Chromosomal‐level genome of a sheet‐web spider provides insight into the composition and evolution of venom

Abstract

Spiders are the most abundant venomous predators in the world. Previous research related to spider venom has mostly relied on transcriptomes and proteomes, with only a few high-quality genomes available. This is far from consistent with the species diversity of spiders. In this study, we constructed a high-quality chromosome-level genome assembly of Hylyphantes graminicola, which contained 13 chromosomes, with a genome length of 931.68 Mb and scaffold N50 of 77.07 Mb. Integrating genome, transcriptome, and proteome profiling, we identified a total of 59 coding genes among nine toxin gene families. Among them, Group 7 allergen (ALL7) protein was reported in spider venom for the first time. Its coding genes had a predicted signal peptide and maintained high expression levels in the venom, suggesting that ALL7 plays an important role in venom and maybe is a type of newly discovered venom toxin in the spider. By implementing comparative genomics, we found a similar gene number of main toxin gene families in spiders and the scorpion genome with conservative evolutionary rates, indicating that these toxin genes could be an ancient (~400 million years) and a conserved "basic toolkit" for spiders and scorpions to perform primary defence functions. Obtaining high-quality chromosome-level genomes from spiders not only facilitates venom research and toxin resource application, but also can improve comparative genomic analysis in other important traits, like the evolution of silk or behaviour.

Genomic and transcriptomic analyses support a silk gland origin of spider venom glands

“…1 a). Unexpectedly, only a few previously identified toxin-coding genes [ 12 ] or genes detected in the venom proteome [ 24 ] were found in module 1, and many of them were assigned to the grey60 module (module 16; Additional file 1 : Table S5), suggesting that the core network may have relatively weak regulation for toxins in the common house spider venom glands.

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“…Previous reviews have highlighted that spider venom systems are derived from the salivary glands or evolved from the silk-producing glands present in early chelicerates [ 8 , 9 ]. For the former hypothesis, many digestive proteases that are also produced by spider venom glands cause tissue destruction and facilitate toxin penetration or are involved in the initial extra-oral digestion process of the prey [ 10 – 12 ]. Spider venom systems were thus assumed to be derived from modified salivary glands [ 9 , 13 ], similar to snakes [ 14 ] and a handful of insectivorous mammals [ 2 ].…”

Chromosome-level genome and the identification of sex chromosomes in Uloborus diversus

“…Spider genomes are enormous with high repeat content, making them challenging to assemble [ 24–26 ]. While 22 spider genomes have been assembled and made publicly available [ 24 , 27–42 ] ( Supplementary Table S1 ), most are highly fragmented, with 7 assembled to chromosome scale [ 29 , 32 , 35 , 37 , 38 , 41 , 42 ]. Of the 22 genomes, only 7 represent the Araneoidea [ 28 , 29 , 32 , 39 ] or ecribellate orb-weavers, 2 of which have been assembled to chromosome scale [ 29 , 32 ].…”

Chromosome-level genome and the identification of sex chromosomes in Uloborus diversus

“…Spider genomes are enormous with high repeat content, making them challenging to assemble(Sanggaard et al 2014; Stellwagen and Renberg 2019; Ayoub et al 2013). While 22 spider genomes have been assembled and made publicly available(Sanggaard et al 2014; Babb et al 2017; Kono et al 2019; Sheffer et al 2021; Sánchez-Herrero et al 2019; Schwager et al 2017; Fan et al 2021; Yu et al 2019; Liu et al 2019; Escuer et al 2022; Cerca et al 2021; Zhu et al 2022; Hendrickx et al 2022; Kono et al 2021a; Purcell and Pruitt 2019; Li et al 2022; Kono et al 2021b) ( Table S1 ), most are highly fragmented, with 6 assembled to chromosome-scale(Sheffer et al 2021; Fan et al 2021; Escuer et al 2022; Zhu et al 2022; Hendrickx et al 2022; Kono et al 2021b). Of the 22 genomes, only 7 represent the Araneoidea(Kono et al 2019; Sheffer et al 2021; Fan et al 2021; Kono et al 2021a) or ecribellate orb-weavers, 2 of which have been assembled to chromosome-scale(Sheffer et al 2021; Fan et al 2021).…”