Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation

The egg capsules of marine prosobranch gastropods, commonly know as whelks, function as a protective encapsulant for whelk embryos in wave-swept marine environments. The proteinaceous sheets comprising the wall of whelk egg capsules (WEC) exhibit long-range reversible extensibility with a hysteresis of up to 50 per cent, previously suggested to result from reversible changes in the structure of the constituent protein building blocks. Here, we further investigate the structural changes of the WEC biopolymer at various hierarchical levels using several different time-resolved in situ approaches. We find strong evidence in these biological polymers for a strain-induced reversible transition from an ordered conformational phase to a largely disordered one that leads to the characteristic reversible hysteretic behaviour, which is reminiscent of the pseudoelastic behaviour in some metallic alloys. On the basis of these results, we generate a simple numerical model incorporating a worm-like chain equation to explain the phase transition behaviour of the WEC at the molecular level.

[1]  L. Kreplak,et al.  New Aspects of the a-Helix to b-Sheet Transition in Stretched Hard a-Keratin Fibers , 2004 .

[2]  André E. X. Brown,et al.  Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. , 2007, Biophysical journal.

[3]  T. Lefèvre,et al.  Orientation-Insensitive Spectra for Raman Microspectroscopy , 2006, Applied spectroscopy.

[4]  Gernot Kostorz,et al.  Phase Transformations in Materials , 2001 .

[5]  A. Talari,et al.  Raman Spectroscopy of Biological Tissues , 2007 .

[6]  T. Creighton Proteins: Structures and Molecular Properties , 1986 .

[7]  A. Oberhauser,et al.  Multiple conformations of PEVK proteins detected by single-molecule techniques , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Klaus Schulten,et al.  Mechanical unfolding intermediates in titin modules , 1999, Nature.

[9]  H. Steeb,et al.  Superelasticity and Self-Healing of Proteinaceous Biomaterials , 2011 .

[10]  Laurent Kreplak,et al.  New Aspects of the α-Helix to β-Sheet Transition in Stretched Hard α-Keratin Fibers , 2004 .

[11]  M. Rief,et al.  Designing the folding mechanics of coiled coils. , 2009, Chemphyschem : a European journal of chemical physics and physical chemistry.

[12]  J. Gosline,et al.  Molecular design of the α–keratin composite: insights from a matrix–free model, hagfish slime threads , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  N. Stellwagen,et al.  DNA persistence length revisited. , 2001, Biopolymers.

[14]  S. Bykov,et al.  Peptide secondary structure folding reaction coordinate: correlation between uv raman amide III frequency, Psi Ramachandran angle, and hydrogen bonding. , 2006, The journal of physical chemistry. B.

[15]  Klaus Schulten,et al.  Molecular basis of fibrin clot elasticity. , 2008, Structure.

[16]  Ali Miserez,et al.  Non-entropic and reversible long-range deformation of an encapsulating bioelastomer. , 2009, Nature materials.

[17]  E. Siggia,et al.  Entropic elasticity of lambda-phage DNA. , 1994, Science.

[18]  R. Shadwick,et al.  Reversibly labile, sclerotization-induced elastic properties in a keratin analog from marine snails: whelk egg capsule biopolymer (WECB) , 2007, Journal of Experimental Biology.

[19]  Wolfgang Wagermaier,et al.  Cooperative deformation of mineral and collagen in bone at the nanoscale , 2006, Proceedings of the National Academy of Sciences.

[20]  Maria Victoria Biezma Moraleda,et al.  How much background in chemistry do material science and engineering students require , 2010 .

[21]  T. A. Rawlings Adaptations to Physical Stresses in the Intertidal Zone: The Egg Capsules of Neogastropod Molluscs , 1999 .

[22]  P. Fratzl,et al.  A new experimental station for simultaneous X-ray microbeam scanning for small- and wide-angle scattering and fluorescence at BESSY II , 2006 .

[23]  F. Vollrath,et al.  Comparison of the spinning of selachian egg case ply sheets and orb web spider dragline filaments. , 2001, Biomacromolecules.

[24]  Robert E Shadwick,et al.  Mechanical characterization of an unusual elastic biomaterial from the egg capsules of marine snails (Busycon spp.). , 2002, Biomacromolecules.

[25]  Disorder-driven first-order phase transformations: A model for hysteresis , 1994 .

[26]  G. Kostorz Phase Transformations in Materials: KOSTORZ:PHASE TRANSFORM. O-BK , 2005 .

[27]  Matthias Rief,et al.  The myosin coiled-coil is a truly elastic protein structure , 2002, Nature materials.

[28]  Shore,et al.  Hysteresis and hierarchies: Dynamics of disorder-driven first-order phase transformations. , 1992, Physical review letters.

[29]  Christian Riekel,et al.  The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. , 2003, Biophysical journal.

[30]  J. Pechenik Role of Encapsulation in Invertebrate Life Histories , 1979, The American Naturalist.

[31]  P. Burkhard,et al.  Coiled coils: a highly versatile protein folding motif. , 2001, Trends in cell biology.

[32]  J. Bandekar,et al.  Amide modes and protein conformation. , 1992, Biochimica et biophysica acta.

[33]  Z. Guan,et al.  Modular domain structure: a biomimetic strategy for advanced polymeric materials. , 2004, Journal of the American Chemical Society.

[34]  Philippe Colomban,et al.  Nanomechanics of single keratin fibres: A Raman study of the α‐helix →β‐sheet transition and the effect of water , 2007 .

[35]  S. Asher,et al.  Dihedral psi angle dependence of the amide III vibration: a uniquely sensitive UV resonance Raman secondary structural probe. , 2001, Journal of the American Chemical Society.

[36]  G. Rose,et al.  Redrawing the Ramachandran plot after inclusion of hydrogen-bonding constraints , 2010, Proceedings of the National Academy of Sciences.