Molecular characterization of cell types in the squid Loligo vulgaris

Abstract

Cephalopods are set apart from other mollusks by their advanced behavioral abilities and by the complexity of their nervous systems. Because of the great evolutionary distance that separates vertebrates from cephalopods, it is evident that higher cognitive features have evolved separately in these clades despite the similarities that they share. Alongside their complex behavioral abilities, cephalopods have evolved specialized cells and tissues, such as the chromatophores for camouflage or suckers to grasp prey. Despite significant progress in genome and transcriptome sequencing, the molecular identities of cell types in cephalopods remain largely unknown. We here combine single-cell transcriptomics with in situ gene expression analysis to uncover cell type diversity in the European squid Loligo vulgaris. We describe cell types that are conserved with other phyla such as neurons, muscles, or connective tissues but also cephalopod-specific cells, such as chromatophores or sucker cells. Moreover, we investigate major components of the squid nervous system including progenitor and developing cells, differentiated cells of the brain and optic lobes as well as sensory systems of the head. Our study provides a molecular assessment for conserved and novel cell types in cephalopods and a framework for mapping the nervous system of L. vulgaris.

Expanded Expression of Pro-Neurogenic Factor SoxB1 during Larval Development of GastropodLymnaea stagnalisSuggests Preadaptation to Prolonged Neurogenesis in Mollusca

“…SoxB1-positive ectodermal regions in cephalopods are accompanied by epithelial thickenings, which are hypothesized to give rise to neuronal precursors of the centralized brain (Deryckere et al, 2021). Single-cell transcriptomic data suggest the presence of SoxB1 both in neural migrative precursors together with the expression of Ascl and in some maturing neurons (Duruz et al, 2023).…”

“…In Lottia goshmanii , another representative of the Patellogastropoda, SoxB1 expression has been described in compact zones on the ventral posterior surface of the trochophore (Tan et al, 2022). The role of SoxB1 and SoxB2 in neurogenesis has been most thoroughly studied in cephalopods, Octopus vulgaris and Sepia officinalis (Buresi et al, 2016; Focareta and Cole, 2016; Deryckere et al, 2021; Duruz et al, 2023). The authors of all these papers mention that SoxB1 exhibits broad ectodermal expression at early neurogenic stages and further in development.…”

“…Such factors have been identified for all the main groups of Neuralia representatives from cnidarians to vertebrates and demonstrated high evolutionarily conserved features (Marlow et al, 2014; Moroz, 2015; Arendt et al, 2016; Arendt, 2018; Martín-Durán et al, 2018). In the case of mollusks, such sets of early and late neurogenic factors have been described in detail only for cephalopods (Focareta and Cole, 2016; Deryckere et al, 2021; Duruz et al, 2023) which demonstrate a lot of specific features in their complex nervous system. Data about presence and distribution of pan-neuronal proneurogenic and neurogenic factors are scarce in case of other Molluscan groups, particularly in gastropods.…”

“…In particular, their functions in the most diverse group of Lophotrochozoans - Mollusca - remain obscure. Recent studies on cephalopods have shed light on SoxB-family gene expression and their involvement in the neuronal precursor specification within head ectoderm and developing ganglia (Focareta and Cole, 2016; Deryckere et al, 2021; Duruz et al, 2023). However, cephalopods have a largely modified development without larvae in their life cycle.…”

Functional organization of visual responses in the octopus optic lobe

“…Neurons of the medulla have processes within superficial layers of the optic lobe as well as locally within the medulla, and many project axons out from the optic lobe to downstream visual areas. Recent transcriptomic studies have further revealed a rich diversity of cell types within the optic lobe, as well as extensive sub-laminar organization (Songco-Casey et al 2022; Styfhals et al 2022; Gavriouchkina et al, 2022; Duruz et al 2023).…”