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First published online October 16, 2009
Journal of Experimental Biology 212, 3499-3510 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.029884

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Barnacle cement: a polymerization model based on evolutionary concepts

Gary H. Dickinson^1,*, Irving E. Vega², Kathryn J. Wahl³, Beatriz Orihuela¹, Veronica Beyley², Eva N. Rodriguez², Richard K. Everett⁴, Joseph Bonaventura^1,5 and Daniel Rittschof^1,

¹ Duke University Marine Laboratory, Nicholas School of the Environment, Beaufort, NC 28516, USA
² Department of Biology and Protein Mass Spectrometry Facility, College of Natural Sciences, University of Puerto Rico, Rio Piedras Campus, San Juan, PR 00931, USA
³ Chemistry Division, US Naval Research Laboratory, Washington DC 20375, USA
⁴ Materials Science and Technology Division, US Naval Research Laboratory, Washington DC 20375, USA
⁵ Protein Research and Development Center, University of Puerto Rico-Mayagüez Campus, Mayagüez, PR 00681, USA

Author for correspondence (ritt{at}duke.edu)

Accepted 16 July 2009

Enzymes and biochemical mechanisms essential to survival are under extreme selective pressure and are highly conserved through evolutionary time. We applied this evolutionary concept to barnacle cement polymerization, a process critical to barnacle fitness that involves aggregation and cross-linking of proteins. The biochemical mechanisms of cement polymerization remain largely unknown. We hypothesized that this process is biochemically similar to blood clotting, a critical physiological response that is also based on aggregation and cross-linking of proteins. Like key elements of vertebrate and invertebrate blood clotting, barnacle cement polymerization was shown to involve proteolytic activation of enzymes and structural precursors, transglutaminase cross-linking and assembly of fibrous proteins. Proteolytic activation of structural proteins maximizes the potential for bonding interactions with other proteins and with the surface. Transglutaminase cross-linking reinforces cement integrity. Remarkably, epitopes and sequences homologous to bovine trypsin and human transglutaminase were identified in barnacle cement with tandem mass spectrometry and/or western blotting. Akin to blood clotting, the peptides generated during proteolytic activation functioned as signal molecules, linking a molecular level event (protein aggregation) to a behavioral response (barnacle larval settlement). Our results draw attention to a highly conserved protein polymerization mechanism and shed light on a long-standing biochemical puzzle. We suggest that barnacle cement polymerization is a specialized form of wound healing. The polymerization mechanism common between barnacle cement and blood may be a theme for many marine animal glues.

Key words: barnacle cement, bioadhesive, polymerization, coagulation, trypsin-like serine protease, transglutaminase, Balanus amphitrite, biofouling

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