Spider genomes provide insight into composition and evolution of venom and silk

Nature Communications

Volumn 5, Issue , 2014, Pages

  Sanggaard, Kristian W ^a   Bechsgaard, Jesper S ^a   Fang, Xiaodong ^b,c   Duan, Jinjie ^a   Dyrlund, Thomas F ^a   Gupta, Vikas ^a   Jiang, Xuanting ^b   Cheng, Ling ^b   Fan, Dingding ^b   Feng, Yue ^b   Han, Lijuan ^b   Huang, Zhiyong ^b   Wu, Zongze ^b   Liao, Li ^b   Settepani, Virginia ^a   Thøgersen, Ida B ^a   Vanthournout, Bram ^a   Wang, Tobias ^a   Zhu, Yabing ^b   Funch, Peter ^a   Enghild, Jan J ^a   Schauser, Leif ^d   Andersen, Stig U ^a   Villesen, Palle ^a   Schierup, Mikkel H ^a   Bilde, Trine ^a   Wang, Jun ^b,c,e   more..

^a AARHUS UNIVERSITY   (Denmark)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d CLC Bio   (Denmark)

^e KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

(S) 2 HYDROXY ACID OXIDASE; ARGININE; ENDOTHELIN; PROTEOME; SERINE PROTEINASE; SILK; SPIDER VENOM; STRUCTURAL PROTEIN; TRANSCRIPTOME; INSECT PROTEIN; PEPTIDE HYDROLASE;

ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; MAMMAL; PREDATOR; PREY CAPTURE; PROTEIN; SPIDER; TAXONOMY; TICK; VENOM;

ACARI; AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EXON; FEMALE; GENE CONVERSION; GENOME; GENOME SIZE; GENOMICS; HETEROZYGOSITY; INTRON; ISOCHORE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR EVOLUTION; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYPHYLY; PROTEIN ANALYSIS; PROTEOMICS; SEGMENTAL DUPLICATION; SINGLE NUCLEOTIDE POLYMORPHISM; SPIDER; TANDEM MASS SPECTROMETRY; TARANTULA; TRANSCRIPTOMICS; ANIMAL; DNA SEQUENCE; GENETICS;

ACARI; ARANEAE; IXODIDA; MAMMALIA;

ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENOME; INSECT PROTEINS; PEPTIDE HYDROLASES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SILK; SPIDER VENOMS; SPIDERS;

EID: 84902348404     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4765     Document Type: Article

References (70)

