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Journal of Chemical Ecology

, Volume 46, Issue 1, pp 48–62 | Cite as

Novel Amino Acid Assembly in the Silk Tubes of Arid-Adapted Segestriid Spiders

  • Erminia ContiEmail author
  • Sandro Dattilo
  • Andrea Scamporrino
  • Giovanni Costa
  • Filippo Samperi
Article

Abstract

We investigated in different sites inside or outside the Namib Desert the amino acids composition of the protein material forming the tube silk of Ariadna spiders. These spiders belong to the primitive Segestriidae family and spend their life inside vertical silk burrows dug within the sandy and gravelly soil of arid areas. The silks, previously purified by solubilization in hexafluoroisopropanol, were subjected to partial or total acid hydrolysis. Partial hydrolyzed samples, analyzed by mass spectrometry (matrix assisted laser desorption/ionization and electrospray), led to relevant information on the amino acid sequences in the proteins. The free amino acids formed by complete hydrolysis were derivatized with the Marfey’s reagent and characterized by electrospray mass spectrometry. The reconstruction of the amino acids highlights a homogeneous plan in the chemical structure of all the analyzed silks. Eight amino acids constituting the primary structure of the proteins were identified. Alanine and glycine are the most abundant ones, with a prevalence of alanine, constituting together at least 61% of the chemical composition of the protein material, differently from what occurs in known spidroins. High percentages of proline, serine and threonine and low percentages of leucine complete the peculiarity of these proteins. The purified silks were also characterized by Fourier-transform Infrared Spectroscopy and their thermal properties were investigated by differential scanning calorimetry. The comparison of the silk tubes among the various Namibian populations, carried out through a multivariate statistical analysis, shows significant differences in their amino acid assembly possibly due to habitat features.

Keywords

Amino acids Ecological adaptations Namibia Segestriidae Spider silk 

Notes

Acknowledgements

We wish to thank the Ministry of Environment and Tourism, Namibia, for a permit (permit number 2035/2015) to work in the Namib-Naukluft Park and to collect some silken tubes of Ariadna spiders in the framework of our project on behavioral adaptations of desert arthropods. We are deeply indebted to the editor and to the anonymous referees for their precious suggestions and assistance and to Christian Mulder for the final review. English was carefully checked thorough monolingual verification by a professional native speaker. Financial support was provided by the Ministry of University and Scientific Research (MIUR) of Italy and the Italian National Research Council (CNR).

