Skip to main content

Interfacial Phenomena in Marine and Freshwater Mussel Adhesion

  • Chapter
  • First Online:
Biological Adhesives

Abstract

The attachment of mussels to underwater surfaces is one of the best-studied examples of biological adhesion, yet it continues to provide new insights into the phenomenon of wet adhesion. Both marine and freshwater mussels secrete a proteinaceous byssus, which attaches the mussel to a wide variety of surfaces with considerable strength. In marine mussels, Dopa (3,4-dihydroxyphenylalanine)-containing proteins have been shown to play key roles in this process, while less is known about the mechanism of adhesion in freshwater mussels, which contain much less Dopa. This chapter will highlight some of the recent developments in the mechanistic understanding of byssal adhesion, with a focus on the adhesive interface itself. In marine mussels, the extensive foundational work that preceded the last edition of this book has allowed a more recent emphasis on protein function, leading to important new insights regarding redox chemistry at the adhesive interface, the effect of surface chemistry on adhesion, and the role of amino acids other than Dopa in adhesion. Prior to this, adhesion of freshwater mussels will be reviewed. Here, the state of knowledge is much more nascent, with current emphasis still on protein sequencing and distribution. Nevertheless, careful structural characterization of the freshwater mussel adhesion has led to new understandings on the nature of the byssal adhesive interface. Furthermore, the comparison of the separately evolved adhesion strategies of freshwater and marine mussels may lead to new insights into the essential requirements of underwater adhesion.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akdogan Y, Wei W, Huang KY, Kageyama Y, Danner EW, Miller DR, Rodriguez NRM, Waite JH, Han S (2014) Intrinsic surface-drying properties of bioadhesive proteins. Angew Chem Int Ed 53(42):11253–11256

    Article  CAS  Google Scholar 

  • Anderson KE, Waite JH (1998) A major protein precursor of zebra mussel (Dreissena polymorpha) byssus: deduced sequence and significance. Biol Bull 194(2):150–160

    Article  CAS  PubMed  Google Scholar 

  • Anderson KE, Waite JH (2000) Immunolocalization of Dpfp1, a byssal protein of the zebra mussel Dreissena polymorpha. J Exp Biol 203(20):3065–3076

    CAS  PubMed  Google Scholar 

  • Anderson KE, Waite JH (2002) Biochemical characterization of a byssal protein from Dreissena bugensis (Andrusov). Biofouling 18(1):37–45

    Article  CAS  Google Scholar 

  • Anderson TH, Yu J, Estrada A, Hammer MU, Waite JH, Israelachvili JN (2010) The contribution of DOPA to substrate-peptide adhesion and internal cohesion of mussel-inspired synthetic peptide films. Adv Funct Mater 20(23):4196–4205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bairati A, Zuccarello LV (1976) Ultrastructure of the byssal apparatus of Mytilus galloprovincialis 4. Observations by transmission electron-microscopy. Cell Tissue Res 166(2):219–234

    Article  CAS  PubMed  Google Scholar 

  • Bandara N, Zeng H, Wu J (2013) Marine mussel adhesion: biochemistry, mechanisms, and biomimetics. J Adhes Sci Technol 27(18–19):2139–2162

    Article  CAS  Google Scholar 

  • Benedict CV, Waite JH (1986) Composition and ultrastructure of the byssus of Mytilus edulis. J Morphol 189(3):261–270

    Article  CAS  PubMed  Google Scholar 

  • Bonner TP, Rockhill RL (1994a) Functional morphology of the Zebra Mussel Byssus Dreissena polymorpha. Inform Rev 5:3

    Google Scholar 

  • Bonner TP, Rockhill RL (1994b) Ultrastructure of the Byssus of the Zebra Mussel (Dreissena-Polymorpha, Mollusca, Bivalvia). Trans Am Microsc Soc 113(3):302–315

    Article  Google Scholar 

  • Burzio LA, Waite JH (2000) Crosslinking in adhesive quinoproteins: studies with model decapeptides. Biochemistry 39(36):11147–11153

    Article  CAS  PubMed  Google Scholar 

  • Connely NA, O'Neill CR Jr, Knuth BA, Brown TL (2007) Economic impacts of zebra mussels on drinking water treatment and electric power generation facilities. Environ Manag 40:150–112

