Characterization of the genome and silk-gland transcriptomes of Darwin’s bark spider (Caerostris darwini)

Abstract

Natural silks crafted by spiders comprise some of the most versatile materials known. Artificial silks–based on the sequences of their natural brethren–replicate some desirable biophysical properties and are increasingly utilized in commercial and medical applications today. To characterize the repertoire of protein sequences giving silks their biophysical properties and to determine the set of expressed genes across each unique silk gland contributing to the formation of natural silks, we report here draft genomic and transcriptomic assemblies of Darwin’s bark spider, Caerostris darwini, an orb-weaving spider whose dragline is one of the toughest known biomaterials on Earth. We identify at least 31 putative spidroin genes, with expansion of multiple spidroin gene classes relative to the golden orb-weaver, Trichonephila clavipes. We observed substantial sharing of spidroin repetitive sequence motifs between species as well as new motifs unique to C. darwini. Comparative gene expression analyses across six silk gland isolates in females plus a composite isolate of all silk glands in males demonstrated gland and sex-specific expression of spidroins, facilitating putative assignment of novel spidroin genes to classes. Broad expression of spidroins across silk gland types suggests that silks emanating from a given gland represent composite materials to a greater extent than previously appreciated. We hypothesize that the extraordinary toughness of C. darwini major ampullate dragline silk may relate to the unique protein composition of major ampullate spidroins, combined with the relatively high expression of stretchy flagelliform spidroins whose union into a single fiber may be aided by novel motifs and cassettes that act as molecule-binding helices. Our assemblies extend the catalog of sequences and sets of expressed genes that confer the unique biophysical properties observed in natural silks.

Chromosome-level genome of spider Pardosa pseudoannulata and cuticle protein genes in environmental stresses

“…Moreover, spiders are important model for evolution and adaptive radiation given the varied environmental conditions of their habitats 3 . Taking advantage of the ever expanding genomic information, researchers are able to untangle different aspects of spider biology, with particular interest on venom, silk, and the phylogeny 4 – 17 . The increasing numbers of genomes will facilitate the phylogenomic study to unravel the roots of spiders and comparative studies to decipher the morphological and behavioural traits of spiders.…”

Grand challenges in research on arachnid diversity, conservation, and biogeography

“…Furthermore, arachnids are prolific producers of biomaterials most notable among which are venoms and silks (Foelix, 2011). The variety of such biomaterials (Sethy and Ahi, 2022), and their genetic underpinnings (Arakawa et al, 2022;Babb et al, 2022)-most of which remain largely unknown (e.g. we know only a handful of the likely hundreds of thousands of silk types produced by tens of thousands of species)represent underappreciated dimensions of biodiversity.…”

The seven grand challenges in arachnid science

“…Evidence has been found for ancient lateral gene transfer events to arachnids from bacteria or fungi (Dong et al, 2018). Genomic and transcriptomic studies have so far focused on annotating gene families that encode for morphological development (Hoy et al, 2016;Zhang et al, 2019;Harper et al, 2021), for venom neurotoxins (Cao et al, 2013;Yu et al, 2019), for silks (Babb et al, 2017;Garb et al, 2019;Kono et al, 2021;Babb et al, 2022), for dietary characteristics (Grbicé t al., 2011;Hoy et al, 2016;Fan et al, 2021), for enzymes that cause allergies in vertebrates (Dong et al, 2018), for candidate genes for sex determination (Hoy et al, 2016;Miller et al, 2022), and for genes important for the innate immune system (Shingate et al, 2020). Large scale comparative genomics has also started to understand the genetic basis for tick-borne diseases (Jia et al, 2020).…”

“…Babb et al (2017) annotated 28 spidroin genes in Trichonephila clavipes and found their expression in several silk glands to be complex, as well as sex-specific (Correa-Garhwal et al, 2021). The genomes and transcriptomes of bark spiders (genus Caerostris) reveal a repertoire of no fewer than 31 spidroins (Garb et al, 2019;Kono et al, 2021;Babb et al, 2022). In comparison, studies of the genomes of other spiders have annotated fewer spidroins: 11 in Araneus ventricosus (Kono et al, 2019), 10 in Uloborus diversus (Miller et al, 2022), 16 in a non-web-building wolf spider (Yu et al, 2019).…”