs with perivitellins that are defensive against predators. Although the AG makes a considerable contribution to apple snail biomass, field observations indicate that it is rejected by avian and mammalian predators, although the underlying reason remains unknown. By analyzing the structure-function properties of P. canaliculata perivitellin precursors, we provide insight into perivitellin maturation and its relationship with apple snail predator feeding behavior. Structural analysis using small-angle X-ray scattering, absorption and fluorescence spectroscopy, circular dichroism, electrophoresis, chromatography, and partial proteolysis showed that the size, shape, and structure of perivitellin precursors resemble those of egg mature forms. Functional analysis indicates that the precursors of the defensive perivitellins ovorubin (PcOvo) and perivitellin-2 (PcPV2) are highly stable and antinutritive, withstanding proteinase digestion and displaying structural stability of their quaternary structure under a wide pH range (4.0–10.0). Furthermore, AG extracts limit a predator’s ability to digest nutrients and are toxic to mice (median lethal concentration 96 h after administration: 5.9 mg/kg). Treated mice displayed neurologic signs similar to those produced by egg PcPV2. Results indicate that apple snails store active precursors of egg proteins inside the AG, providing evidence that gastropod perivitellin precursors do not experience the large structural processing of invertebrate vitellogenin maturation. These defensive proteins provide the apple snail AG with neurotoxic, antinutritive, and antidigestive activity, a likely explanation for the predators’ feeding behavior.
Fil: Cadierno, María Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina
Fil: Dreon, Marcos Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de la Plata. Facultad de Ciencias Médicas; Argentina
Fil: Heras, Horacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Bioquímicas de La Plata "Prof. Dr. Rodolfo R. Brenner". Universidad Nacional de la Plata. Facultad de Ciencias Médicas. Instituto de Investigaciones Bioquímicas de La Plata ; Argentina. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo; Argentina
description In contrast with vitellogenin maturation, it is unknown whether gastropod perivitellin precursors are subject to large structural changes. The gastropod reproductive tract includes an accessory organ, the albumen gland (AG), that produces and secretes perivitelline fluid. In the apple snail Pomacea canaliculata, the large, reddish-pink AG provides eggs with perivitellins that are defensive against predators. Although the AG makes a considerable contribution to apple snail biomass, field observations indicate that it is rejected by avian and mammalian predators, although the underlying reason remains unknown. By analyzing the structure-function properties of P. canaliculata perivitellin precursors, we provide insight into perivitellin maturation and its relationship with apple snail predator feeding behavior. Structural analysis using small-angle X-ray scattering, absorption and fluorescence spectroscopy, circular dichroism, electrophoresis, chromatography, and partial proteolysis showed that the size, shape, and structure of perivitellin precursors resemble those of egg mature forms. Functional analysis indicates that the precursors of the defensive perivitellins ovorubin (PcOvo) and perivitellin-2 (PcPV2) are highly stable and antinutritive, withstanding proteinase digestion and displaying structural stability of their quaternary structure under a wide pH range (4.0–10.0). Furthermore, AG extracts limit a predator’s ability to digest nutrients and are toxic to mice (median lethal concentration 96 h after administration: 5.9 mg/kg). Treated mice displayed neurologic signs similar to those produced by egg PcPV2. Results indicate that apple snails store active precursors of egg proteins inside the AG, providing evidence that gastropod perivitellin precursors do not experience the large structural processing of invertebrate vitellogenin maturation. These defensive proteins provide the apple snail AG with neurotoxic, antinutritive, and antidigestive activity, a likely explanation for the predators’ feeding behavior.
publishDate 2017
dc.date.none.fl_str_mv 2017-12
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/11336/48720
Cadierno, María Pilar; Dreon, Marcos Sebastian; Heras, Horacio; Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior; University of Chicago Press; Physiological and Biochemical Zoology; 90; 4; 12-2017; 461-470
1522-2152
CONICET Digital
CONICET
url http://hdl.handle.net/11336/48720
identifier_str_mv Cadierno, María Pilar; Dreon, Marcos Sebastian; Heras, Horacio; Apple Snail Perivitellin Precursor Properties Help Explain Predators’ Feeding Behavior; University of Chicago Press; Physiological and Biochemical Zoology; 90; 4; 12-2017; 461-470
1522-2152
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
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info:eu-repo/semantics/altIdentifier/url/https://www.journals.uchicago.edu/doi/10.1086/691526
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eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
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dc.publisher.none.fl_str_mv University of Chicago Press
publisher.none.fl_str_mv University of Chicago Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
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reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
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