Early Events in the Evolution of Spider Silk Genes

Abstract

Silk spinning is essential to spider ecology and has had a key role in the expansive diversification of spiders. Silk is composed primarily of proteins called spidroins, which are encoded by a multi-gene family. Spidroins have been studied extensively in the derived clade, Orbiculariae (orb-weavers), from the suborder Araneomorphae (‘true spiders’). Orbicularians produce a suite of different silks, and underlying this repertoire is a history of duplication and spidroin gene divergence. A second class of silk proteins, Egg Case Proteins (ECPs), is known only from the orbicularian species, Lactrodectus hesperus (Western black widow). In L. hesperus, ECPs bond with tubuliform spidroins to form egg case silk fibers. Because most of the phylogenetic diversity of spiders has not been sampled for their silk genes, there is limited understanding of spidroin gene family history and the prevalence of ECPs. Silk genes have not been reported from the suborder Mesothelae (segmented spiders), which diverged from all other spiders >380 million years ago, and sampling from Mygalomorphae (tarantulas, trapdoor spiders) and basal araneomorph lineages is sparse. In comparison to orbicularians, mesotheles and mygalomorphs have a simpler silk biology and thus are hypothesized to have less diversity of silk genes. Here, we present cDNAs synthesized from the silk glands of six mygalomorph species, a mesothele, and a non-orbicularian araneomorph, and uncover a surprisingly rich silk gene diversity. In particular, we find ECP homologs in the mesothele, suggesting that ECPs were present in the common ancestor of extant spiders, and originally were not specialized to complex with tubuliform spidroins. Furthermore, gene-tree/species-tree reconciliation analysis reveals that numerous spidroin gene duplications occurred after the split between Mesothelae and Opisthothelae (Mygalomorphae plus Araneomorphae). We use the spidroin gene tree to reconstruct the evolution of amino acid compositions of spidroins that perform different ecological functions.

The Nephila clavipes genome highlights the diversity of spider silk genes and their complex expression

“…First, we saw evidence of new spidroin genes originating from A r t i c l e s tandem-duplication events, as hypothesized in earlier studies 17,26,29,[58][59][60] . We identified pairs of tandem spidroins on two genomic scaffolds (scaffold_16392,…”

Pipeline to Identify Hydroxyproline-Rich Glycoproteins

“…Features of other IDPs can be incorporated into MAAB and used to identify IDPs in available genomes/transcriptomes. This would allow the identification of, for example, the repetitive domains of elastins (Roberts et al, 2015), salivary PRPs (Manconi et al, 2016), insect silks (Starrett et al, 2012), AGL proteins from arbuscular mycorrhizal fungi (Schultz and Harrison, 2008), and LATE EMBRYOGENESIS ABUNDANT proteins in plants (Sun et al, 2013), with low rates of false negatives and false positives.…”

Protein secondary structure of Green Lynx spider dragline silk investigated by solid-state NMR and X-ray diffraction

“…Green Lynx spiders along with other RTA clade spiders are believed to have only one type of spidroin protein (MaSp1) in their dragline silk [43,46–48]. However, the discovery of Pro in Green Lynx dragline silk cannot be explained by the small amount of Pro in the terminal region of the MaSp1 sequence (Fig.…”

“…Assuming Green Lynx dragline silk is similar to other dragline silks and contains two proteins that are similar to MaSp1 and 2 in composition, molecular weight and composition, then we can guess that the MaSp1:MaSp2 ratio in Green Lynx dragline silk would be very close to that of the N. clavipes and Black Widow dragline silks [18,67]. The two spidroins, besides Pro content, show high similarity in amino acid composition, amino acid repetitive motifs and molecular architecture [33,43]. The slight difference in the mechanical properties of the two spidroins [26] ensures the spiders can tailor the physical properties of their silk fibers to adapt to the changes of environment by varying the ratio of the two spidroins.…”

“…Similar to orb-weaver spiders, the RTA clade is also one sub-family in the super family of Entelegynae [34,43–45]. The Green Lynx spiders can produce two types of silks similar to the major and minor ampullate silks of orb-weaver spiders.…”