Changing environments and structure--property relationships in marine biomaterials.

Most marine organisms make functional biomolecular materials that extend to varying degrees ‘beyond their skins’. These materials are very diverse and include shells, spines, frustules, tubes, mucus trails, egg capsules and byssal threads, to mention a few. Because they are devoid of cells, these materials lack the dynamic maintenance afforded intra-organismic tissues and thus are usually assumed to be inherently more durable than their internalized counterparts. Recent advances in nanomechanics and submicron spectroscopic imaging have enabled the characterization of structure–property relationships in a variety of extra-organismic materials and provided important new insights about their adaptive functions and stability. Some structure–property relationships in byssal threads are described to show how available analytical methods can reveal hitherto unappreciated interdependences between these materials and their prevailing chemical, physical and ecological environments. * AFM : atomic force microscopy BESSY : Berliner Elektronenspeicherring-Gesellschaft fur Synchrotronstrahlung EDX : energy dispersive X-ray spectroscopy EXAFS : extended X-ray absorption fine structure spectroscopy FECO : fringes of equal chromatic order MALDI : matrix-assisted laser desorption-ionization mass spectroscopy PIXE : proton induced X-ray emission spectroscopy SAXS : small angle X-ray scattering SFA : surface forces apparatus ssNMR : solid-state nuclear magnetic resonance WAXS : wide angle X-ray scattering XANES : X-ray absorption for near edge structure XAS : X-ray absorption spectroscopy

[1]  J. Warwicker Comparative studies of fibroins. II. The crystal structures of various fibroins. , 1960, Journal of molecular biology.

[2]  M. Mann,et al.  Analysis of proteins and proteomes by mass spectrometry. , 2001, Annual review of biochemistry.

[3]  S. Lindquist,et al.  The heat-shock proteins. , 1988, Annual review of genetics.

[4]  Jacob N Israelachvili,et al.  The Contribution of DOPA to Substrate–Peptide Adhesion and Internal Cohesion of Mussel‐Inspired Synthetic Peptide Films , 2010, Advanced functional materials.

[5]  J. Videler The Extended Organism , 2001 .

[6]  J. Waite,et al.  Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads , 2007, Journal of Experimental Biology.

[7]  G. Stucky,et al.  High Abrasion Resistance with Sparse Mineralization: Copper Biomineral in Worm Jaws , 2002, Science.

[8]  Frank Zok,et al.  Jumbo squid beaks: inspiration for design of robust organic composites. , 2007, Acta biomaterialia.

[9]  J. Waite,et al.  Linking Adhesive and Structural Proteins in the Attachment Plaque of Mytilus californianus* , 2006, Journal of Biological Chemistry.

[10]  J H Waite,et al.  Role of transition metals in sclerotization of biological tissue. , 2008, Acta biomaterialia.

[11]  I. Svane,et al.  Attachment and orientation of Mytilus Edulis L. in flowing water , 1994 .

[12]  J. Castilla,et al.  Phenotypic variability in byssus thread production of intertidal mussels induced by predators with different feeding strategies , 2008 .

[13]  E. D. Langre Methodological advances in predicting flow-induced dynamics of plants using mechanical-engineering theory. , 2012 .

[14]  Emily Carrington,et al.  Seasonal variation in mussel byssal thread mechanics , 2006, Journal of Experimental Biology.

[15]  C. Yonge On The Primitive Significance of the Byssus in the Bivalvia and its Effects in Evolution , 1962, Journal of the Marine Biological Association of the United Kingdom.

[16]  H. Price Seasonal variation in the strength of byssal attachment of the common mussel Mytilus edulis L. , 1980, Journal of the Marine Biological Association of the United Kingdom.

[17]  K. Raymond,et al.  Biochemical and Physical Properties of Siderophores , 2004 .

[18]  J. Waite,et al.  Oxidative stress and the mechanical properties of naturally occurring chimeric collagen-containing fibers. , 2001, Biophysical journal.

[19]  T. L. Coombs,et al.  Mytilus byssal threads as an environmental marker for metals , 1981 .

[20]  W. Winkle Effect of environmental factors on byssal thread formation , 1970 .

[21]  J. Waite Catechol Oxidase in the Byssus of the Common Mussel, Mytilus Edulis L. , 1985, Journal of the Marine Biological Association of the United Kingdom.

