The Immune Response of the Invasive Golden Apple Snail to a Nematode-Based Molluscicide Involves Different Organs

Abstract

The spreading of alien and invasive species poses new challenges for the ecosystem services, the sustainable production of food, and human well-being. Unveiling and targeting the immune system of invasive species can prove helpful for basic and applied research. Here, we present evidence that a nematode (<i>Phasmarhabditis hermaphrodita</i>)-based molluscicide exerts dose-dependent lethal effects on the golden apple snail, <i>Pomacea canaliculata</i>. When used at 1.7 g/L, this biopesticide kills about 30% of snails within one week and promotes a change in the expression of <i>Pc-bpi</i>, an orthologue of mammalian bactericidal/permeability increasing protein (BPI). Changes in <i>Pc-bpi</i> expression, as monitored by quantitative PCR (qPCR), occurred in two immune-related organs, namely the anterior kidney and the gills, after exposure at 18 and 25 °C, respectively. Histological analyses revealed the presence of the nematode in the snail anterior kidney and the gills at both 18 and 25 °C. The mantle and the central nervous system had a stable <i>Pc-bpi</i> expression and seemed not affected by the nematodes. Fluorescence in situ hybridization (FISH) experiments demonstrated the expression of <i>Pc-bpi</i> in circulating hemocytes, nurturing the possibility that increased <i>Pc-bpi</i> expression in the anterior kidney and gills may be due to the hemocytes patrolling the organs. While suggesting that <i>P. hermaphrodita</i>-based biopesticides enable the sustainable control of <i>P. canaliculata</i> spread, our experiments also unveiled an organ-specific and temperature-dependent response in the snails exposed to the nematodes. Overall, our data indicate that, after exposure to a pathogen, the snail <i>P. canaliculata</i> can mount a complex, multi-organ innate immune response.