References

  1. Andersen SO (1970) Amino acid composition of spider silks. Comp Biochem Physiol 35:705–711.  https://doi.org/10.1016/0010-406X(70)90988-6 CrossRefGoogle Scholar
  2. Aparecido Dos Santos-Pinto JR, Arcuri HA, Lubec G, Palma MS (2016) Structural characterization of the major ampullate silk spidroin-2 protein produced by the spider Nephila clavipes. Biochim Biophys Acta 1964:144–1454.  https://doi.org/10.1016/j.bbapap.2016.05.007 CrossRefGoogle Scholar
  3. Basiuk VA, Salerno M, Heredia A, Basiuk EV (2018) Unusual microstructure and mechanical properties of egg case of the bolas spieder Mastophora corpulenta banks (Araneae, Araneidae). Fibers Polym 8:1632–1639.  https://doi.org/10.1007/s12221-018-1128-y CrossRefGoogle Scholar
  4. Bich C, Zenobi R (2009) Mass spectrometry of large complexes. Curr Opin Struct Biol 19:632–639.  https://doi.org/10.1016/j.sbi.2009.08.004 CrossRefPubMedGoogle Scholar
  5. Blackledge TA (2013) Spider silk: molecular structure and function in webs. In: Nentwig W (ed) Spider Ecophysiology. Springer-Verlag, Berlin, Heidelberg, pp 267–282Google Scholar
  6. Blondelle SE, Forood B, Houghten RA, Pérez-Payá E (1997) Poly-alanine-based peptides as models for self-associated β-pleated-sheet complexes. Biochemistry 36:8393–8400.  https://doi.org/10.1021/bi963015b CrossRefPubMedGoogle Scholar
  7. Bramanti E, Catalano D, Forte C, Giovanneschi M, Masetti M, Veracini CA (2005) Solid state (13) C NMR and FT-IR spectroscopy of the cocoon silk of two common spiders. Spectrochim Acta A Mol Biomol Spectrosc 62(1–3):105–111.  https://doi.org/10.1016/j.saa.2004.12.008 CrossRefPubMedGoogle Scholar
  8. Bristowe WS (1958) The world of spiders. Collins, London. ISBN : 0002132567Google Scholar
  9. Casem ML, Turner D, Houchin K (1999) Protein and amino acid composition of silks from the cob weaver, Latrodectus hesperus (black widow). Int J Biol Macromol 24:103–108.  https://doi.org/10.1016/S0141-8130(98)00078-6 CrossRefPubMedGoogle Scholar
  10. Chen F, Gerber S, Heuser K, Korkhov VM, Lizak C, Mireku S, Locher KP, Zenobi R (2013) High-mass matrix-assisted laser desorption ionization-mass spectrometry of integral membrane proteins and their complexes. Anal Chem 85:3483–3488.  https://doi.org/10.1021/ac4000943 CrossRefPubMedGoogle Scholar
  11. Chen J, Venkatesan H, Hu J (2018) Biomimetic strategies for the spinning of artificial silk fibers. Adv Res Text Eng 3(3):2031 ISSN: 2572-9373Google Scholar
  12. Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 22:565–592.  https://doi.org/10.1146/22.110191.003025 CrossRefGoogle Scholar
  13. Comstock JH (1912) The spider book. Garden City, New York. ISBN 13:9780341954736Google Scholar
  14. Conti E, Barbagallo E, Battiato S, Marletta A, Costa G, Samperi F (2015a) Do habitat features affect the composition of silk proteins by Namibian arid-adapted Ariadna spiders (Araneae: Segestriidae)? Ital J Zool 82:48–60.  https://doi.org/10.1080/11250003.2014.975288 CrossRefGoogle Scholar
  15. Conti E, Costa G, Marletta A, Viscuso R, Vitale DGM (2015b) The chorion of eggs in a Namibian Ariadna species (Araneae: Segestriidae): morphological and SEM analyses. J Arachnol 43:224–227.  https://doi.org/10.1636/M14.72 CrossRefGoogle Scholar
  16. Conti E, Costa G, Liberatori G, Vannuccini ML, Protano G, Nannoni F, Corsi I (2018) Ariadna spiders as bioindicator of heavy elements contamination in the central Namib Desert. Ecol Indic 95:663–672.  https://doi.org/10.1016/j.ecolind.2018.08.014 CrossRefGoogle Scholar