[22]  D. Ginzinger,et al.  Silk Properties Determined by Gland-Specific Expression of a Spider Fibroin Gene Family , 1996, Science.

[23]  Bruce P. Lee,et al.  Mussel-Inspired Adhesives and Coatings. , 2011, Annual review of materials research.

[24]  M. Byrne,et al.  Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean , 2011, Proceedings of the Royal Society B: Biological Sciences.

[25]  D. S. Lee,et al.  Metal and transuranic records in mussel shells, byssal threads and tissues , 1982 .

[26]  H. W. Lefevre,et al.  PIXE-STIM microtomography: Zinc and manganese concentrations in a scorpion stinger , 1992 .

[27]  G. Jackson Seascapes: the world of aquatic organisms as determined by their particulate natures , 2012, Journal of Experimental Biology.

[28]  E. Carrington,et al.  Interspecific Comparison of the Mechanical Properties of Mussel Byssus , 2006, The Biological Bulletin.

[29]  R. Tremblay,et al.  Biotic and abiotic factors influencing attachment strength of blue mussels Mytilus edulis in suspended culture , 2008 .

[30]  A. B. Yule,et al.  Adhesion and substrate choice in mussels and barnacles , 1985 .

[31]  E. Carrington Seasonal variation in the attachment strength of blue mussels: Causes and consequences , 2002 .

[32]  J. Waite,et al.  The peculiar collagens of mussel byssus. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[33]  K. Venkateswaran,et al.  Pseudoalteromonas peptidolytica sp. nov., a novel marine mussel-thread-degrading bacterium isolated from the Sea of Japan. , 2000, International journal of systematic and evolutionary microbiology.

[34]  E. Kádár,et al.  Unidentified extracellular prokaryotes within the byssal threads of the deep-sea vent mussel Bathymodiolus azoricus , 2006, Parasitology.

[35]  J. Waite,et al.  The formation of mussel byssus: anatomy of a natural manufacturing process. , 1992, Results and problems in cell differentiation.

[36]  T. L. Coombs,et al.  The kinetics of accumulation and excretion of ferric hydroxide in Mytilus edulis (I.) and its distribution in the tissues , 1976 .

[37]  J. Waite,et al.  Rotational Echo Double Resonance Detection of Cross-links Formed in Mussel Byssus under High-Flow Stress* , 1999, The Journal of Biological Chemistry.

[38]  J. Herbert Waite,et al.  Mussel protein adhesion depends on thiol-mediated redox modulation , 2011, Nature chemical biology.

[39]  Dariusz Stramski,et al.  Optical variability of seawater in relation to particle concentration, composition, and size distribution in the nearshore marine environment at Imperial Beach, California , 2010 .

[40]  G. Young Byssus-thread production by the mussel Mytilus edulis : effects of environmental factors , 1985 .

[41]  Henrik Birkedal,et al.  Zinc and mechanical prowess in the jaws of Nereis, a marine worm , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Brian M. Hopkinson,et al.  Effect of Ocean Acidification on Iron Availability to Marine Phytoplankton , 2010, Science.

[43]  J. Waite,et al.  Mapping Chemical Gradients within and along a Fibrous Structural Tissue, Mussel Byssal Threads* , 2005, Journal of Biological Chemistry.

[44]  T. Suchanek,et al.  Mussels in flow: drag and dislodgement by epizoans , 1984 .

[45]  Simon J L Billinge,et al.  The Problem with Determining Atomic Structure at the Nanoscale , 2007, Science.

[46]  Georg E Fantner,et al.  Protective coatings on extensible biofibres. , 2007, Nature materials.

[47]  J. Waite,et al.  Probing the Adhesive Footprints of Mytilus californianus Byssus* , 2006, Journal of Biological Chemistry.

[48]  Peter Fratzl,et al.  Collagen insulated from tensile damage by domains that unfold reversibly: in situ X-ray investigation of mechanical yield and damage repair in the mussel byssus. , 2009, Journal of structural biology.

[49]  Hongbo Zeng,et al.  Strong reversible Fe3+-mediated bridging between dopa-containing protein films in water , 2010, Proceedings of the National Academy of Sciences.

[50]  D. Nordstrom,et al.  Negative pH and Extremely Acidic Mine Waters from Iron Mountain, California , 2000 .

