The genome of the simultaneously hermaphroditic snail Lymnaea stagnalis reveals an evolutionary expansion of FMRFamide-like receptors

The great pond snail Lymnaea stagnalis has served as a model organism for over a century in diverse disciplines such as neurophysiology, evolution, ecotoxicology and developmental biology. To support both established uses and newly emerging research interests we have performed whole genome sequencing (avg.176 × depth), assembly and annotation of a single individual derived from an inbred line. These efforts resulted in a final assembly of 943 Mb (L50 = 257; N50 = 957,215) with a total of 22,499 predicted gene models. The mitogenome was found to be 13,834 bp long and similarly organized as in other lymnaeid species, with minor differences in location of tRNA genes. As a first step towards understanding the hermaphroditic reproductive biology of L. stagnalis, we identified molecular receptors, specifically nuclear receptors (including newly discovered 2xDNA binding domain-NRs), G protein-coupled receptors, and receptor tyrosine kinases, that may be involved in the cellular specification and maintenance of simultaneously active male and female reproductive systems. A phylogenetic analysis of one particular family of GPCRs (Rhodopsin neuropeptide FMRFamide-receptor-like genes) shows a remarkable expansion that coincides with the occurrence of simultaneous hermaphroditism in the Euthyneura gastropods. As some GPCRs and NRs also showed qualitative differences in expression in female (albumen gland) and male (prostate gland) organs, it is possible that separate regulation of male and female reproductive processes may in part have been enabled by an increased abundance of receptors in the transition from a separate-sexed state to a hermaphroditic condition. These findings will support efforts to pair receptors with their activating ligands, and more generally stimulate deeper insight into the mechanisms that underlie the modes of action of compounds involved in neuroendocrine regulation of reproduction, induced toxicity, and development in L. stagnalis, and molluscs in general.

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Publication Details

Journal
Scientific Reports
Published
2024-11-25
DOI
https://doi.org/10.1038/s41598-024-78520-1
Citations
6
Primary Topic
Neurobiology and Insect Physiology Research
Type
article
Field-Weighted Citation Impact
1.61

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article

The genome of the simultaneously hermaphroditic snail Lymnaea stagnalis reveals an evolutionary expansion of FMRFamide-like receptors

Mohammed‐Amin Madoui, Benjamin Noël, Corinne Da Silva, Patrick Wincker et al.
6 citations
Scientific Reports
Neurobiology and Insect Physiology Research
1.61
article

The genome of the simultaneously hermaphroditic snail Lymnaea stagnalis reveals an evolutionary expansion of FMRFamide-like receptors

Mohammed‐Amin Madoui, Benjamin Noël, Corinne Da Silva, Patrick Wincker, Karine Labadie, Julie Poulain, Yumi Nakadera, Coen M. Adema, Daniel J. Jackson, Nicolas Cerveau, Joris M. Koene, Véronique Jamilloux, Jean‐Marc Aury, Zhong‐Ping Feng, Christophe Klopp, Marie‐Agnès Coutellec, Angus Davison
article en
6 citations

Abstract

The great pond snail Lymnaea stagnalis has served as a model organism for over a century in diverse disciplines such as neurophysiology, evolution, ecotoxicology and developmental biology. To support both established uses and newly emerging research interests we have performed whole genome sequencing (avg.176 × depth), assembly and annotation of a single individual derived from an inbred line. These efforts resulted in a final assembly of 943 Mb (L50 = 257; N50 = 957,215) with a total of 22,499 predicted gene models. The mitogenome was found to be 13,834 bp long and similarly organized as in other lymnaeid species, with minor differences in location of tRNA genes. As a first step towards understanding the hermaphroditic reproductive biology of L. stagnalis, we identified molecular receptors, specifically nuclear receptors (including newly discovered 2xDNA binding domain-NRs), G protein-coupled receptors, and receptor tyrosine kinases, that may be involved in the cellular specification and maintenance of simultaneously active male and female reproductive systems. A phylogenetic analysis of one particular family of GPCRs (Rhodopsin neuropeptide FMRFamide-receptor-like genes) shows a remarkable expansion that coincides with the occurrence of simultaneous hermaphroditism in the Euthyneura gastropods. As some GPCRs and NRs also showed qualitative differences in expression in female (albumen gland) and male (prostate gland) organs, it is possible that separate regulation of male and female reproductive processes may in part have been enabled by an increased abundance of receptors in the transition from a separate-sexed state to a hermaphroditic condition. These findings will support efforts to pair receptors with their activating ligands, and more generally stimulate deeper insight into the mechanisms that underlie the modes of action of compounds involved in neuroendocrine regulation of reproduction, induced toxicity, and development in L. stagnalis, and molluscs in general.

Scientific ReportsVol. 14(1)
University of New Brunswick (CA), Centre National de la Recherche Scientifique (FR), University of Nottingham (GB), Ifremer (FR), University of New Mexico (US), University of Toronto (CA), Bielefeld University (DE), Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR), Université Paris-Saclay (FR), Canada Research Chairs (CA), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Génomique Métabolique du Genoscope (FR), CEA Paris-Saclay - Etablissement de Fontenay-aux-roses (FR), Direction de la Recherche Fondamentale (FR), Genoscope (FR), CEA Paris-Saclay (FR), Ecology and Ecosystem Health (FR), Écologie et Biologie des Interactions (FR), Génétique Physiologie et Systèmes d'Elevage (FR), University of Göttingen (DE), Vrije Universiteit Amsterdam (NL)
Deutsche Forschungsgemeinschaft, Agence Nationale de la Recherche, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Openalex Percentile: Top 17%
Neurobiology and Insect Physiology Research
1.61
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