A highly stable, nondigestible lectin from Pomacea diffusa unveils clade-related protection systems in apple snail eggs

Author:

Brola T. R.1ORCID,Dreon M. S.12ORCID,Qiu J. W.3ORCID,Heras H.14ORCID

Affiliation:

1. Instituto de Investigaciones Bioquímicas de La Plata Prof. R.R. Brenner (INIBIOLP), Universidad Nacional de La Plata (UNLP) – CONICET, La Plata, Argentina

2. Cátedra de Bioquímica y Biología Molecular, Facultad de Ciencias Médicas, UNLP, La Plata, Argentina

3. Department of Biology, Hong Kong Baptist University, Hong Kong, P.R. China

4. Cátedra de Química Biológica, Facultad de Ciencias Naturales y Museo, UNLP, La Plata, Argentina

Abstract

The acquisition of egg protection is vital for species survival. Poisonous eggs from Pomacea apple snails have defensive macromolecules for protection. Here we isolated and characterized a novel lectin called PdPV1 that is massively accumulated in the eggs of Pomacea diffusa and seems part of its protective cocktail. The native protein, an oligomer of ca. 256 kDa, has high structural stability, withstanding 15 min boiling and denaturing by sodium dodecyl sulphate. It resists in vitro proteinase digestion and displays structural stability between pH 2.0–12.0 and up to 85 °C. These properties, as well as its subunit sequences, glycosylation pattern, presence of carotenoids, size, and global shape resemble those of its orthologs from other Pomacea. Further, like members of the canaliculata clade, PdPV1 is recovered unchanged in faeces of mice ingesting it, supporting an antinutritive defensive function. PdPV1 also displays a strong hemagglutinating activity specifically recognizing selected ganglioside motifs with high affinity. This activity is only shared with PsSC, a perivitelline from the same clade (bridgesii clade). As a whole, these results indicate that species in the genus Pomacea have diversified their eggs defences: Those from the bridgesii clade are protected mostly by non-digestible lectins that lower the nutritional value of eggs, in contrast with protection by neurotoxins of other Pomacea clades, indicating apple snail egg defensive strategies are clade-specific. The harsh gastrointestinal environment of predators would have favoured their appearance, extending by convergent evolution the presence of plant-like highly stable lectins, a strategy not reported in other animals.

Funder

Agencia Nacional de Promoción Científica y Tecnológica

Comisión de Investigaciones Científicas

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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