[51]  J. Waite,et al.  Immunolocalization of Dpfp1, a byssal protein of the zebra mussel Dreissena polymorpha. , 2000, The Journal of experimental biology.

[52]  W. Astbury The X‐Ray Interpretation of Fibre Structure , 1933 .

[53]  J. Waite,et al.  Critical role of zinc in hardening of Nereis jaws , 2006, Journal of Experimental Biology.

[54]  K. Simkiss,et al.  The uptake of zinc from artificial sediments by Mytilus edulis , 1996, Journal of the Marine Biological Association of the United Kingdom.

[55]  J. Israelachvili,et al.  Recent advances in the surface forces apparatus (SFA) technique , 2010 .

[56]  Youli Li,et al.  Four-stranded coiled-coil elastic protein in the byssus of the giant clam, Tridacna maxima. , 2012, Biomacromolecules.

[57]  Hongbo Zeng,et al.  Protein- and Metal-dependent Interactions of a Prominent Protein in Mussel Adhesive Plaques* , 2010, The Journal of Biological Chemistry.

[58]  M. Frohman,et al.  Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Delphine Gourdon,et al.  Adhesion mechanisms of the mussel foot proteins mfp-1 and mfp-3 , 2007, Proceedings of the National Academy of Sciences.

[60]  Peter Fratzl,et al.  Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings , 2010, Science.

[61]  Gosline,et al.  Mechanical design of mussel byssus: material yield enhances attachment strength , 1996, The Journal of experimental biology.

[62]  J. Waite,et al.  Hyperunstable matrix proteins in the byssus of Mytilus galloprovincialis , 2009, Journal of Experimental Biology.

[63]  D. Bruce Chase,et al.  Ferric Ion Complexes of a DOPA-Containing Adhesive Protein from Mytilus edulis , 1996 .

[64]  J. S. Turner,et al.  The Extended Organism: The Physiology of Animal-Built Structures , 2000 .

[65]  Michelle L. Reyzer,et al.  MALDI imaging mass spectrometry: molecular snapshots of biochemical systems , 2007, Nature Methods.

[66]  Henrik Birkedal,et al.  pH-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli , 2011, Proceedings of the National Academy of Sciences.

[67]  J. van de Koppel,et al.  The influence of local- and landscape-scale processes on spatial self-organization in estuarine ecosystems , 2012, Journal of Experimental Biology.

[68]  A. McElnea,et al.  Changes in water quality following tidal inundation of coastal lowland acid sulfate soil landscapes , 2009 .

[69]  Kristine Steen Jensen,et al.  Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation. , 2009, Antioxidants & redox signaling.

[70]  M. Boller,et al.  Seasonal disturbance to mussel beds: Field test of a mechanistic model predicting wave dislodgment , 2009 .

[71]  P. S. Meadows,et al.  Experimental analysis of byssus thread production by Mytilus edulis and Modiolus modiolus in sediments , 1989 .

[72]  G. Pharr,et al.  An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments , 1992 .

[73]  G. Stucky,et al.  Melanin and Glycera Jaws , 2006, Journal of Biological Chemistry.

[74]  J. Waite,et al.  Effects of hydration on mechanical properties of a highly sclerotized tissue. , 2008, Biophysical journal.

[75]  R. Schneider Conditioning Film-Induced Modification of Substratum Physicochemistry—Analysis by Contact Angles , 1996 .

[76]  J. Waite,et al.  Yield and post-yield behavior of mussel byssal thread: a self-healing biomolecular material. , 2001, Biomacromolecules.

[77]  J. Babarro,et al.  Secretion of byssal threads in Mytilus galloprovincialis: quantitative and qualitative values after spawning stress , 2009, Journal of Comparative Physiology B.

[78]  John M. Gosline,et al.  Mechanical design of mussell byssus: Load cycle and strain rate dependence , 2004 .

[79]  G. Young The effect of sediment type upon the position and depth at which byssal attachment occurs in Mytilus edulis , 1983, Journal of the Marine Biological Association of the United Kingdom.

[80]  K. Biemann,et al.  Hydroxyarginine-containing Polyphenolic Proteins in the Adhesive Plaques of the Marine Mussel Mytilus edulis(*) , 1995, The Journal of Biological Chemistry.