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Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host–symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum , a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection. Symbiotic partners are rarely studied in equal depth. By assembling new genomes, Lan et al . report a novel dual symbiosis in the snail Gigantopelta aegis with two evolutionarily distant gammaproteobacterial endosymbionts: one which oxidises sulfur, the other, methane in a metabolically mutualistic relationship.

As ecosystem disruptors and intermediate hosts for various parasites, freshwater snails have significant socioeconomic impacts on human health, livestock production, and aquaculture. Although traditional molluscicides have been widely used to mitigate these effects, their environmental impact has encouraged research into alternative, biologically based strategies to create safer, more effective molluscicides and diminish the susceptibility of snails to parasites. This review focuses on alterations in glucose metabolism in snails under the multifaceted stressors of parasitic infections, drug exposure, and environmental changes and proposes a novel approach for snail management. Key enzymes within the glycolytic pathway, such as hexokinase and pyruvate kinase; tricarboxylic acid (TCA) cycle; and electron transport chains, such as succinate dehydrogenase and cytochrome c oxidase, are innovative targets for molluscicide development. These targets can affect both snails and parasites and provide an important direction for parasitic disease prevention research. For the first time, this review summarises the reverse TCA cycle and alternative oxidase pathway, which are unique metabolic bypasses in invertebrates that have emerged as suitable targets for the formulation of low-toxicity molluscicides. Additionally, it highlights the importance of other metabolic pathways, including lactate, alanine, glycogenolysis, and pentose phosphate pathways, in snail energy supply, antioxidant stress responses, and drug evasion mechanisms. By analysing the alterations in key metabolic enzymes and their products in stressed snails, this review deepens our understanding of glucose metabolic alterations in snails and provides valuable insights for identifying new pharmacological targets.

Invasive invertebrate pests have become a major threat to food security as global populations increase. Pesticides, often containing organophosphates, have long been used as agents for providing immediate short-term recovery, yet are often broad-spectrum, leading to the development of resistance. In insect species, one mechanism for resistance is known to be driven by mutations in acetylcholinesterase (AChE), an enzyme that catalyses the hydrolysis of acetylcholine. In this study, we explored a potential role for resistance-modified AChE in invasive pest land snails, using the Mediterranean snail Theba pisana . Following tissue transcriptomic investigation, an expanded family of AChE-like genes were identified that clustered phylogenetically into three individual clades, with one clade including vertebrate AChE. The majority of T. pisana AChE-like genes demonstrated the highest expression in the snail mucous gland during its reproductive stage. Subsequent proteomic analysis of trail mucus at the reproductive stage identified four AChE-like proteins as a major component. Immunolocalisation revealed that AChE-like protein(s) were prominent in the mucous gland secretory cells and widespread throughout the reproductive stage trail mucus, yet were largely absent from trail mucus at the non-reproductive stage. In summary, this study established a potential role for resistance-modified AChE-like proteins in pest land snail pesticide resistance via their deployment into trail mucus that may bio-scavenge organophosphates, rendering them ineffective. Their abundance during the reproductive stage is likely due to the snail’s increased mobility, following periods of immobile aestivation.

This is a critical review of what we know so far about the evolution of metallothioneins (MTs) in Gastropoda (snails, whelks, limpets and slugs), an important class of molluscs with over 90,000 known species. Particular attention will be paid to the evolution of snail MTs in relation to the role of some metallic trace elements (cadmium, zinc and copper) and their interaction with MTs, also compared to MTs from other animal phyla. The article also highlights the important distinction, yet close relationship, between the structural and metal-selective binding properties of gastropod MTs and their physiological functionality in the living organism. It appears that in the course of the evolution of Gastropoda, the trace metal cadmium (Cd) must have played an essential role in the development of Cd-selective MT variants. It is shown how the structures and Cd-selective binding properties in the basal gastropod clades have evolved by testing and optimizing different combinations of ancestral and novel MT domains, and how some of these domains have become established in modern and recent gastropod clades. In this context, the question of how adaptation to new habitats and lifestyles has affected the original MT traits in different gastropod lineages will also be addressed. The 3D structures and their metal binding preferences will be highlighted exemplarily in MTs of modern littorinid and helicid snails. Finally, the importance of the different metal requirements and pathways in snail tissues and cells for the shaping and functionality of the respective MT isoforms will be shown.

