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MBE Advance Access published online on July 7, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh204
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted July 5, 2004

Original Articles

Molecular and Mechanical Characterization of Aciniform Silk: Uniformity of Iterated Sequence Modules in a Novel Member of the Spider Silk Fibroin Gene Family

Cheryl Y. Hayashi 1*, Todd A. Blackledge 1, Randolph V. Lewis 2

1 Department of Biology, University of California, Riverside, CA 92521
2 Department of Molecular Biology, University of Wyoming, Laramie, WY 82071

* To whom correspondence should be addressed. E-mail: cheryl.hayashi{at}ucr.edu.


  Abstract

Araneoid spiders use specialized abdominal glands to produce up to seven different protein based silks/glues that have diverse physical properties. The fibroin sequences that encode aciniform fibers (wrapping silk) and the mechanical properties of these fibers have not been characterized previously. In order to gain a better understanding of the molecular radiation of spider silk fibroin genes, cDNA libraries derived from aciniform glands of the banded garden spider, Argiope trifasciata, were constructed, and unique silk transcripts were sequenced. There was evidence for a single silk fibroin gene that was expressed in the aciniform glands, and the inferred amino acid composition of the novel fibroin closely matched the amino acid contents of these glands. The inferred protein, aciniform spidroin 1 (AcSp1), is composed of highly homogenized repeats that are 200 amino acids in length. The long stretches of poly-alanine and glycine-alanine subrepeats, that are thought to account for the crystalline regions of minor ampullate and major ampullate fibers, are very poorly represented in AcSp1. The AcSp1 repeat unit is iterated minimally fourteen times and does not display substantial sequence similarity to any previously described genes or proteins. Database searches, however, showed that the non-repetitive carboxy-terminus contains stretches of matches to known spider fibroin sequences, suggesting that the AcSp1 gene is a highly divergent member of the spider silk gene family. In phylogenetic analyses of carboxy-terminal sequences from araneid spiders, the aciniform sequence did not group strongly with clusters of fibroins from the flagelliform, minor ampullate, or major ampullate silk glands. Comparisons of stress/strain curves for major ampullate, minor ampullate, and aciniform silks from Argiope trifasciata showed significant differences in ultimate strength, extensibility, and toughness. Remarkably, the toughness of aciniform silk was 50% greater than the highest values typically recorded for major ampullate silk. These differences in performance, in combination with the radical divergence at the sequence level among fibroin paralogues, suggest a possible linkage between silk fibroin sequences and performance that should be explored in future structural/functional studies of aciniform silk.

Keywords: aciniform silk; Argiope trifasciata; cDNA; fibroin; gene family; spider.
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