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

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 nema...

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Bibliographic Details
Main Authors: Alice Montanari, Giulia Bergamini, Agnese Ferrari, Anita Ferri, Milena Nasi, Roberto Simonini, Davide Malagoli
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/9/11/371
Description
Summary: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</i><i> </i><i>hermaphrodita</i>)-based molluscicide exerts dose-dependent lethal effects on the golden apple snail, <i>Pomacea</i><i> </i><i>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>,<i> </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 <i>in situ</i> 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. </i><i>hermaphrodita</i>-based biopesticides enable the sustainable control of <i>P. </i><i>canaliculata</i><i> </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. </i><i>canaliculata</i> can mount a complex, multi-organ innate immune response.
ISSN:2079-7737