Cadmium (Cd) pollution poses an important problem, but limited information is available about the toxicology effects of Cd on freshwater invertebrates. We investigated the accumulation, oxidative stress, microbial community changes, and transcriptomic alterations in apple snails (Pomacea canaliculata) under Cd stress. The snails were exposed to the 10 μg/L Cd solution for 16 days, followed by a 16-day elimination period. Our results showed that the liver accumulated the highest Cd concentration (17.41 μg/g), followed by the kidneys (8.00 μg/g) and intestine-stomach (6.68 μg/g), highlighting these tissues as primary targets for Cd accumulation. During the elimination period, Cd concentrations decreased in all tissues, with the head-foot and shell exhibiting over 30% elimination rates. Cd stress also resulted in reduced activities of superoxide dismutase (SOD), catalase (CAT), and glutathione transferase (GST) compared to the control group. Notably, even after 16 days of depuration, the enzyme activities did not return to normal levels, indicating persistent toxicological effects. Cd exposure significantly reduced the diversity of gut microbiota in P. canaliculata. Moreover, transcriptome analysis identified differentially expressed genes (DEGs) primarily associated with lysosome function, motor proteins, protein processing in the endoplasmic reticulum, drug metabolism via cytochrome P450 (CYP450), arachidonic acid metabolism, and ECM–receptor interactions. These findings suggest that Cd stress predominantly disrupts cellular transport and metabolic processes. Overall, our study provides comprehensive insights into the toxicological impact of Cd on P. canaliculata and emphasizes the importance of understanding the mechanisms underlying Cd toxicity in aquatic organisms.

The snail that turned The chirality (direction of coiling) of snail shells is an enduring biological puzzle. Cristina Grande and Nipam Patel now show that snail chirality is regulated by nodal , a gene well known for its role in vertebrate left-right asymmetry. Most animals are bilaterally symmetrical, but within that framework display varying amounts of left-right asymmetry. In vertebrates and other deuterostomes, the molecular pathway that leads to asymmetry utilizes the signalling molecule Nodal. Grande and Patel found orthologues (evolutionary equivalents) of Nodal and one of its targets, Pitx, in two species of snail, and show that loss of nodal disrupts shell coiling. This shows that the nodal signalling pathway is primitive for all bilaterians, and is not a particular feature of deuterostomes, as had been suspected. In vertebrates and other deuterostomes, the molecular pathway that leads to asymmetry utilizes the signalling molecule Nodal, a member of the TGF-β superfamily. But no orthologues of Nodal have been found in the other two great groups of bilaterians. This paper finds orthologues of nodal and one of its targets, Pitx , in two species of snail, and show that loss of nodal disrupts shell coiling. Many animals display specific internal or external features with left–right asymmetry. In vertebrates, the molecular pathway that leads to this asymmetry uses the signalling molecule Nodal, a member of the transforming growth factor-β superfamily 1 , which is expressed in the left lateral plate mesoderm 2 , and loss of nodal function produces a randomization of the left–right asymmetry of visceral organs 3 , 4 . Orthologues of nodal have also been described in other deuterostomes, including ascidians and sea urchins 5 , 6 , but no nodal orthologue has been reported in the other two main clades of Bilateria: Ecdysozoa (including flies and nematodes) and Lophotrochozoa (including snails and annelids). Here we report the first evidence for a nodal orthologue in a non-deuterostome group. We isolated nodal and Pitx (one of the targets of Nodal signalling) in two species of snails and found that the side of the embryo that expresses nodal and Pitx is related to body chirality: both genes are expressed on the right side of the embryo in the dextral (right-handed) species Lottia gigantea and on the left side in the sinistral (left-handed) species Biomphalaria glabrata . We pharmacologically inhibited the Nodal pathway and found that nodal acts upstream of Pitx, and that some treated animals developed with a loss of shell chirality. These results indicate that the involvement of the Nodal pathway in left–right asymmetry might have been an ancestral feature of the Bilateria.

Terrestrial snails tolerate elevated concentrations of cadmium and copper, accumulating both metals in their soft tissues. The snails are able to inactivate the toxic cadmium while meeting their metabolic requirement for copper. Here we report evidence for the metabolic discrimination between the two metals based on the existence of distinct metallothionein isoforms, one dedicated to cadmium detoxification and another to copper regulation.

