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

Stellwagen, Sarah D.; Renberg, Rebecca L.

doi:10.1101/492025

Cited by 5 publications

(7 citation statements)

References 70 publications

(73 reference statements)

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“…This curation was realized using a previously reported method combining hybrid sequencing and the SMoC algorithm (Spidroin Motif Collection) 48,49 . Since it is impossible to sequence the heavily repetitive domains in spidroin using a short read sequencer 53,54 , the hybrid approach with short and long read sequencing is essential. Contig extension with an extremely large k-mer based on the short and long reads provided almost all spidroins.…”

Section: Discussionmentioning

confidence: 99%

“…Sequence conservation dismisses the possibility of convergent evolution and strongly supports the existence of a common ancestor harbouring cribellate orb webs like uloborid spiders. AgSp has been reported not only from the orb-weaving spiders, but also from Theridiidae spiders that build a cob web 54 , 58 – 61 . Hence, our molecular analyses suggest the possibility that complex ANE and UR grades appear as a result of the simple evolutionary history of CrSp or orb web losses or AgSp gains.…”

Section: Discussionmentioning

confidence: 99%

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Spidroin profiling of cribellate spiders provides insight into the evolution of spider prey capture strategies

Kono

Nakamura

Mori

et al. 2020

Sci Rep

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Orb-weaving spiders have two main methods of prey capture: cribellate spiders use dry, sticky capture threads, and ecribellate spiders use viscid glue droplets. Predation behaviour is a major evolutionary driving force, and it is important on spider phylogeny whether the cribellate and ecribellate spiders each evolved the orb architecture independently or both strategies were derived from an ancient orb web. These hypotheses have been discussed based on behavioural and morphological characteristics, with little discussion on this subject from the perspective of molecular materials of orb web, since there is little information about cribellate spider-associated spidroin genes. Here, we present in detail a spidroin catalogue of six uloborid species of cribellate orb-weaving spiders, including cribellate and pseudoflagelliform spidroins, with transcriptome assembly complemented with long read sequencing, where silk composition is confirmed by proteomics. Comparative analysis across families (Araneidae and Uloboridae) shows that the gene architecture, repetitive domains, and amino acid frequencies of the orb web constituting silk proteins are similar among orb-weaving spiders regardless of the prey capture strategy. Notably, the fact that there is a difference only in the prey capture thread proteins strongly supports the monophyletic origin of the orb web.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Spidroin profiling of cribellate spiders provides insight into the evolution of spider prey capture strategies

Kono

Nakamura

Mori

et al. 2020

Sci Rep

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“…Genes with higher expression in Spiny Legs include protease inhibitors such as zonadhesins, as well as transferases and transporter proteins. We observed reduced expression in Spiny Legs of some genes with aggregate gland-specific expression in other spiders, including an N-acetylgalactosaminyltransferase (pp-GalNAc-T) [ 41 ] and a globin protein [ 40 ]. Other genes with lower expression in Spiny Legs include an aminotransferase, a semaphorin membrane protein, and a cathepsin endopeptidase.…”

Section: Resultsmentioning

confidence: 99%

“…Consistent with the loss of aggregate glands, Spiny Legs exhibited reduced expression of genes with aggregate gland-specific expression in other spiders, including a pp-GalNAc-T, a type of transferase that participates in O-glycosylation [ 54 ]. O-glycosylation contributes to the adhesive qualities of aggregate glue [ 55 ], and pp-GalNAc-T is highly expressed in the aggregate glands of the orb-weaver Argiope trifasciata [ 41 ]. The reduced expression of this gene in Spiny Legs accompanied by their loss of aggregate glands suggests that this gene could play a similar role in aggregate silk production in tetragnathids.…”

Section: Discussionmentioning

confidence: 99%

Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders

et al. 2021

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Background A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages. Results The cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae. Conclusions Our results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors.

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“…The extrapolated molecular weight ( M w ) was 1.2 MDa for flagelliform (FLAG), indicating a dimeric state in solution by comparison to the 570 kDa estimated from the amino acid sequence. 27 The new and more complete flagelliform protein’s gene sequences 28 suggest a molecular weight of 759.5 kDa for the monomeric units. Given the uncertainty on the extrapolated M w estimate, we believed that FLAG was dimeric in solution.…”

Section: Resultsmentioning

confidence: 99%

Structural Diversity of Native Major Ampullate, Minor Ampullate, Cylindriform, and Flagelliform Silk Proteins in Solution

et al. 2020

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The foundations of silk spinning, the structure, storage, and activation of silk proteins, remain highly debated. By combining solution small-angle neutron and X-ray scattering (SANS and SAXS) alongside circular dichroism (CD), we reveal a shape anisotropy of the four principal native spider silk feedstocks from Nephila edulis . We show that these proteins behave in solution like elongated semiflexible polymers with locally rigid sections. We demonstrated that minor ampullate and cylindriform proteins adopt a monomeric conformation, while major ampullate and flagelliform proteins have a preference for dimerization. From an evolutionary perspective, we propose that such dimerization arose to help the processing of disordered silk proteins. Collectively, our results provide insights into the molecular-scale processing of silk, uncovering a degree of evolutionary convergence in protein structures and chemistry that supports the macroscale micellar/pseudo liquid crystalline spinning mechanisms proposed by the community.

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

Cited by 5 publications

References 70 publications

Spidroin profiling of cribellate spiders provides insight into the evolution of spider prey capture strategies

Spidroin profiling of cribellate spiders provides insight into the evolution of spider prey capture strategies

Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders

Structural Diversity of Native Major Ampullate, Minor Ampullate, Cylindriform, and Flagelliform Silk Proteins in Solution

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