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      Bioprospecting Finds the Toughest Biological Material: Extraordinary Silk from a Giant Riverine Orb Spider

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      PLoS ONE
      Public Library of Science

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          Abstract

          Background

          Combining high strength and elasticity, spider silks are exceptionally tough, i.e., able to absorb massive kinetic energy before breaking. Spider silk is therefore a model polymer for development of high performance biomimetic fibers. There are over 41.000 described species of spiders, most spinning multiple types of silk. Thus we have available some 200.000+ unique silks that may cover an amazing breadth of material properties. To date, however, silks from only a few tens of species have been characterized, most chosen haphazardly as model organisms ( Nephila) or simply from researchers' backyards. Are we limited to ‘blindly fishing’ in efforts to discover extraordinary silks? Or, could scientists use ecology to predict which species are likely to spin silks exhibiting exceptional performance properties?

          Methodology

          We examined the biomechanical properties of silk produced by the remarkable Malagasy ‘Darwin's bark spider’ ( Caerostris darwini), which we predicted would produce exceptional silk based upon its amazing web. The spider constructs its giant orb web (up to 2.8 m 2) suspended above streams, rivers, and lakes. It attaches the web to substrates on each riverbank by anchor threads as long as 25 meters. Dragline silk from both Caerostris webs and forcibly pulled silk, exhibits an extraordinary combination of high tensile strength and elasticity previously unknown for spider silk. The toughness of forcibly silked fibers averages 350 MJ/m 3, with some samples reaching 520 MJ/m 3. Thus, C. darwini silk is more than twice tougher than any previously described silk, and over 10 times better than Kevlar®. Caerostris capture spiral silk is similarly exceptionally tough.

          Conclusions

          Caerostris darwini produces the toughest known biomaterial. We hypothesize that this extraordinary toughness coevolved with the unusual ecology and web architecture of these spiders, decreasing the likelihood of bridgelines breaking and collapsing the web into the river. This hypothesis predicts that rapid change in material properties of silk co-occurred with ecological shifts within the genus, and can thus be tested by combining material science, behavioral observations, and phylogenetics. Our findings highlight the potential benefits of natural history–informed bioprospecting to discover silks, as well as other materials, with novel and exceptional properties to serve as models in biomimicry.

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          Most cited references34

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          Reconstructing web evolution and spider diversification in the molecular era.

          The evolutionary diversification of spiders is attributed to spectacular innovations in silk. Spiders are unique in synthesizing many different kinds of silk, and using silk for a variety of ecological functions throughout their lives, particularly to make prey-catching webs. Here, we construct a broad higher-level phylogeny of spiders combining molecular data with traditional morphological and behavioral characters. We use this phylogeny to test the hypothesis that the spider orb web evolved only once. We then examine spider diversification in relation to different web architectures and silk use. We find strong support for a single origin of orb webs, implying a major shift in the spinning of capture silk and repeated loss or transformation of orb webs. We show that abandonment of costly cribellate capture silk correlates with the 2 major diversification events in spiders (1). Replacement of cribellate silk by aqueous silk glue may explain the greater diversity of modern orb-weaving spiders (Araneoidea) compared with cribellate orb-weaving spiders (Deinopoidea) (2). Within the "RTA clade," which is the sister group to orb-weaving spiders and contains half of all spider diversity, >90% of species richness is associated with repeated loss of cribellate silk and abandonment of prey capture webs. Accompanying cribellum loss in both groups is a release from substrate-constrained webs, whether by aerially suspended webs, or by abandoning webs altogether. These behavioral shifts in silk and web production by spiders thus likely played a key role in the dramatic evolutionary success and ecological dominance of spiders as predators of insects.
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            The structure and properties of spider silk

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              Greatly increased toughness of infiltrated spider silk.

              In nature, tiny amounts of inorganic impurities, such as metals, are incorporated in the protein structures of some biomaterials and lead to unusual mechanical properties of those materials. A desire to produce these biomimicking new materials has stimulated materials scientists, and diverse approaches have been attempted. In contrast, research to improve the mechanical properties of biomaterials themselves by direct metal incorporation into inner protein structures has rarely been tried because of the difficulty of developing a method that can infiltrate metals into biomaterials, resulting in a metal-incorporated protein matrix. We demonstrated that metals can be intentionally infiltrated into inner protein structures of biomaterials through multiple pulsed vapor-phase infiltration performed with equipment conventionally used for atomic layer deposition (ALD). We infiltrated zinc (Zn), titanium (Ti), or aluminum (Al), combined with water from corresponding ALD precursors, into spider dragline silks and observed greatly improved toughness of the resulting silks. The presence of the infiltrated metals such as Al or Ti was verified by energy-dispersive x-ray (EDX) and nuclear magnetic resonance spectra measured inside the treated silks. This result of enhanced toughness of spider silk could potentially serve as a model for a more general approach to enhance the strength and toughness of other biomaterials.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                16 September 2010
                : 5
                : 9
                : e11234
                Affiliations
                [1 ]Department of Biology, Faculty of Natural Sciences, University of Puerto Rico, San Juan, Puerto Rico, United States of America
                [2 ]Institute of Biology, Scientific Research Centre, Slovenian Academy of Sciences and Arts, Ljubljana, Slovenia
                [3 ]Department of Biology and Integrated Bioscience Program, University of Akron, Akron, Ohio, United States of America
                Institute of Evolutionary Biology (CSIC-UPF), Spain
                Author notes

                Conceived and designed the experiments: IA MK TAB. Performed the experiments: IA MK. Analyzed the data: IA TAB. Contributed reagents/materials/analysis tools: IA TAB. Wrote the paper: IA MK TAB.

                Article
                10-PONE-RA-16162R1
                10.1371/journal.pone.0011234
                2939878
                20856804
                4ee057ec-e93a-4f7d-883a-8df874c3e614
                Agnarsson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 9 February 2010
                : 24 May 2010
                Page count
                Pages: 8
                Categories
                Research Article
                Ecology
                Evolutionary Biology
                Physics/Interdisciplinary Physics

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