Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Abstract
In nature, numerous mechanisms have evolved by which organisms fabricate biological structures with an impressive array of physical characteristics. Some examples of metazoan biological materials include the highly elastic byssal threads by which bivalves attach themselves to rocks, biomineralized structures that form the skeletons of various animals, and spider silks that are renowned for their exceptional strength and elasticity. The remarkable properties of silks, which are perhaps the best studied biological materials, are the result of the highly repetitive, modular, and biased amino acid composition of the proteins that compose them. Interestingly, similar levels of modularity/repetitiveness and similar bias in amino acid compositions have been reported in proteins that are components of structural materials in other organisms, however the exact nature and extent of this similarity, and its functional and evolutionary relevance, is unknown. Here, we investigate this similarity and use sequence features common to silks and other known structural proteins to develop a bioinformatics-based method to identify similar proteins from large-scale transcriptome and whole-genome datasets. We show that a large number of proteins identified using this method have roles in biological material formation throughout the animal kingdom. Despite the similarity in sequence characteristics, most of the silk-like structural proteins (SLSPs) identified in this study appear to have evolved independently and are restricted to a particular animal lineage. Although the exact function of many of these SLSPs is unknown, the apparent independent evolution of proteins with similar sequence characteristics in divergent lineages suggests that these features are important for the assembly of biological materials. The identification of these characteristics enable the generation of testable hypotheses regarding the mechanisms by which these proteins assemble and direct the construction of biological materials with diverse morphologies. The SilkSlider predictor software developed here is available at https://github.com/wwood/SilkSlider.
Fig 1. A. ROC curves displaying the performance of different predictors. B. Categorisation of silk-like proteins identified in the B. mori dataset. The pie chart shows division of the 178 predicted silk-like proteins into the categories indicated in the legend. ‘Known’ and ‘likely biological material’ categories refer to proteins that are known or likely to have a role in biological material formation. All 12 known B. mori silk-like sequences found in the literature (box) were identified by the predictor.
Fig 2. Results of survey of silk-like proteins in the Metazoa.Dendrogram on the left indicates currently accepted phylogenetic relationships of investigated taxa. Columns on the right indicate the total number of sequences evaluated by the predictor, the total number of predicted silk-like proteins, and the categorisation of identified silk-like proteins, for each taxon.
Fig 3. Spatial localization of genes encoding predicted silk-like proteins.Blue staining corresponds to cells expressing the gene. A. Dorsal view of juvenile H. asinina, removed from shell. Has-CL10Con2 expression is restricted to the mantle (arrows). B. Expanded view of boxed area in ‘A’. Has-CL10Con2 expression is in cells in the nacreous zone of the mantle. C. Dorsal view of juvenile H. asinina, removed from shell. Has-GRBP transcripts are localized to the mantle (arrows). D. Expanded view of boxed area in ‘C’. Has-GRBP expression is restricted to cells in the nacreous zone of the mantle, and is higher at the boundary between prismatic and nacreous zones. E. Late gastrula-stage (40 hours post fertilisation) S. purpuratus embryo. The sea urchin SM30E gene is expressed in PMCs (arrows). F. Late gastrula-stage (40 hours post fertilisation) S. purpuratus embryo. The sea urchin Cara7LA gene is expressed in PMCs (arrows). p, prismatic zone; n, nacreous zone.
Addadi,
Mollusk shell formation: a source of new concepts for understanding biomineralization processes.
2007, Pubmed
Addadi,
Mollusk shell formation: a source of new concepts for understanding biomineralization processes.
2007,
Pubmed
Aspöck,
Caenorhabditis elegans has scores of hedgehog-related genes: sequence and expression analysis.
1999,
Pubmed
Ayoub,
Blueprint for a high-performance biomaterial: full-length spider dragline silk genes.
2010,
Pubmed
Beckmann,
A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge.
2015,
Pubmed
Bini,
Mapping domain structures in silks from insects and spiders related to protein assembly.
2004,
Pubmed
Bonnal,
Biogem: an effective tool-based approach for scaling up open source software development in bioinformatics.
2012,
Pubmed
Buckley,
Extraordinary diversity among members of the large gene family, 185/333, from the purple sea urchin, Strongylocentrotus purpuratus.
2007,
Pubmed
,
Echinobase
Camacho,
BLAST+: architecture and applications.
