Pomacea canaliculata Ampullar Proteome: A Nematode-Based Bio-Pesticide Induces Changes in Metabolic and Stress-Related Pathways

Simple Summary Pomacea canaliculata is a South American invasive freshwater snail, affecting biodiversity, crop production and public health, now retrieved in Asian, North American and European countries. The identification of molecules connected to P. canaliculata adaptability may prove helpful in developing strategies that could overcome the snail’s resilience and stop its spread in non-original countries. This research presents the changes occurring in the proteome of a small organ, i.e., the ampulla, after challenging the snails with a nematode-based bio-pesticide. Transmission electron microscopy (TEM) analysis demonstrated that this organ has a complex connective ultrastructure and contains rhogocytes. TEM also confirmed the ampulla as a deposit of nitrogen-based material. After exposure to the nematode-based bio-pesticide, significant changes were observed for enzymes mainly involved in antioxidant defence, energy metabolism and cytoskeletal dynamics. These changes recall the systemic oxidative stress response that the snails undergo during the arousal after aestivation/hibernation, a physiological response involving other organs that, similarly to the ampulla, store nitrogen-based compounds. As fundamental players of the response against bio-pesticides and environmental cues, the enzymes identified in this research and involved in stress-related pathways may represent a suitable target for the efficacious and sustainable control of P. canaliculata spread. Abstract Pomacea canaliculata is a freshwater gastropod known for being both a highly invasive species and one of the possible intermediate hosts of the mammalian parasite Angiostrongylus cantonensis. With the aim of providing new information concerning P. canaliculata biology and adaptability, the first proteome of the ampulla, i.e., a small organ associated with the circulatory system and known as a reservoir of nitrogen-containing compounds, was obtained. The ampullar proteome was derived from ampullae of control snails or after exposure to a nematode-based molluscicide, known for killing snails in a dose- and temperature-dependent fashion. Proteome analysis revealed that the composition of connective ampulla walls, cell metabolism and oxidative stress response were affected by the bio-pesticide. Ultrastructural investigations have highlighted the presence of rhogocytes within the ampullar walls, as it has been reported for other organs containing nitrogen storage tissue. Collected data suggested that the ampulla may belong to a network of organs involved in controlling and facing oxidative stress in different situations. The response against the nematode-based molluscicide recalled the response set up during early arousal after aestivation and hibernation, thus encouraging the hypothesis that metabolic pathways and antioxidant defences promoting amphibiousness could also prove useful in facing other challenges stimulating an oxidative stress response, e.g., immune challenges or biocide exposure. Targeting the oxidative stress resistance of P. canaliculata may prove helpful for increasing its susceptibility to bio-pesticides and may help the sustainable control of this pest’s diffusion.