Desmosomal connectomics of all somatic muscles in an annelid larva

Abstract

Cells form networks in animal tissues through synaptic, chemical and adhesive links. Invertebrate muscle cells often connect to other cells through desmosomes, adhesive junctions anchored by intermediate filaments. To study desmosomal networks, we skeletonised 853 muscle cells and their desmosomal partners in volume electron microscopy data covering an entire larva of the annelid Platynereis. Muscle cells adhere to each other, to epithelial, glial, ciliated, and bristle-producing cells and to the basal lamina, forming a desmosomal connectome of over 2,000 cells. The aciculae - chitin rods that form an endoskeleton in the segmental appendages - are highly connected hubs in this network. This agrees with the many degrees of freedom of their movement, as revealed by video microscopy. Mapping motoneuron synapses to the desmosomal connectome allowed us to infer the extent of tissue influenced by motoneurons. Our work shows how cellular-level maps of synaptic and adherent force networks can elucidate body mechanics.

Whole-body connectome of a segmented annelid larva

“…The effector system is multi-modal, and includes muscles, locomotor multiciliated cells, glands and pigment cells. The musculature is composed of 53 distinct muscle cell-types, is segmental, and extends to the parapodia that are supported by a chitin-based endoskeleton (aciculae) (Jasek et al, 2022).…”

“…Of these, 3128 were classified into 92 nonneuronal cell types (Supplementary Table 1, Figure 3-figure supplement 1). These included epidermal cells (1334 cells), various pigment cells (158 cells of 7 types), muscle cells (853 cells of 53 types, described in (Jasek et al, 2022)), locomotor ciliated cells (80 cells of 6 types, described in (Verasztó et al, 2017)), glial cells (78 cells of 3 types), gland cells (54 cells of 6 types), various support and sheet cells, nephridia, putative migratory cells, parapodial cells producing chitin chaetae (106 cells) or aciculae (12 cells), and the follicle cells (566 cells of 5 types) ensheathing them (Supplementary Table 1; Video 1; Figure 3-figure supplement 1).…”

“…Here we report the complete synaptic connectome and the cell-type complement of a three-day-old larva (nectochaete stage) of the marine annelid Platynereis dumerilii . This larval stage has three trunk segments, adult and larval eyes, segmental ciliary bands and a well-developed somatic musculature (Jasek et al, 2022). The larvae show several behaviours, including visual phototaxis (Randel et al, 2014), UV avoidance (Verasztó et al, 2018), a startle response (Bezares-Calderón et al, 2018) and coordinated ciliary activity (Verasztó et al, 2017).…”

Mechanism of barotaxis in marine zooplankton

“…The sensory and neuronal bases of light-guided (Gühmann et al 2015 ;Randel et al 2014 ;Verasztó et al 2018 ) and mechanically-driven behaviours (Luis A. Bezares-Calderón et al 2018) in Platynereis larvae have been dissected due to the experimental tractability of this system. Its small size has allowed the entire reconstruction of the cellular and synaptic wiring map of the three-day-old larva (Verasztó et al 2020 ;Jasek et al 2022 ). Here we study Platynereis larvae to understand the cellular and neuronal bases of pressure sensation in zooplankton.…”

Mechanism of barotaxis in marine zooplankton

“…The sensory and neuronal bases of light-guided (Gühmann et al, 2015; Randel et al, 2014; Verasztó et al, 2018) and mechanically-driven behaviours (Bezares-Calderón et al, 2018) in Platynereis larvae have been dissected due to the experimental tractability of this system. Its small size has allowed the entire reconstruction of the cellular and synaptic wiring map of the three-day-old larva (Jasek et al, 2022; Jékely et al, 2024). Here we study Platynereis larvae to understand the cellular and neuronal bases of pressure sensation in zooplankton.…”