Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders

R Chaw,Cheryl Y Hayashi,Kirmanj Atrushi,Yonghui Zhao,Jie Wei,Ryan Allen,Nadia A Ayoub

doi:10.1186/1471-2148-14-31

R Chaw, Cheryl Y Hayashi + Show 5 more

Open Access

https://doi.org/10.1186/1471-2148-14-31

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Abstract

BackgroundSpider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution. An individual spider can produce an array of specialized silks, with the majority of constituent silk proteins encoded by members of the spidroin gene family. Spidroins are dominated by tandem repeats flanked by short, non-repetitive N- and C-terminal coding regions. The remarkable mechanical properties of spider silks have been largely attributed to the repeat sequences. However, the molecular evolutionary processes acting on spidroin terminal and repetitive regions remain unclear due to a paucity of complete gene sequences and sampling of genetic variation among individuals. To better understand spider silk evolution, we characterize a complete aciniform spidroin gene from an Argiope orb-weaving spider and survey aciniform gene fragments from congeneric individuals.ResultsWe present the complete aciniform spidroin (AcSp1) gene from the silver garden spider Argiope argentata (Aar_AcSp1), and document multiple AcSp1 loci in individual genomes of A. argentata and the congeneric A. trifasciata and A. aurantia. We find that Aar_AcSp1 repeats have >98% pairwise nucleotide identity. By comparing AcSp1 repeat amino acid sequences between Argiope species and with other genera, we identify regions of conservation over vast amounts of evolutionary time. Through a PCR survey of individual A. argentata, A. trifasciata, and A. aurantia genomes, we ascertain that AcSp1 repeats show limited variation between species whereas terminal regions are more divergent. We also find that average dN/dS across codons in the N-terminal, repetitive, and C-terminal encoding regions indicate purifying selection that is strongest in the N-terminal region.ConclusionsUsing the complete A. argentata AcSp1 gene and spidroin genetic variation between individuals, this study clarifies some of the molecular evolutionary processes underlying the spectacular mechanical attributes of aciniform silk. It is likely that intragenic concerted evolution and functional constraints on A. argentata AcSp1 repeats result in extreme repeat homogeneity. The maintenance of multiple AcSp1 encoding loci in Argiope genomes supports the hypothesis that Argiope spiders require rapid and efficient protein production to support their prolific use of aciniform silk for prey-wrapping and web-decorating. In addition, multiple gene copies may represent the early stages of spidroin diversification.

Highlights

Spider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution
Repeat aa sequence corresponds to secondary structures that are partly responsible for silk mechanical properties (e.g. [13,14,15]), and conservation of the N- and C-terminal regions [12] and their presence in spun silk fibers suggests an important role in spider silk biology [16,17,18]
Argiope argentata AcSp1 complete sequence and phylogenetic placement Despite obtaining 59 AcSp1 complementary deoxyribonucleic acid (cDNA) clones, including one that was >8 kb [1], a complete Argiope AcSp1 remained elusive until the present study

Summary

Introduction

Spider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution. An individual spider can produce an array of specialized silks, with the majority of constituent silk proteins encoded by members of the spidroin gene family. Spidroins are dominated by tandem repeats flanked by short, non-repetitive N- and C-terminal coding regions. The remarkable mechanical properties of spider silks have been largely attributed to the repeat sequences. The molecular evolutionary processes acting on spidroin terminal and repetitive regions remain unclear due to a paucity of complete gene sequences and sampling of genetic variation among individuals. An individual spider can produce and use different silk types singly or in combination for specific tasks, with each silk type having mechanical properties well-suited to its function. Spidroins are typically very large (>200 kDa), and are dominated by a series of iterated repeats flanked by short amino (N)- and carboxy (C)terminal regions [9,10]. Repeat aa sequence corresponds to secondary structures that are partly responsible for silk mechanical properties (e.g. [13,14,15]), and conservation of the N- and C-terminal regions [12] and their presence in spun silk fibers suggests an important role in spider silk biology [16,17,18]

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