Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution

Abstract

1Understanding the drivers of morphological diversity is a persistent challenge in evolutionary 1 2 biology. Here, we investigate functional diversification of secretory cells in the sea anemone 1 3Nematostella vectensis to understand the mechanisms promoting cellular specialization across 1 4 animals. We demonstrate regionalized expression of gland cell subtypes in the internal ectoderm 1 5 of N. vectensis and show that adult gland cell identity is acquired very early in development. A 1 6phylogenetic survey of trypsins across animals suggests this gene family has undergone 1 7 numerous expansions. We reveal unexpected diversity in trypsin protein structure and show that 1 8 trypsin diversity arose through independent acquisitions of non-trypsin domains. Finally, we 1 9 3 1 arise by secondary epithelial fold morphogenesis following completion of gastrulation (1). 2Additional growth and differentiation of both internalized layers results in the morphogenesis of 3 3 3 the pharynx and mesenteries and in an adult form quite different from that of medusozoans. In 3 4 anthozoans, both layers (endoderm and ectoderm) are in contact with the gastric cavity, whereas 3 5 in medusozoans (and, indeed, most other animals), the gastrovascular cavity is lined only by 3 6 endoderm. 3 7 3 8 Nematostella vectensis, the starlet sea anemone, has become a valuable model for studies of 3 9 animal body plan evolution (2-6); yet, little is known about the extent of cell diversity in the 4 0 tissues that comprise the pharynx and mesenteries. The endodermal component of the 4 1 mesenteries houses the germ cell precursors and two types of muscle cells and the few recent 4 2 studies of the mesenteries in Nematostella have focused largely on these endodermal functions 4 3 (7-9). The ectodermal component of the mesenteries is known to be populated by cnidocytes and 4 4 gland cells (10) and two recent studies demonstrated the expression of multiple proteases in the 4 5 mesenteries of N. vectensis (11, 12). Trypsins are the largest family of proteases, and although 4 6 they have diverse functions, most trypsins are secreted to the extracellular environment and are 4 7 therefore expressed in zymogen-type gland cells (13). A previous study cataloging trypsin 4 8 diversity from prokaryotes and eukaryotes identified 75 trypsins in the genome of N. vectensis 4 9

Revealing the Systematic Nature of Coral Attachment to Reef Substrates

“…Histological analysis of the laments also con rmed that the cnidoglandular band possesses numerous secretory gland cells (Fig. 4), which are capable of producing variations in mucus development 23 and digesting matter 52 (Fig. 4E).…”

“…Hence, we can infer that these cells remove foreign debris and function to protect the epidermis from foreign materials, including benthic organisms, bacteria, or pathogens. Perhaps either by producing zymogen vesicles capable of exocytosis 52 , which are also known to migrate to the apical surface of the cell 54, or lipopolysaccharide endotoxins that protect the epithelium from bacteria 55,70 . However, further analysis will be required to verify their exact function.…”

“…Mesenterial laments possess several secretory cells that are capable of cell digestion and mucus production (Fig. 3, 6) [52][53][54][55][56] .…”

Evolutionary assembly of cooperating cell types in an animal chemical defense system

“…Venom glands of wasps, scorpions, and cone snails; the explosive weaponry of bombardier beetles; and diverse mammalian scent glands are multicellular novelties composed of taxon-restricted cell types found nowhere else. For many such organs, including vertebrate salivary glands (Roussa, 2011), moth silk glands (Suzuki et al, 1990), cnidarian digestive glands (Babonis et al, 2019), and venom glands of many species (Surm and Moran, 2021), the final secretion is a cocktail produced by distinct secretory cell types. Biosynthetic synergism between cell types is pronounced in many small molecule-based chemical defense systems.…”

Knockout of a singleSoxgene resurrects an ancestral cell type in the sea anemoneNematostella vectensis

“…An infrared laser ablation system (XYClone, Hamilton Thorne) was used to induce discharge from tentacle tip cnidocytes with 100% power and a 500us pulse. Phylogenetic analysis of HMG domains was performed using translated transcriptomes as described previously (40). Full methods are provided in the Supplementary Information.…”