    Google Scholar 

  • Danner EW, Kan YJ, Hammer MU, Israelachvili JN, Waite JH (2012) Adhesion of mussel foot protein Mefp-5 to mica: an underwater superglue. Biochemistry 51(33):6511–6518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckroat L (1993) The Byssus of the Zebra Mussel (Dreissena Polymorpha): morphology, byssal thread formation, and detachment. In: Nalepa TF, Schloesser DW (eds) Zebra Mussels: biology, impacts, and control. CRC Press, Boca Raton, pp 239–263

    Google Scholar 

  • Farsad N, Sone ED (2012) Zebra mussel adhesion: structure of the byssal adhesive apparatus in the freshwater mussel, Dreissena polymorpha. J Struct Biol 177(3):613–620

    Article  PubMed  Google Scholar 

  • Gantayet A, Ohana L, Sone ED (2013) Byssal proteins of the freshwater zebra mussel, Dreissena polymorpha. Biofouling 29(1):77–85

    Article  CAS  PubMed  Google Scholar 

  • Gantayet A, Rees DJ, Sone ED (2014) Novel proteins identified in the insoluble byssal matrix of the freshwater Zebra Mussel. Mar Biotechnol 16(2):144–155

    Article  CAS  PubMed  Google Scholar 

  • Gilbert T, Sone E (2010) The byssus of the zebra mussel (Dreissena polymorpha): spatial variations in protein composition. Biofouling 26:829–836

    Article  CAS  PubMed  Google Scholar 

  • Guerette PA, Hoon S, Seow Y, Raida M, Masic A, Wong FT, Ho VHB, Kong KW, Demirel MC, Pena-Francesch A, Amini S, Tay GZ, Ding D, Miserez A (2013) Accelerating the design of biomimetic materials by integrating RNA-seq with proteomics and materials science. Nat Biotechnol 31(10):908–915

    Article  CAS  PubMed  Google Scholar 

  • Harrington MJ, Waite JH (2009) How nature modulates a fiber’s mechanical properties: mechanically distinct fibers drawn from natural mesogenic block copolymer variants. Adv Mater 21(4):440–444

    Article  CAS  Google Scholar 

  • Harrington MJ, Masic A, Holten-Andersen N, Waite JH, Fratzl P (2010) Iron-clad fibers: a metal-based biological strategy for hard flexible coatings. Science 328(5975):216–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hennebert E, Maldonado B, Ladurner P, Flammang P, Santos R (2015) Experimental strategies for the identification and characterization of adhesive proteins in animals: a review. Interface Focus 5:20140064, http://dx.doi.org/20140010.20141098/rsfs.20142014.20140064

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang DS, Zeng HB, Masic A, Harrington MJ, Israelachvili JN, Waite JH (2010) Protein- and metal-dependent Interactions of a prominent protein in mussel adhesive plaques. J Biol Chem 285(33):25850–25858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang DS, Zeng H, Lu Q, Israelachvili J, Waite JH (2012) Adhesion mechanism in a DOPA-deficient foot protein from green mussels. Soft Matter 8(20):5640–5648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang DS, Wei W, Rodriguez-Martinez NR, Danner E, Waite JH (2013) A microcosm of wet adhesion: dissection protein interactions in mussel attachment plaques. In: Zeng H (ed) Polymer adhesion, friction, and lubrication. Wiley, Hoboken, pp 319–349

    Chapter  Google Scholar 

  • Israelachvili J, Min Y, Akbulut M, Alig A, Carver G, Greene W, Kristiansen K, Meyer E, Pesika N, Rosenberg K, Zeng H (2010) Recent advances in the surface forces apparatus (SFA) technique. Rep Prog Phys 73(3)

    Google Scholar 

  • Kim S, Faghihnejad A, Lee Y, Jho Y, Zeng H, Hwang DS (2015) Cation-pi interaction in DOPA-deficient mussel adhesive protein mfp-1. J Mater Chem B 3(5):738–743

    Article  CAS  Google Scholar 

  • Lee H, Scherer NF, Messersmith PB (2006) Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci USA 103(35):12999–13003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee BP, Messersmith PM, Israelachvili JN, Waite JH (2011) Mussel-inspired adhesives and coatings. Annu Rev Mater Res 41:99–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Zeng H (2016) Marine mussel adhesion and bio-inspired wet adhesives. Biotribology 5:44–51. doi:10.1016/j.biotri.2015.1009.1004

    Article  Google Scholar 

  • Lu QY, Danner E, Waite JH, Israelachvili JN, Zeng HB, Hwang DS (2013) Adhesion of mussel foot proteins to different substrate surfaces. J R Soc Interface 10:20120759, http://dx.doi.org/20120710.20121098/rsif.20122012.20120759