2010,
Pubmed
Cameron,
Biomineral ultrastructure, elemental constitution and genomic analysis of biomineralization-related proteins in hemichordates.
2012,
Pubmed
Cao,
Sequence of abductin, the molluscan 'rubber' protein.
1998,
Pubmed
Chang,
Fibroin-like substance is a major component of the outer layer of fertilization envelope via which carp egg adheres to the substratum.
2003,
Pubmed
Chen,
A fast Peptide Match service for UniProt Knowledgebase.
2014,
Pubmed
Cheng,
How sequence determines elasticity of disordered proteins.
2011,
Pubmed
Coyne,
Extensible collagen in mussel byssus: a natural block copolymer.
1997,
Pubmed
Craig,
Comparative architecture of silks, fibrous proteins and their encoding genes in insects and spiders.
2003,
Pubmed
David,
Evolution of complex structures: minicollagens shape the cnidarian nematocyst.
2009,
Pubmed
Deans,
Mammalian Otolin: a multimeric glycoprotein specific to the inner ear that interacts with otoconial matrix protein Otoconin-90 and Cerebellin-1.
2011,
Pubmed
Degens,
Molecular mechanisms on carbonate, phosphate, and silica deposition in the living cell.
1976,
Pubmed
Emanuelsson,
Locating proteins in the cell using TargetP, SignalP and related tools.
2007,
Pubmed
Evans,
Aragonite-associated biomineralization proteins are disordered and contain interactive motifs.
2013,
Pubmed
Fang,
cDNA sequence of a virus-inducible, glycine-rich protein gene from rice.
1991,
Pubmed
Fu,
CD-HIT: accelerated for clustering the next-generation sequencing data.
2013,
Pubmed
Gage,
Internal structure of the silk fibroin gene of Bombyx mori. I The fibroin gene consists of a homogeneous alternating array of repetitious crystalline and amorphous coding sequences.
1980,
Pubmed
Goto,
BioRuby: bioinformatics software for the Ruby programming language.
2011,
Pubmed
Harrington,
Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads.
2008,
Pubmed
Hayashi,
Molecular architecture and evolution of a modular spider silk protein gene.
2000,
Pubmed
Hayashi,
Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins.
1999,
Pubmed
Hibner,
Sequence identity in an early chorion multigene family is the result of localized gene conversion.
1991,
Pubmed
Hinman,
Retinoic acid perturbs Otx gene expression in the ascidian pharynx.
2001,
Pubmed
Hohl,
Characterization of human loricrin. Structure and function of a new class of epidermal cell envelope proteins.
1991,
Pubmed
Hronska,
NMR characterization of native liquid spider dragline silk from Nephila edulis.
2005,
Pubmed
Huang,
CAP3: A DNA sequence assembly program.
1999,
Pubmed
Huang,
Biomineralization regulation by nano-sized features in silk fibroin proteins: synthesis of water-dispersible nano-hydroxyapatite.
2015,
Pubmed
Hwang,
Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra.
2010,
Pubmed
Iatrou,
Developmental classes and homologous families of chorion genes in Bombyx mori.
1982,
Pubmed
Iconomidou,
Amyloid fibril formation propensity is inherent into the hexapeptide tandemly repeating sequence of the central domain of silkmoth chorion proteins of the A-family.
2007,
Pubmed
Innamorati,
An intracellular role for the C1q-globular domain.
2006,
Pubmed
Ioannidou,
CutProtFam-Pred: detection and classification of putative structural cuticular proteins from sequence alone, based on profile hidden Markov models.
2015,
Pubmed
Jackson,
Parallel evolution of nacre building gene sets in molluscs.
2010,
Pubmed
,
Echinobase
Jackson,
Dynamic expression of ancient and novel molluscan shell genes during ecological transitions.
2007,
Pubmed
Jackson,
A rapidly evolving secretome builds and patterns a sea shell.
2006,
Pubmed
Kalmar,
Structural disorder in proteins brings order to crystal growth in biomineralization.
2012,
Pubmed
Keller,
Glycine-rich cell wall proteins in bean: gene structure and association of the protein with the vascular system.
1989,
Pubmed
Killian,
Molecular aspects of biomineralization of the echinoderm endoskeleton.
2009,
Pubmed
,
Echinobase
Killian,
SpSM30 gene family expression patterns in embryonic and adult biomineralized tissues of the sea urchin, Strongylocentrotus purpuratus.