  17. Conti E, Mulder C, Pappalardo AM, Ferrito V, Costa G (2019) How soil granulometry, temperature, and water predict genetic differentiation in Namibian spiders (Ariadna: Segestriidae) and explain their behavior. Ecol Evol 9:4382–4391.  https://doi.org/10.1002/ece3.4929 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Costa G (1995) Behavioral adaptations of desert animals. Springer Verlag, Berlin, Heidelberg ISBN 10: 3540585788CrossRefGoogle Scholar
  19. Costa G, Petralia A, Conti E, Hänel C, Seely MK (1993) Seven stone spiders of the gravel plains of the Namib Desert. Boll Acc Gioenia Sci Nat 26:77–83Google Scholar
  20. Costa G, Petralia A, Conti E, Hänel C (1995) A mathematical spider living on gravel plains of the Namib Desert. J Arid Environ 29:485–494.  https://doi.org/10.1016/S0140-1963(95)80020-4 CrossRefGoogle Scholar
  21. Costa G, Petralia A, Conti E (2000) Population dynamics of stone-ring spiders of the genus Ariadna Audouin (Araneae: Segestriidae), in western Namibia. Cimbebasia 16:223–229Google Scholar
  22. Craig CL, Hsu M, Kaplan D, Pierce NE (1999) A comparison of the composition of silk proteins produced by spiders and insects. Int J Biol Macromol 24:109–118.  https://doi.org/10.1016/S0141-8130(99)00006-9 CrossRefPubMedGoogle Scholar
  23. Craig CL, Riekel C, Herberstein ME, Weber RS, Kaplan D, Pierce NE (2000) Evidence for diet effects on the composition of silk proteins produced by spiders. Mol Biol Evol 17:1904–1913.  https://doi.org/10.1093/oxfordjournals.molbev.a026292 CrossRefPubMedGoogle Scholar
  24. Darragh AJ, Garrick DJ, Moughan PJ, Hendriks WH (1996) Correction for amino acid loss during acid hydrolysis of a purified protein. Anal Biochem 236:199–207.  https://doi.org/10.1006/abio.1996.0157 CrossRefPubMedGoogle Scholar
  25. Decae AE (1984) A theory on the origin of spiders and the primitive function of spider silk. J Arachnol 12:21–28 https://www.jstor.org/stable/3705099 Google Scholar
  26. Domon B, Aebersold R (2006) Mass spectrometry and protein analysis. Science 312:212–217.  https://doi.org/10.1126/science.1124619 CrossRefPubMedGoogle Scholar
  27. Foelix R (2010) Biology of spiders. Oxford Univ Press, Oxford ISBN: 9780199734825Google Scholar
  28. Fountoulakis M, Lahm HV (1998) Hydrolysis and amino acid composition analysis of proteins. J Chromatogr A 826:109–134.  https://doi.org/10.1016/S0021-9673(98)00721-3 CrossRefPubMedGoogle Scholar
  29. Garwood RJ, Dunlop JA (2014) Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders. PeerJ 2:641.  https://doi.org/10.7717/peerj.641 CrossRefGoogle Scholar
  30. Garwood RJ, Dunlop JA, Selden PA, Spencer ART, Atwood RC, Vo NT, Drakopoulos M (2016) Almost a spider: a 305-million-year-old fossil arachnid and spider origins. Proc Biol Sci Lond 283:20160125.  https://doi.org/10.1098/rspb.2016.0125 CrossRefGoogle Scholar
  31. Gatesy J, Hayashi C, Motriuk D, Woods J, Lewis R (2001) Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 291:2603–2605.  https://doi.org/10.1126/science.1057561 CrossRefPubMedGoogle Scholar
  32. Ghosh T, Garde S, Garcia AE (2003) Role of backbone hydration and salt-bridge formation in stability of α-helix in solution. Biophys J 85:3187–3193.  https://doi.org/10.1016/S0006-3495(03)74736-5 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Glatz L (1972) Der Spinnapparat haplogyner Spinnen (Arachnida, Araneae). Z Morphol Tiere 72:1–26.  https://doi.org/10.1007/BF00281752 CrossRefGoogle Scholar
