Biology subjects

Dreon, M. S.

Publications and source records attributed to Dreon, M. S..

4 recordsLinked to original sources

bioRxiv2023

Stability and functional evolution of a novel family of hyperstable apple snail egg proteins

The relationship between protein stability and function evolution has not been explored in proteins from natural sources. Here, we investigate the phylogenetic differences of Perivitellin-1 (PV1) a novel family of hyperstable egg carotenoproteins crucial to the reproductive success of Pomacea snails, as they have evolved clade-specific protective functions. We studied P. patula PV1 (PpaPV1) from Flagellata clade eggs, the most basal of Pomacea and compared it with PV1s orthologs from derived clades. PpaPV1 stands as the most stable, with longer unfolding half-life, resistance to detergent unfolding, and therefore higher kinetic stability than PV1s from derived clades. In fact, PpaPV1 is among the most hyperstable proteins described in nature. In addition, its spectral characteristics providing a pale egg coloration, mild lectin activity and glycan specificity are narrower than derived clades. Our results provide evidence indicating large structural and functional changes along the evolution of the genus. Notably, the lectin binding of PpaPV1 is less pronounced, and its glycan specificity is narrower compared to PV1s in the sister Bridgesii clade. Our findings underscore the phylogenetic disparities in terms of structural and kinetic stability, as well as defensive traits like a potent lectin activity affecting the gut morphology of potential predators within the Bridgesii clade or a conspicuous, likely warning coloration, within the Canaliculata clade. This work provides a comprehensive comparison of the structural attributes, stability profiles, and functional roles of apple snail egg PV1s from multiple species within a phylogenetic context. Furthermore, it proposes an evolutionary hypothesis suggesting a trade-off between structural stability and the functional aspects of apple snails major egg defense protein.

evolutionary biology↗

bioRxiv2020

Ingestion of poisonous eggs from the invasive apple snail Pomacea canaliculata adversely affects bullfrog Lithobathes catesbeianus intestine morphophysiology

The poisonous eggs of Pomacea canaliculata (Caenogastropoda, Ampullariidae) hardly have any predator. This invasive snail, listed among the 100 worst invasive species, is a serious crop pest and a vector of a human parasitosis. Females lay eggs in pink-reddish masses, presumably as a warning coloration of their chemical defenses. Egg ingestion alters rodents gastrointestinal tract and is lethal if injected, but its effect on other taxa is unknown. Here we explored the toxic effects of Pomacea canaliculata eggs on bullfrog Lithobathes catesbeianus (Anura, Ranidae). Juvenile bullfrogs were gavaged with egg extracts and their digestive tract analyzed after 24 h and 48 h using histological, immunohistochemical and lectin-histochemical techniques. Toxicity was also evaluated by intraperitoneal injection of eggs extracts. Egg extract ingestion adversely affected small intestine of bullfrogs. Short term (24 h) effects included large, reversible changes of the intestinal wall, villi morphology, and changes in the glycosylation patterns of enterocytes. The mucosal area increased and infiltration of inflammatory cells, mainly eosinophils and macrophages, were observed together with a weak hemorrhage. Most of these changes reversed after 48 h. Besides, intraperitoneal injection of egg extract was nontoxic to bullfrog juveniles and no lethality or behavioral changes were observed, a remarkable difference with egg effect on mammals. As a whole, these results indicate that toxins of apple snail eggs reversibly modify gut morphology, which may alter bullfrog physiology limiting their ability to absorb egg nutrients. This study extends the known targets of the apple snail egg defenses against predation to amphibians.

zoology↗

bioRxiv2020

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

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 {degrees}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. Summary statementAnalysis of key snail egg proteins shows evolutionary defensive trends associated with the phylogenetic position, extending by convergent evolution the presence of plant-like defensive strategies not reported in other animals

biochemistry↗

bioRxiv2019

Exaptation of two ancient immune proteins into a new dimeric pore-forming toxin in snails

The Membrane Attack Complex-Perforin (MACPF) family is ubiquitously found in all kingdoms. They have diverse cellular roles but MACPF but pore-forming toxic function are very rare in animals. Here we present the structure of PmPV2, a MACPF toxin from the poisonous apple snail eggs, that can affect the digestive and nervous systems of potential predators. We report the three-dimensional structure of PmPV2, at 15 [A] resolution determined by negative stain electron microscopy (NS-EM) and its solution structure by small angle X-ray scattering (SAXS). We found that PV2s differ from nearly all MACPFs in two respects: it is a dimer in solution and protomers combine two immune proteins into an AB toxin. MACPF chain is linked by a single disulfide bond to a tachylectin chain, and two heterodimers are arranged head-to-tail by non-covalent forces in the native protein. MACPF domain is fused with a putative new Ct-accessory domain exclusive to invertebrates. Tachylectin is a six-bladed {beta}-propeller, similar to animal tectonins. We experimentally validated the predicted functions of both subunits and demonstrated for the first time that PV2s are true pore-forming toxins. The tachylectin ..B.. delivery subunit would bind to target membranes, and then its MACPF ..A.. toxic subunit disrupt lipid bilayers forming large pores altering the plasma membrane conductance. These results indicate that PV2s toxicity evolved by linking two immune proteins where their combined preexisting functions give rise to a new toxic entity with a novel role in defense against predation. This structure is an unparalleled example of protein exaptation.

biochemistry↗