1. Platnick, N. I. The American Museum of Natural History. Available at http://www.research.amnh.org/iz/spiders/catalog/COUNTS.html (2012).
2. Dimitrov, D. et al. Tangled in a sparse spider web: single origin of orb weavers and their spinning work unravelled by denser taxonomic sampling. Proc. Biol. Sci. 279, 1341-1350 (2012).
3. Langellotto, G. A. & Denno, R. F. Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139, 1-10 (2004).
4. Schmitz, O. J., Beckerman, A. P. & Obrien, K. M. Behaviorally mediated trophic cascades: Effects of predation risk on food web interactions. Ecology 78, 1388-1399 (1997).
5. Terborgh, J. et al. Ecological meltdown in predator-free forest fragments. Science 294, 1923-1926 (2001).
6. Nyffeler, M. & Knörnschild, M. Bat predation by spiders. PLoS ONE 8, e58120 (2013).
7. Lee, S. Y. & MacKinnon, R. A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom. Nature 430, 232-235 (2004).
8. Rash, L. D. & Hodgson, W. C. Pharmacology and biochemistry of spider venoms. Toxicon 40, 225-254 (2002).
9. Escoubas, P., Diochot, S. & Corzo, G. Structure and pharmacology of spider venom neurotoxins. Biochimie 82, 893-907 (2000).
10. King, G. F. & Hardy, M. C. Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Annu. Rev. Entomol. 58, 475-496 (2013).
11. Elices, M., Plaza, G. R., Perez-Rigueiro, J. & Guinea, G. V. The hidden link between supercontraction and mechanical behavior of spider silks. J. Mech. Behav. Biomed. Mater. 4, 658-669 (2011).
12. Rising, A. et al. Spider silk proteins-mechanical property and gene sequence. Zoolog. Sci. 22, 273-281 (2005).
13. Altman, G. H. et al. Silk-based biomaterials. Biomaterials 24, 401-416 (2003).
14. Pepato, A. R., da Rocha, C. E. F. & Dunlop, J. A. Phylogenetic position of the acariform mites: sensitivity to homology assessment under total evidence. BMC Evol. Biol. 10, 235 (2010).
15. Khadjeh, S. et al. Divergent role of the Hox gene Antennapedia in spiders is responsible for the convergent evolution of abdominal limb repression. Proc. Natl Acad. Sci. USA 109, 4921-4926 (2012).
16. Pechmann, M. et al. Novel function of distal-less as a gap gene during spider segmentation. PLoS Genet. 7, e1002342 (2011).
17. Hilbrant, M., Damen, W. G. M. & McGregor, A. P. Evolutionary crossroads in developmental biology: the spider Parasteatoda tepidariorum. Development 139, 2655-2662 (2012).
18. Janssen, R., Damen, W. G. M. & Budd, G. E. Expression of pair rule gene orthologs in the blastoderm of a myriapod: evidence for pair rule-like mechanisms? BMC Dev. Biol. 12, 15 (2012).
19. Mattila, T. M., Bechsgaard, J. S., Hansen, T. T., Schierup, M. H. & Bilde, T. Orthologous genes identified by transcriptome sequencing in the spider genus Stegodyphus. BMC Genomics 13, 70 (2012).
20. Guindon, S. et al. New Algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).
21. Regier, J. C. et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079-1083 (2010).
22. Jeyaprakash, A. & Hoy, M. A. First divergence time estimate of spiders, scorpions, mites and ticks (subphylum: Chelicerata) inferred from mitochondrial phylogeny. Exp. Appl. Acarol. 47, 1-18 (2009).
23. De Bie, T., Cristianini, N., Demuth, J. P. & Hahn, M. W. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269-1271 (2006).
24. Li, H. et al. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 34, D572-D580 (2006).
25. Foradori, M. J., Tillinghast, E. K., Smith, J. S., Townley, M. A. & Mooney, R. E. Astacin family metallopeptidases and serine peptidase inhibitors in spider digestive fluid. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 143, 257-268 (2006).
26. Da Silveira, R. B. et al. Identification, cloning, expression and functional characterization of an astacin-like metalloprotease toxin from Loxosceles intermedia (brown spider) venom. Biochem. J. 406, 355-363 (2007).
27. Liang, S. Proteome and peptidome profiling of spider venoms. Expert Rev. Proteomics 5, 731-746 (2008).
28. Tang, X. et al. Molecular diversification of peptide toxins from the tarantula haplopelma hainanum (ornithoctonus hainana) venom based on transcriptomic, peptidomic, and genomic analyses. J. Proteome. Res. 9, 2550-2564 (2010).
29. Milne, T. J., Abbenante, G., Tyndall, J. D., Halliday, J. & Lewis, R. J. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J. Biol. Chem. 278, 31105-31110 (2003).
30. Sunagar, K., Johnson, W. E., O'Brien, S. J., Vasconcelos, V. & Antunes, A. Evolution of CRISPs associated with toxicoferan-reptilian venom and mammalian reproduction. Mol. Biol. Evol. 29, 1807-1822 (2012).
31. Clement, H. et al. Identification, cDNA cloning and heterologous expression of a hyaluronidase from the tarantula Brachypelma vagans venom. Toxicon 60, 1223-1227 (2012).
32. Savelniemann, A. Tarantula (Eurypelma californicum) venom, a multicomponent system. Biol. Chem. Hoope Seyler 370, 485-498 (1989).
