A chromosome-level genome of the spider Trichonephila antipodiana reveals the genetic basis of its polyphagy and evidence of an ancient whole-genome duplication event

Abstract

Background The spider Trichonephila antipodiana (Araneidae), commonly known as the batik golden web spider, preys on arthropods with body sizes ranging from ∼2 mm in length to insects larger than itself (>20‒50 mm), indicating its polyphagy and strong dietary detoxification abilities. Although it has been reported that an ancient whole-genome duplication event occurred in spiders, lack of a high-quality genome has limited characterization of this event. Results We present a chromosome-level T. antipodiana genome constructed on the basis of PacBio and Hi-C sequencing. The assembled genome is 2.29 Gb in size with a scaffold N50 of 172.89 Mb. Hi-C scaffolding assigned 98.5% of the bases to 13 pseudo-chromosomes, and BUSCO completeness analysis revealed that the assembly included 94.8% of the complete arthropod universal single-copy orthologs (n = 1,066). Repetitive elements account for 59.21% of the genome. We predicted 19,001 protein-coding genes, of which 96.78% were supported by transcriptome-based evidence and 96.32% matched protein records in the UniProt database. The genome also shows substantial expansions in several detoxification-associated gene families, including cytochrome P450 mono-oxygenases, carboxyl/cholinesterases, glutathione-S-transferases, and ATP-binding cassette transporters, reflecting the possible genomic basis of polyphagy. Further analysis of the T. antipodiana genome architecture reveals an ancient whole-genome duplication event, based on 2 lines of evidence: (i) large-scale duplications from inter-chromosome synteny analysis and (ii) duplicated clusters of Hox genes. Conclusions The high-quality T. antipodiana genome represents a valuable resource for spider research and provides insights into this species’ adaptation to the environment.

Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

“…It seems likely that having a single copy of ftz is common across all spiders (Figures 1-2), consistent with the loss of a duplicate in their common ancestor. A recently published high-quality genome from Trichonephila antipodiana also reported a single copy of ftz (Fan et al 2021), as did another mygalomorph transcriptome, Aphonopelma hentzi (Ontano et al 2020). The absence of Hox3 duplicates in M. muscosa, P. pseudoannulata and P. amentata may indicate a lineage-specific loss in the RTA clade, which unites salticids, lycosids and their allies.…”

“…The origin of Ubx , Dfd , Lab , Hox3 and Scr duplicates in arachnopulmonates is not clear from our phylogenetic analysis alone, with neither orthologs nor paralogs resolving together consistently, and topology that is a poor reflection of phylogeny. However, spider sequences broadly formed two clades with other arachnopulmonates, and synteny analysis in both P. tepidariorum (Schwager et al 2017) and Trichonephila antipodiana (Fan et al 2021) demonstrate clearly that Hox gene duplications therein are the result of WGD. The placement of the amblypygid and scorpion duplicates was more variable.…”

“…If selected Hox duplicates are indeed absent from the genomes of these two species, this represents an interesting divergence between the three major groups of spiders. Although it may seem unusual for Hox duplicates to be lost within lineages, a recent high-quality genome of Trichonephila antipodiana revealed likely absences of Hox3 , Ubx and abdA ohnologs in addition to ftz (Fan et al 2021). Though they are unlikely to be directly responsible, the apparent divergence in gene repertoires we see between A. geniculata , P. phalangioides and the other spider lineages might provide a starting point for understanding the important morphological differences between mygalomorphs, synspermiatans and entelegynes.…”

Chromosome-scale assembly of the Canary Island endemic spider Dysdera silvatica (Arachnida, Araneae) sheds light on the origin and genome structure of chemoreceptor gene families in spiders

“…Despite this great representation and special interest in many basic and translational research areas, such as material sciences (silk from spiders), bioactive natural compounds (venom toxins from spiders and scorpions), or pest control (mites, Acari), there are currently very few available genome sequences of species from this group (Garb et al, 2018;Thomas et al, 2020;Vizueta, Rozas, & Sánchez-Gracia, 2018), being most of them highly fragmented and incomplete. In fact, only two chromosome-level spider genomes have been reported to date (Fan et al, 2021;Sheffer et al, 2021).…”

Darwin’s bark spider shares a spidroin repertoire with Caerostris extrusa but achieves extraordinary silk toughness through gene expression

“…2c, d, and Table 2). The genome size of C. darwini was estimated with GenomeScop 18 based on the k-mer distribution to be 1.58 Gbp, which is relatively small relative to other spider genomes, which average over 2.50 Gbp in size 19 . The assembled scaffolds were assessed by Benchmarking Universal Single-Copy Ortholog (BUSCO) analysis 20 , and the completeness scores of C. darwini and C. extrusa were 92.6% and 82.7%, respectively (Fig.…”