The eggs of the apple snailPomacea maculataare defended by indigestible polysaccharides and toxic proteins

Abstract

The freshwater snails Pomacea Perry, 1810 lay conspicuous aerial egg clutches that are ignored by most predators. Egg biochemical defenses in the apple snail Pomacea canaliculata (Lamarck, 1822) are provided by multifunctional proteins. We analyzed the eggs of a sympatric species, Pomacea maculata Perry, 1810, studying the gross composition, toxicity, hemagglutinating activity, and its antinutritive and antidigestive properties. Eggs are mostly composed of polysaccharides (mainly galactogen) and proteins, followed by lipids and nonsoluble calcium. Two perivitellins account for ∼85% dry mass of the egg protein. The major lipids are phospholipids and sterols. A suite of potential defenses was determined, including strong lethal neurotoxicity on mice and moderate antidigestive and lectin activities. Remarkably, their polysaccharides were refractive to in vitro digestion by digestive glycosidases. This study characterized ∼99% of egg composition and identified multiple potential defenses, provided not only by proteins but also by polysaccharides. This is the first evidence to our knowledge that reserve sugars may be involved in defenses, giving further insight into the unusual reproductive strategy of these well-defended snail eggs.

Egg perivitelline fluid proteome of a freshwater snail: Insight into the transition from aquatic to terrestrial egg deposition

“…Nevertheless, P. diffusa and M. cornuarietis invest more on immune proteins and protease inhibitors. The three Pomacea species have a unique CaBP required for the formation of the calcareous shell of terrestrial eggs, and a Kunitz/Bovine pancreatic trypsin inhibitor that, at least in P. canaliculata and P. maculate , inhibit multiple digestive proteases of mice . In addition, duplication and positive selection of the CaBP and PV2 subunits were likely responsible for the aerial egg deposition and the evolution of the PV2 toxic protein as an anti‐predation mechanism in P. canaliculata and P. maculata .…”

“…PV2, which constitutes around 7.5% of total PVF protein ? is a protein complex composed of two subunits: a membrane attack complex/perforin (MACPF) protein as the toxic subunit, and a tachylectin‐like protein as the delivery subunit, which are linked with a disulfide bridge . Laboratory experiments have shown that PV2 is neurotoxic to mice in P. canaliculata and probably is also a neurotoxin in P. maculata . However, the neurotoxicity was not observed in the PVF of P. scalaris , suggesting that PV2‐active toxins may not be present in all species of Pomacea.…”

“…Laboratory experiments have shown that PV2 is neurotoxic to mice in P. canaliculata and probably is also a neurotoxin in P. maculata . However, the neurotoxicity was not observed in the PVF of P. scalaris , suggesting that PV2‐active toxins may not be present in all species of Pomacea. Since there are multiple copies of MACPF and tachylectin genes in Pomacea , to avoid confusion we named the PV2 toxin associated subunits as PV2‐MACPF and PV2‐tachylectin, and other paralogs as MACPF‐like and tachylectin‐like proteins, respectively.…”

“…5,6 These perivitellins serve as stores of nutrients that fuel the embryonic development and are involved in embryo protection in some Pomacea. 6,7 Although previous proteomic studies named the major perivitellin protein PV1 as PcOvo for P. canaliculata, 8 PmPV1 for P. maculata 9 and PsSC for P. scalaris, 10 to avoid confusion of the major protein in PVF, we used "PV1" throughout this study. Among two major perivitelline groups, PV1 is an oligomer composed of several subunits and plays several critical roles: photoprotection, antioxidant, and nutrient provision in P. canaliculata and P. maculate, 4,8,11,12 and immune response in P. scalaris.…”

Resaca supports range expansion of invasive apple snails (Pomacea maculata Perry, 1810; Caenogastropoda: Ampullariidae) to the Rio Grande Valley, Texas

“…Small hatchlings would be more vulnerable to predation by crayfish (Dorn & Hafsadi 2016), but the overall number of offspring potentially produced probably provides sufficient numbers to survive enhanced predation. Furthermore, the highly visible and seemingly vulnerable egg clutches are chemically defended and unpalatable to predators (Giglio et al 2016). Coupled with the climate and habitat in South Texas, all these factors (e.g., ability to overwinter, hundreds of propagules and egg defense) indicate the likely persistence and spread of this species.…”