  34. Guo C, Zhang J, Jordan JS, Wang X, Henning RW (2018) Structural comparison of various silkworm silks. An insight into the structure-property relationship. Biomacromolecules 19:906–917.  https://doi.org/10.1021/acs.biomac.7b01687 CrossRefPubMedGoogle Scholar
  35. Harmer AMT, Blackledge TA, Madin JS, Herberstein ME (2011) High-performance spider webs: integrating biomechanics, ecology and behaviour. J R Soc Interface 8:457–471.  https://doi.org/10.1098/rsif.2010.0454 CrossRefPubMedGoogle Scholar
  36. Hayashi CY, Shipley NH, Lewis RV (1999) Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. Int J Bio Macromol 24:271–275.  https://doi.org/10.1098/rsif.2010.0454 CrossRefGoogle Scholar
  37. Hayashi CY, Blackledge TA, Lewis R (2004) Molecular and mechanical characterization of aciniform silk: uniformity of iterated sequence modules in a novel member of the spider silk fibroin gene family. Mol Biol Evol 21:1950–1959.  https://doi.org/10.1093/molbev/msh204 CrossRefPubMedGoogle Scholar
  38. Henschel IR (1995) Tool use by spiders: stone selection and placement by corolla spiders Ariadna (Segestriidae) of the Namib Desert. Ethology 101:187–199.  https://doi.org/10.1111/j.1439-0310.1995.tb00357.x CrossRefGoogle Scholar
  39. Hess S, van Beek J, Pannell LK (2002) Acid hydrolysis of silk fibroins and determination of the enrichment of isotopically labelled amino acids using precolumn derivatization and high-performance liquid chromatography–electrospray ionization–mass spectrometry. Anal Biochem 311:19–26.  https://doi.org/10.1016/S0003-2697(02)00402-5 CrossRefPubMedGoogle Scholar
  40. Hu X, Lawrence B, Kohler K, Falick AM, Moore AMF, McMullen E, Jones PR, Vierra C (2005) Araneoid egg case silk: a fibroin with novel ensemble repeat units from the black widow spider, Latrodectus hesperus. Biochemistry 44:10020–10027.  https://doi.org/10.1021/bi050494i CrossRefPubMedGoogle Scholar
  41. Hu X, Kohler K, Falick AM, Moore AM, Jones PR, Vierra C (2006) Spider egg case core fibers: trimeric complexes assembled from TuSp1, ECP-1, and ECP-2. Biochemistry 45:3506–3516.  https://doi.org/10.1021/bi052105q CrossRefPubMedGoogle Scholar
  42. Hu X, Yuan J, Wang X, Vasanthavada K, Falick AM, Jones PR, La Mattina C, Vierra CA (2007) Analysis of aqueous glue coating proteins on the silk fibers of the cob weaver, Latrodectus hesperus. Biochemistry 46:3294–3303.  https://doi.org/10.1021/bi602507e CrossRefPubMedGoogle Scholar
  43. Ittah S, Michaeli A, Goldblum A, Gat U (2007) A model for the structure of the C-terminal domain of dragline spider silk and the role of its conserved cysteine. Biomacromolecules 8:2768–2773.  https://doi.org/10.1021/bm7004559 CrossRefPubMedGoogle Scholar
  44. Jackson M, Mantsch HH (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit Rev Biochem Mol Biol 30(2):95–120.  https://doi.org/10.3109/10409239509085140 CrossRefPubMedGoogle Scholar
  45. Jiang P, Guo C, Lv T, Xiao Y, Xiao X, Zhou B (2011) Structure, composition and mechanical properties of the silk fibres of the egg case of the Joro spider, Nephila clavata (Araneaee, Nephilidae). J Biosci 36:897–910.  https://doi.org/10.1007/s12038-011-9165-3 CrossRefPubMedGoogle Scholar
  46. Kaplan DL, Adams WW, Viney C, Farmer BL (1994) Silk polymers: materials science and biotechnology. ACS Books, Washington, DC.  https://doi.org/10.1021/bk-1994-0544 CrossRefGoogle Scholar