33. Schanbac, F. L. et al. Composition and properties of tarantula Dugesiella hentzi (Girard) venom. Toxicon 11, 21-29 (1973).
34. Kuhn-Nentwig, L., Stocklin, R. & Nentwig, W. Venom composition and strategies in spiders: is everything possible? Adv. Insect Physiol. 40, 1-86 (2011).
35. Fry, B. G. et al. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics. Hum. Genet. 10, 483-511 (2009).
36. Kini, R. M. Excitement ahead: structure, function and mechanism of snake venom phospholipase A(2) enzymes. Toxicon 42, 827-840 (2003).
37. Vassilevski, A. A., Kozlov, S. A. & Grishin, E. V. Molecular diversity of spider venom. Biochemistry (Mosc) 74, 1505-1534 (2009).
38. Saez, N. J. et al. Spider venom peptides as therapeutics. Toxins 2, 2851-2871 (2010).
39. Cao, Z. et al. The genome of Mesobuthus martensii reveals a unique adaptation model of arthropods. Nat. Commun. 4, 2602 (2013).
40. Guerette, P. A., Ginzinger, D. G., Weber, B. H. F. & Gosline, J. M. Silk properties determined by gland-specific expression of a spider fibroin gene family. Science 272, 112-115 (1996).
41. Palmer, J. M. The silk and silk production system of the funnel-web mygalomorph spider Euagrus (Araneae, Dipluridae). J. Morphol. 186, 195-207 (1985).
42. Vollrath, F. Spider webs and silks. Sci. Am. 266, 70-76 (1992).
43. Platnick, N. I., Coddington, J. A., Forster, R. R. & Griswold, C. E. Spinneret morphology and the phylogeny of haplogyne spiders (Araneae, Araneomorphae). Am. Museum Novit. 3016, 1-73 (1991).
44. Askarieh, G. et al. Self-assembly of spider silk proteins is controlled by a pH-sensitive relay. Nature 465, 236-238 (2010).
45. Hagn, F. et al. A conserved spider silk domain acts as a molecular switch that controls fibre assembly. Nature 465, 239-242 (2010).
46. Gatesy, J., Hayashi, C., Motriuk, D., Woods, J. & Lewis, R. Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 291, 2603-2605 (2001).
47. Vollrath, F. Biology of spider silk. Int. J. Biol. Macromol. 24, 81-88 (1999).
48. Colgin, M. A. & Lewis, R. V. Spider minor ampullate silk proteins contain new repetitive sequences and highly conserved non-silk-like 'spacer regions'. Protein Sci. 7, 667-672 (1998).
49. Lane, K. L., Hayashi, C. H., Whitworth, G. B. & Ayoub, N. A. Complex gene expression in the dragline silk producing glands of the Western black widow (Latrodectus hesperus). BMC Genomics 14, 846 (2013).
50. Craig, C. L. Evolution of arthropod silks. Annu. Rev. Entomol. 42, 231-267 (1997).
51. Candelas, G. C., Ortiz, A. & Molina, C. The cylindrical or tubiliform glands of Nephila clavipes. J. Exp. Zool. 237, 281-285 (1986).
52. Vasanthavada, K. et al. Aciniform spidroin, a constituent of egg case sacs and wrapping silk fibers from the black widow spider Latrodectus hesperus. J. Biol. Chem. 282, 35088-35097 (2007).
53. Ayoub, N. A., Garb, J. E., Kuelbs, A. & Hayashi, C. Y. Ancient properties of spider silks revealed by the complete gene sequence of the prey-wrapping silk protein (AcSp1). Mol. Biol. Evol. 30, 589-601 (2013).
54. Garb, J. E., Ayoub, N. A. & Hayashi, C. Y. Untangling spider silk evolution with spidroin terminal domains. BMC Evol. Biol. 10, 243 (2010).
55. Starrett, J., Garb, J. E., Kuelbs, A., Azubuike, U. O. & Hayashi, C. Y. Early events in the evolution of spider silk genes. PLoS ONE 7, e38084 (2012).
56. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
57. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-U174 (2010).
58. Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859-1875 (2005).
59. Stanke, M., Steinkamp, R., Waack, S. & Morgenstern, B. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32, W309-W312 (2004).
60. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580 (1999).
61. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
62. De Pristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
63. Yang, Z. H. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
64. Loytynoja, A. & Goldman, N. An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl Acad. Sci. USA 102, 10557-10562 (2005).
65. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552 (2000).
66. Talavera, G. & Castresana, J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564-577 (2007).
67. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. & Mann, M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860 (2006).
68. Vizcaino, J. A. et al. The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res. 41, D1063-D1069 (2013).
69. Perkins, D. N., Pappin, D. J. C., Creasy, D. M. & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).
70. Dyrlund, T. F., Poulsen, E. T., Scavenius, C., Sanggaard, K. W. & Enghild, J. J. MS Data Miner: a web-based software tool to analyze, compare, and share mass spectrometry protein identifications. Proteomics 12, 2792-2796 (2012).