    Article  PubMed  PubMed Central  Google Scholar 

  • Maier GP, Rapp MV, Waite JH, Israelachvili JN, Butler A (2015) Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Science 349(6248):628–632

    Article  CAS  PubMed  Google Scholar 

  • Miller DR, Spahn JE, Waite JH (2015) The staying power of adhesion-associated antioxidant activity in Mytilus californianus. J R Soc Interface 12(111):10.1098/rsif.2015.0614

    Google Scholar 

  • Mirshafian R, Wei W, Israelachvili JN, Waite JH (2016) α, β-Dehydro-dopa. A hidden participant in mussel adhesion. Biochemistry 55(5):743–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morton B (1993) The anatomy of Dreissena polymorpha and the evolution and success of the heteromyarian form in the Dreissenoidea. In: Nalepa TF, Schloesser D (eds) Zebra mussels—biology, impacts, and control. Lewis Publishers, Boca Raton, pp 185–215

    Google Scholar 

  • Nicklisch SC, Waite JH (2012) Mini-review: the role of redox in Dopa-mediated marine adhesion. Biofouling 28(8):865–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrone L, Kumar A, Sutanto CN, Patil NJ, Kannan S, Palaniappan A, Amini S, Zappone B, Verma C, Miserez A (2015) Mussel adhesion is dictated by time-regulated secretion and molecular conformation of mussel adhesive proteins. Nat Commun 6:8737. doi:10.1038/ncomms9737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rees DJ, Hanifi A, Manion J, Gantayet A, Sone ED (2016) Spatial distribution of proteins in the quagga mussel adhesive apparatus. Biofouling 32(2):205–213

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez NRM, Das S, Kaufman Y, Israelachvili JN, Waite JH (2015) Interfacial pH during mussel adhesive plaque formation. Biofouling 31(2):221–227

    Article  PubMed Central  Google Scholar 

  • Rzepecki LM, Waite JH (1993a) The byssus of the zebra mussel, Dreissena polymorpha. I: Morphology and in situ protein processing during maturation. Mol Mar Biol Biotechnol 2(5):255–266

    CAS  PubMed  Google Scholar 

  • Rzepecki LM, Waite JH (1993b) The byssus of the zebra mussel, Dreissena polymorpha. II: Structure and polymorphism of byssal polyphenolic protein families. Mol Mar Biol Biotechnol 2(5):267–279

    CAS  PubMed  Google Scholar 

  • Rzepecki LM, Nagafuchi T, Waite JH (1991) α, β-Dehydro-3.4-dihydroxyphenylalanine derivates: potential sclerotization intermediates in natural composite materials. Arch Biochem Biophys 285:27–36

    Article  CAS  PubMed  Google Scholar 

  • Sagert J, Sun C, Waite JH (2006) Chemical subtleties of the mussel and polychaete holdfasts. In: Smith AM, Callow JA (eds) Biological adhesives. Springer International Publishing, Germany, pp 125–143

    Chapter  Google Scholar 

  • Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ (2004) Metal-mediated crosslinking in the generation of a marine-mussel adhesive. Angew Chem Int Ed 43(4):448–450

    Article  CAS  Google Scholar 

  • Silverman HG, Roberto FF (2007) Understanding marine mussel adhesion. Mar Biotechnol 9(6):661–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverman HG, Roberto FF (2010) Byssus formation in Mytilus. In: von Byern J, Grunwald I (eds) Biological adhesive systems. Springer, Austria, pp 273–282

    Chapter  Google Scholar 

  • Sousa R, Novais A, Costa R, Strayer D (2014) Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735:233–251

    Article  Google Scholar 

  • Stewart RJ, Ransom TC, Hlady V (2011) Natural Underwater Adhesives. J Polym Sci B Polym Phys 49(11):757–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strayer DL (2009) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Front Ecol Environ 7(3):135–141

    Article  Google Scholar 

  • Strupat K, Karas M, Hillenkamp F, Eckerskorn C, Lottspeich F (1994) Matrix-assisted laser-desorption ionization mass-spectrometry of proteins electroblotted after polyacrylamide-gel electrophoresis. Anal Chem 66(4):464–470

    Article  CAS  Google Scholar 

  • Tamarin A, Lewis P, Askey J (1976) Structure and formation of the byssus attachment plaque in Mytilus. J Morph 149:199–221

    Article  CAS  PubMed  Google Scholar 

  • Waite JH (1986) Mussel glue from Mytilus-Californianus conrad—a comparative-study. J Comp Physiol B Biochem Syst Environm Phys 156(4):491–496