  47. Karschová S, Haier J (2016) Spinnerets and silk-producing system of Segestria senoculata (Araneae, Araneomorphae, Segestriidae). J Entomol Acarol Res 48:388–394.  https://doi.org/10.4081/jear.2016.5934 CrossRefGoogle Scholar
  48. Koehl P, Levitt M (1999) Structure-based conformational preferences of amino acids. Proc Natl Acad Sci U S A 96:12524–12529.  https://doi.org/10.1073/pnas.96.22.12524 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lewis RV (2006) Spider silk: ancient ideas for new biomaterials. Chem Rev 106:3762–3774.  https://doi.org/10.1021/cr010194g CrossRefPubMedGoogle Scholar
  50. Liu Y, Sponner D, Porter F, Vollrath F (2008a) Proline and processing of spider silks. Biomacromolecules 9:116–121.  https://doi.org/10.1021/bm700877g CrossRefPubMedGoogle Scholar
  51. Liu Y, Shao Z, Vollrath F (2008b) Elasticity of spider silks. Biomacromolecules 9:1782–1786.  https://doi.org/10.1021/bm7014174 CrossRefPubMedGoogle Scholar
  52. Lorusso M, Pepe A, Ibris N, Bochicchio B (2011) Molecular and supramolecular studies on poly-Glycine and poly-L-Proline. Soft Matter 7:6327–6336.  https://doi.org/10.1039/C1SM05726J CrossRefGoogle Scholar
  53. Madurga R, Blackledge TA, Perea B, Plaza GL, Riekel C, Burghammer M, Elices M, Guinea G, Pérez-Rigueiro J (2015) Persistence and variation in microstructural design during the evolution of spider silk. Sci Rep 5:14820.  https://doi.org/10.1038/srep14820 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Main BY (1993) From flooding avoidance to foraging: adaptive shifts in trapdoor spider behavior. Mem Queensl Mus 33:599–606 ISSN: 0079-8835Google Scholar
  55. Marsh BA (1990) The microenvironment associated with Welwitschia mirabilis in the Namib Desert. In: Seely MK (Ed.), Namib Ecology. 25 years of Namib research. Transvaal Mus Monogr 7:149-154. ISBN 0 907990 10Google Scholar
  56. McGill M, Holland GP, Kaplan DL (2019) Experimental methods for characterizing the secondary structure and thermal properties of silk proteins. Macromol Rapid Commun 40:e1800390.  https://doi.org/10.1002/marc.201800390 CrossRefPubMedGoogle Scholar
  57. Montaudo G, Lattimer RP (eds) (2002) Mass spectrometry of polymers. CRC Press, Boca Raton, FL ISBN 9780849331275Google Scholar
  58. Montaudo G, Samperi F, Montaudo M (2006) Characterization of synthetic polymers by MALDI-MS. Prog Polym Sci 31:277–357.  https://doi.org/10.1016/j.progpolymsci.2005.12.001 CrossRefGoogle Scholar
  59. Moore WH, Krimm S (1976) Vibrational analysis of peptides, polypeptides, and proteins. II. β-poly(L-alanine) and β-poly(L-alanyl-Glycine). Biopolymers 15:2465–2483.  https://doi.org/10.1002/bip.1976.360151211 CrossRefPubMedGoogle Scholar
  60. Mulder C, Conti E, Costa G (2019) Belowground thermoregulation in Namibian desert spiders that burrow their own chemostats. Acta Oecol 96:18–23.  https://doi.org/10.1016/j.actao.2019.02.003 CrossRefGoogle Scholar
  61. Ozols J (1990) Amino acid analysis. Meth Enzymol 182:587–601.  https://doi.org/10.1016/0076-6879(90)82046-5 CrossRefPubMedGoogle Scholar
  62. Papadopoulos P, Sölter J, Kremer F (2007) Structure-property relationships in major ampullate spider silk as deduced from polarized FTIR spectroscopy. Eur Phys J E Soft Matt 24:193–199.  https://doi.org/10.1140/epje/i2007-10229-9 CrossRefGoogle Scholar
