Duplication and concerted evolution of MiSp-encoding genes underlie the material properties of minor ampullate silks of cobweb weaving spiders

Abstract

BackgroundOrb-web weaving spiders and their relatives use multiple types of task-specific silks. The majority of spider silk studies have focused on the ultra-tough dragline silk synthesized in major ampullate glands, but other silk types have impressive material properties. For instance, minor ampullate silks of orb-web weaving spiders are as tough as draglines, due to their higher extensibility despite lower strength. Differences in material properties between silk types result from differences in their component proteins, particularly members of the spidroin (spider fibroin) gene family. However, the extent to which variation in material properties within a single silk type can be explained by variation in spidroin sequences is unknown. Here, we compare the minor ampullate spidroins (MiSp) of orb-weavers and cobweb weavers. Orb-web weavers use minor ampullate silk to form the auxiliary spiral of the orb-web while cobweb weavers use it to wrap prey, suggesting that selection pressures on minor ampullate spidroins (MiSp) may differ between the two groups.ResultsWe report complete or nearly complete MiSp sequences from five cobweb weaving spider species and measure material properties of minor ampullate silks in a subset of these species. We also compare MiSp sequences and silk properties of our cobweb weavers to published data for orb-web weavers. We demonstrate that all our cobweb weavers possess multiple MiSp loci and that one locus is more highly expressed in at least two species. We also find that the proportion of β-spiral-forming amino acid motifs in MiSp positively correlates with minor ampullate silk extensibility across orb-web and cobweb weavers.ConclusionsMiSp sequences vary dramatically within and among spider species, and have likely been subject to multiple rounds of gene duplication and concerted evolution, which have contributed to the diverse material properties of minor ampullate silks. Our sequences also provide templates for recombinant silk proteins with tailored properties.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0927-x) contains supplementary material, which is available to authorized users.

Molecular evolution of gland cell types and chemical interactions in animals

“…Protein venoms have been widely studied as models of gene family evolution (Fry et al, 2009(Fry et al, , 2006Wong and Belov, 2012), and evidence from venom glands of diverse species including snakes, spiders, cone snails and centipedes indicates that gene duplication is the prevailing mechanism for evolving novel protein secretions (Casewell et al, 2011;Dowell et al, 2016;Ellsworth et al, 2019;Fry et al, 2009Fry et al, , 2006Wong and Belov, 2012). Further support comes from spider silk glands, where largescale duplication of spidroin genes, which encode primary silk proteins, enabled evolution of specialized silk types with different material properties (Clarke et al, 2015;Vienneau-Hathaway et al, 2017). Counter to this trend, almost half the venom proteins in Nasonia wasps are single-copy genes with normal roles in wasp physiology that have been co-opted into the venom gland (Martinson et al, 2017).…”

Towards Spider Glue: Long-read scaffolding for extreme length and repetitious silk family genes AgSp1 and AgSp2 with insights into functional adaptation

“…5). Furthermore, GPG motifs of minor ampullate spidroin proteins are significantly correlated with extensibility (Vienneau-Hathaway et al, 2017). Not surprisingly, the stretches of poly-alanine that impart silk strength to MaSp silk (Gosline et al, 1999) are lacking in the much less strong aggregate glue.…”

Semi‐aquatic spider silks: transcripts, proteins, and silk fibres of the fishing spider, Dolomedes triton (Pisauridae)

“…These MiSp spacers are rich in threonine, serine, and valine, which is distinct from the amino acid composition of the MiSp repetitive motifs. MiSp spacers also are conserved in sequence and length across species (Chen et al, 2012;Vienneau-Hathaway et al, 2017). We searched our AmSp spidroins for MiSp-like repetitive motifs and spacers, and although we found a few AmSp sequences with threonine and serine rich motifs, none of the D. triton AmSp sequences contained all of the araneoid MiSp features (Fig.…”