    Article  CAS  Google Scholar 

  • Waite JH (1987) Nature's underwater adhesive specialist. Int J Adhes Adhes 7(1):9–14

    Article  CAS  Google Scholar 

  • Waite JH (2002) Adhesion a la moule. Integr Comp Biol 42(6):1172–1180

    Article  CAS  PubMed  Google Scholar 

  • Waite JH, Lichtenegger HC, Stucky GD, Hansma P (2004) Exploring molecular and mechanical gradients in structural bioscaffolds. Biochemistry 43(24):7653–7662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waite JH, Andersen NH, Jewhurst S, Sun CJ (2005) Mussel adhesion: finding the tricks worth mimicking. J Adhes 81(3-4):297–317

    Article  CAS  Google Scholar 

  • Wang CS, Stewart RJ (2013) Multipart copolyelectrolyte adhesive of the sandcastle worm, Phragmatopoma californica (Fewkes): catechol oxidase catalyzed curing through peptidyl-dOPA. Biomacromolecules 14:1607–1617

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Yu J, Broomell C, Israelachvili JN, Waite JH (2013) Hydrophobic enhancement of Dopa-mediated adhesion in a mussel foot protein. J Am Chem Soc 135(1):377–383

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Tan YP, Rodriguez NRM, Yu J, Israelachvili JN, Waite JH (2014) A mussel-derived one component adhesive coacervate. Acta Biomater 10(4):1663–1670

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Yu J, Gebbie MA, Tan YP, Rodriguez NRM, Israelachvili JN, Waite JH (2015) Bridging adhesion of mussel-inspired peptides: role of charge, chain length, and surface type. Langmuir 31(3):1105–1112

    Article  CAS  PubMed  Google Scholar 

  • Wilker JJ (2010) Marine bioinorganic materials: mussels pumping iron. Curr Opin Chem Biol 14(2):276–283

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Faisal M (2008) Putative identification of expressed genes associated with attachment of the zebra mussel (Dreissena polymorpha). Biofouling 24(3):157–161

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto H, Hayakawa T (1982) Synthesis of sequential polypeptides containing L-β-3, 4-dihydroxyphenyl-α-alanine (DOPA) and L-lysine. Biopolymers 21:1137–1151

    Article  CAS  Google Scholar 

  • Yang J, Stuart MAC, Kamperman M (2014) Jack of all trades: versatile catechol crosslinking mechanisms. Chem Soc Rev 43(24):8271–8298

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Wei W, Danner E, Ashley RK, Israelachvili JN, Waite JH (2011a) Mussel protein adhesion depends on interprotein thiol-mediated redox modulation. Nat Chem Biol 7(9):588–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Wei W, Danner E, Israelachvili JN, Waite JH (2011b) Effects of interfacial redox in mussel adhesive protein films on mica. Adv Mater 23(20):2362–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Kan YJ, Rapp M, Danner E, Wei W, Das S, Miller DR, Chen YF, Waite JH, Israelachvili JN (2013a) Adaptive hydrophobic and hydrophilic interactions of mussel foot proteins with organic thin films. Proc Natl Acad Sci USA 110(39):15680–15685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Wei W, Menyo MS, Masic A, Waite JH, Israelachvili JN (2013b) Adhesion of mussel foot protein-3 to TiO2 Surfaces: the effect of pH. Biomacromolecules 14(4):1072–1077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng H, Lu Q, Yan B, Huang J, Li L, Liao Z (2015) Mussel Adhesives. In: Bianco-Peled H, Davidovich-Pinhas M (eds) Bioadhesion and biomimetics: from nature to applications. Pan Stanford Publishing, Singapore, pp 49–84

    Google Scholar 

  • Zhao H, Waite JH (2006) Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem 281(36):26150–26158

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Robertson NB, Jewhurst SA, Waite JH (2006) Probing the adhesive footprints of Mytilus californianus byssus. J Biol Chem 281(16):11090–11096

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I am extremely grateful to a number of talented postdoctoral, graduate, and undergraduate students in my lab, past and present, who have contributed to research efforts in this area. Our work is supported by the National Sciences and Engineering Research Council (NSERC) of Canada and the Canadian Foundation for Innovation (CFI).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eli D. Sone .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sone, E.D. (2016). Interfacial Phenomena in Marine and Freshwater Mussel Adhesion. In: Smith, A. (eds) Biological Adhesives. Springer, Cham. https://doi.org/10.1007/978-3-319-46082-6_6

Download citation

Publish with us

Policies and ethics