  63. Platnik NI (2019) The world spider catalog. Version 20.5. Natural History Museum of Bern (accessed on September 20, 2019). 10.24436/2Google Scholar
  64. Pocock RI (1895) Description of two new spiders obtained by Messrs. In: J.J. Quelch, F. MacConnell (Eds.), On the summit of Mount Roraima, in Demerara; with a note upon the systematic position of the genus Desis. Ann Mag Nat Hist Ser 6, 16:139-143.  https://doi.org/10.1080/00222939508680241 CrossRefGoogle Scholar
  65. Reddy AS, Shad Ali G (2011) Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip Rev RNA 2:875–889.  https://doi.org/10.1002/wma.98 CrossRefPubMedGoogle Scholar
  66. Rising A (2007) Spider dragline silk. Molecular properties and recombinant expression. Swedish University of Agricultural Sciences, Uppsala. ISSN: 1652-6880, Doctoral ThesisGoogle Scholar
  67. Rising A, Nimmervoll H, Grip S, Fernandez-Arias A, Storckenfeldt E, Knight DP, Vollrath F, Engström W (2005) Spider silk proteins. Mechanical properties and gene sequence. Zool Sci 22:273–281.  https://doi.org/10.2108/zsj.22.273 CrossRefPubMedGoogle Scholar
  68. Rising A, Hjälm G, Engström W, Johansson J (2006) N-terminal nonrepetitive domain common to dragline, flagelliform and cylindriform spider silk proteins. Biomacromolecules 7:3120–3124.  https://doi.org/10.1021/bm060693x CrossRefPubMedGoogle Scholar
  69. Römer L, Scheibel T (2008) The elaborate structure of spider silk. Prion 2:154–161.  https://doi.org/10.4161/pri.2.4.7490 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Savage KN, Gosline JM (2008) The effect of proline on the network structure of major ampullate silks as inferred from their mechanical and optical properties. J Exp Biol 211:1937–1947.  https://doi.org/10.1242/jeb.014217 CrossRefPubMedGoogle Scholar
  71. Scheibel T (2005) Protein fibers as performance proteins: new technologies and applications. Curr Opin Biotechnol 16:427–433.  https://doi.org/10.1016/j.copbio.2005.05.005 CrossRefPubMedGoogle Scholar
  72. Selden PA (1996) First fossil mesothele spider, from the carboniferous of France. Rev Suisse Zool Vol Hors Sér 2:585–596Google Scholar
  73. Selden PA, Shear WA, Sutton MD (2008) Fossil evidence for the origin of spider spinnerets, and a proposed arachnid order. Proc Natl Acad Sci U S A 105:20781–20785.  https://doi.org/10.1073/pnas.0809174106 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Selden PA, Shcherbakov DE, Dunlop JA, Eskov KY (2014) Arachnids from the carboniferous of Russia and Ukraine, and the Permian of Kazakhstan. Paläontol Z 88:297–307.  https://doi.org/10.1007/s12542-013-0198-9 CrossRefGoogle Scholar
  75. Shanyengana ES, Henschel JR, Seely MK, Sanderson RD (2002) Exploring fog as a supplementary water source in Namibia. Atmos Res 64:251–259.  https://doi.org/10.1016/S0169-8095(02)00096-0 CrossRefGoogle Scholar
  76. Shear W, Palmer J, Coddington JA, Bonamo PN (1989) A Devonian spinneret: early evidence of spiders and silk use. Science 246:479–481.  https://doi.org/10.1126/science.246.4929.479 CrossRefPubMedGoogle Scholar
  77. Shi X, Holland GP, Yarger J (2013) Amino acid analysis of spider dragline silk using 1H-NMR. Anal Biochem 440:150–157.  https://doi.org/10.1016/j.ab.2013.05.006 CrossRefPubMedGoogle Scholar
  78. Singha K, Maity S, Singha M (2012) Spinning and applications of spider silk. Front Sci 2:92–100.  https://doi.org/10.5923/j.fs.20120205.02 CrossRefGoogle Scholar