Perfluorooctane sulfonate (PFOS), which is known for its environmental persistence and bioaccumulation, poses substantial impacts to aquatic ecosystems. This study assesses the toxic effects of PFOS in the freshwater snail Lanistes carinatus using biomarkers for antioxidant activity, neurotoxicity, and tissue damage. Snails exposed to PFOS (1, 3, 10 mg/L for 14 days) displayed lipid peroxidation (LPO) levels that increased by 16.3–67.5%, and malondialdehyde (MDA) levels that rose by 10.0–58.4%, indicating oxidative damage. Enzyme activities for glutathione S-transferase (GST), glutathione peroxidase (GPx), and catalase (CAT) increased, ranging from 10.0 to 58.3%, 10.0 to 58.4%, and 10.0 to 58.4%, respectively, whereas levels of reduced glutathione (GSH) dropped by 15.0–41.5% and Superoxide dismutase (SOD) decreased by 15.0–41.4%. The activity of acetylcholinesterase (AchE) was reduced by a range of 15.0–40.0%, suggesting neurotoxic effects. Histopathological changes in the digestive gland were also noted. Further research on the effects of PFOS on mollusks is required, and investigation into sex-specific toxicity is needed. This shed light on L. carinatus as a sentinel species, providing helpful information for the monitoring and regulation of PFOS in aquatic environments.

The ecotoxicological consequences of azoxystrobin on land snails have not yet been addressed. Therefore, the present study aims to provide novel data on the threat of a commercial grade azoxystrobin (AMISTAR) at two environmentally relevant concentrations (0.3 µg/ml) and tenfold (3 µg/ml) on the model species,  Theba   pisana by physiological, biochemical, and histopathological markers for 28 days. Our results showed a reduction in animal food consumption and growth due to exposure to both azoxystrobin concentrations. It also induced oxidative stress and led to a significant decrease in lipid peroxidation (LPO) levels after 7 days of exposure, while the opposite effect occurred after 28 days. Except for the 7-day exposure, all treated snails had significantly reduced glutathione (GSH) content and increased catalase (CAT) activity at all-time intervals. Glutathione peroxidase (GPx), glutathione-S-transferase (GST) activities, and protein content (PC) were elevated in treated snails at all-time intervals. Moreover, alterations in acetylcholinesterase (AChE) activity between a decrease and an increase were noticed. Additionally, azoxystrobin exerted changes in T. pisana hepatopancreas architecture. Our study suggests that azoxystrobin may have negative ecological consequences for T. pisana and highlights its potential risks to the natural environment.

Angiostrongylus cantonensis, the causative agent of human eosinophilic meningitis, utilizes terrestrial and freshwater gastropods as intermediate hosts. However, the molecular mechanisms underlying these host-parasite interactions remain unclear. We applied four-dimensional label-free quantitative (4D-LFQ) proteomics to examine proteomic alterations in infected versus uninfected specimens of two intermediate snail hosts, Lissachatina fulica and Pomacea canaliculata. Differentially expressed proteins (DEPs) were identified, followed by Gene Ontology (GO) enrichment and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses. In infected Lissachatina, 36 proteins were upregulated and 104 downregulated, while in infected Pomacea, 94 were upregulated and 364 downregulated. GO analysis revealed 111 enriched terms linked to 71 DEPs in Lissachatina and 484 terms associated with 389 DEPs in Pomacea. KEGG pathway enrichment (Level 3) showed predominant downregulation, including 12 of 20 pathways in Lissachatina and 18 of 20 in Pomacea. Both species shared downregulation in essential pathways: ribosome, proteasome, aminoacyl-tRNA biosynthesis (genetic information processing); glycolysis/gluconeogenesis, pyruvate metabolism, sulfur metabolism (metabolic); and phagosome formation and endocytosis (immune-related). Protein-protein association (PPA) analysis identified conserved hub proteins, Tr-type G domain and T-complex chaperonins, indicating coordinated disruption of translational and proteostatic processes in both groups. Our findings suggest that A. cantonensis can modulate host immunity and metabolism, suppressing key protective responses in both gastropod hosts. This proteomic data may serve as a foundation for discovering biomarkers and designing interventions to disrupt the parasite's life cycle.