2010,
Pubmed
,
Echinobase
Kunz,
Sequences of two genomic fragments containing an identical coding region for a putative egg-shell precursor protein of Schistosoma mansoni.
1987,
Pubmed
Liu,
Silkmapin of Hyriopsis cumingii, a novel silk-like shell matrix protein involved in nacre formation.
2015,
Pubmed
Livingston,
A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus.
2007,
Pubmed
,
Echinobase
Lucas,
A molecular, morphometric and mechanical comparison of the structural elements of byssus from Mytilus edulis and Mytilus galloprovincialis.
2003,
Pubmed
Mann,
Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix.
2011,
Pubmed
,
Echinobase
Mann,
In-depth, high-accuracy proteomics of sea urchin tooth organic matrix.
2009,
Pubmed
,
Echinobase
Mann,
The sea urchin (Strongylocentrotus purpuratus) test and spine proteomes.
2009,
Pubmed
,
Echinobase
Mann,
Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis.
2014,
Pubmed
Marelli,
Silk fibroin derived polypeptide-induced biomineralization of collagen.
2012,
Pubmed
Marie,
Proteomic analysis of the organic matrix of the abalone Haliotis asinina calcified shell.
2011,
Pubmed
McDougall,
Ultrastructure of the mantle of the gastropod Haliotis asinina and mechanisms of shell regionalization.
2011,
Pubmed
McDougall,
Rapid evolution of pearl oyster shell matrix proteins with repetitive, low-complexity domains.
2013,
Pubmed
Mita,
Highly repetitive structure and its organization of the silk fibroin gene.
1994,
Pubmed
Miyamoto,
A carbonic anhydrase from the nacreous layer in oyster pearls.
1996,
Pubmed
Nudelman,
Forming nacreous layer of the shells of the bivalves Atrina rigida and Pinctada margaritifera: an environmental- and cryo-scanning electron microscopy study.
2008,
Pubmed
Pereira-Mouriès,
Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima.
2002,
Pubmed
Petersen,
SignalP 4.0: discriminating signal peptides from transmembrane regions.
2011,
Pubmed
Qin,
Tough tendons. Mussel byssus has collagen with silk-like domains.
1998,
Pubmed
Rafiq,
Genome-wide analysis of the skeletogenic gene regulatory network of sea urchins.
2014,
Pubmed
,
Echinobase
Ransick,
Detection of mRNA by in situ hybridization and RT-PCR.
2005,
Pubmed
,
Echinobase
Robson,
Characterization of lamprin, an unusual matrix protein from lamprey cartilage. Implications for evolution, structure, and assembly of elastin and other fibrillar proteins.
1993,
Pubmed
Rose,
Protein constituents of the eggshell: eggshell-specific matrix proteins.
2009,
Pubmed
Ruangsittichai,
Opisthorchis viverrini: identification of a glycine-tyrosine rich eggshell protein and its potential as a diagnostic tool for human opisthorchiasis.
2007,
Pubmed
Scheffel,
Nanopatterned protein microrings from a diatom that direct silica morphogenesis.
2011,
Pubmed
Shen,
Molecular cloning and characterization of lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens.
1998,
Pubmed
Sing,
ROCR: visualizing classifier performance in R.
2005,
Pubmed
Srivastava,
The Trichoplax genome and the nature of placozoans.
2008,
Pubmed
Sudo,
Structures of mollusc shell framework proteins.
1997,
Pubmed
Sutherland,
Insect silk: one name, many materials.
2010,
Pubmed
Takahashi,
A novel silk-like shell matrix gene is expressed in the mantle edge of the Pacific oyster prior to shell regeneration.
2012,
Pubmed
Vincent,
Design and mechanical properties of insect cuticle.
2008,
Pubmed
Walsh,
ESpritz: accurate and fast prediction of protein disorder.
2012,
Pubmed
Wilt,
SM30 protein function during sea urchin larval spicule formation.
2014,
Pubmed
,
Echinobase
Xu,
Structure of a protein superfiber: spider dragline silk.
1990,
Pubmed
Yano,
Shematrin: a family of glycine-rich structural proteins in the shell of the pearl oyster Pinctada fucata.
2006,
Pubmed
Zhang,
A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata.
2006,
Pubmed
Zhao,
Cement proteins of the tube-building polychaete Phragmatopoma californica.
2006,
Pubmed
Zhou,
Fine organization of Bombyx mori fibroin heavy chain gene.
2000,
Pubmed