  79. Sirichaisit J, Young RJ, Vollrath F (1999) Molecular deformation in spider dragline silk subjected to stress. Polymers 40:2493–2500.  https://doi.org/10.1016/S0032-3861(99)00293-1 CrossRefGoogle Scholar
  80. Stowe MK (1986) Prey specialization in the Araneidae. In: Shear WA (ed) Spiders, webs, behavior, and evolution. Stanford University Press, Stanford, pp 101–131 ISBN 13:978-0804712033Google Scholar
  81. Tremblay M-L, Xu L, Lefèvre T, Sarker M, Orrel KE, Leclerc J, Meng Q, Pézolet M, Auger M, Liu X-Q, Rainey JK (2015) Spider wrapping silk fibre architecture arising from its modular soluble protein precursor. Sci Rep 5:11502.  https://doi.org/10.1038/srep11502 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Tso IM, Wu HC, I.R. Hwang IR (2005) Giant wood spider Nephila pilipes alters silk protein in response to prey variation. J Exp Biol 208:1053–1061.  https://doi.org/10.1242/jeb.01437 CrossRefGoogle Scholar
  83. Ubick D (2005) Segestriidae. In: Ubick D, Paquin P, Cushing PE, Roth V (eds) Spiders of North America: an identification manual. Am Arachnol Soc, pp 219–220 ISBN 10: 0977143902Google Scholar
  84. Uyangaa E, Lee H-K, Kug Eo S (2012) Glutamine and Leucine provide enhanced protective immunity against mucosal infection with Herpes simplex virus type 1. Immune Netw 12:196–206.  https://doi.org/10.4110/in.2012.12.5.196 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Viles HA (2005) Microclimate and weathering in the central Namib Desert, Namibia. Geomorphology 67:189–209.  https://doi.org/10.1016/j.geomorph.2004.04.006 CrossRefGoogle Scholar
  86. Vollrath F (2000) Strength and structure of spider’s silk. Rev Mol Biotechnol 74:67–83.  https://doi.org/10.1016/S1389-0352(00)00006-4 CrossRefGoogle Scholar
  87. Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410:541–548.  https://doi.org/10.1038/35069000 CrossRefPubMedGoogle Scholar
  88. Vollrath F, Selden P (2007) The role of behavior in the evolution of spiders, silks and webs. Annu Rev Ecol Syst 38:819–846.  https://doi.org/10.1146/annurev.ecolsys.37.091305.110221 CrossRefGoogle Scholar
  89. Vollrath F, Holtet T, Thogersen H, Frische S (1996) Structural organization of spider silk. Proc R Soc Lond 263:147–151.  https://doi.org/10.1098/rspb/1996.0023 CrossRefGoogle Scholar
  90. Wang S, Huang W, Yang D (2012) NMR structure note: repetitive domain of aciniform spidroin 1 from Nephila antipodiana. J Biomol NMR 54:415–420.  https://doi.org/10.1007/s10858-012-9679-5 CrossRefPubMedGoogle Scholar
  91. Weidmann S, Mikutis G, Barylyuk K, Zenobi R (2013) Mass discrimination in high-mass MALDI-MS. J Am Soc Mass Spectrom 24:1396–1404.  https://doi.org/10.1007/s13361-013-0686-x CrossRefPubMedGoogle Scholar
  92. Work RW, Young CT (1987) The amino-acid compositions of major and minor ampullate silks of certain orb-web-building spiders (Araneae, Araneidae). J Arachnol 15:65–80 https://www.jstor.org/stable/3705510 Google Scholar
  93. Zax DB, Armanios DE, Horak S, Brodowski C, Yang Z (2004) Variation of mechanical properties with amino acid content in the silk of Nephila clavipes. Biomacromolecules 5:732–738.  https://doi.org/10.1021/bm034309x CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Dipartimento di Scienze Biologiche, Geologiche ed AmbientaliUniversità degli Studi di CataniaCataniaItaly
  2. 2.CNR—Istituto per i Polimeri, Compositi e Biomateriali (IPCB)CataniaItaly

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