Cement Proteins of the Tube-building Polychaete Phragmatopoma californica

Abstract

The mineralized tube of the sandcastle worm Phragmatopoma californica is made from exogenous mineral particles (sand, shell, etc.) glued together with a cement secreted from the "building organ" on the thorax of the worm. The glue is a cross-linked mixture of three highly polar proteins. The complete sequences of Pc-1 (18 kDa) and Pc-2 (21 kDa) were deduced from cDNAs derived from previously reported peptide sequences (Waite, J. H., Jensen, R., and Morse, D. E. (1992) Biochemistry 31, 5733-5738). Both proteins are basic (pI ϳ10) and exhibit Gly-rich peptide repeats. The consensus repeats in Pc-1 and -2 are VGGYGYGGKK (15 times), and HPAVX-HKALGGYG (eight times), respectively, in which X denotes an intervening nonrepeated sequence and Y is modified to 3,4-dihydroxyphenyl-L-alanine (Dopa). The third protein, Pc-3, was deduced from the cement to be about 80 mol % phosphoserine/ serine, and the cDNA was obtained by exploiting the presence of poly-serine repeats. Pc-3 consists of a family of at least seven variants with 60 -90 mol % serine most of which is phosphorylated in the cement. Pc-1, -2, and -3 contain cysteine some of which reacts to form 5-S-cysteinyl-Dopa cross-links during the setting process.The California sandcastle worm, Phragmatopoma californica (Fewkes), is a premier sand mason (1). In common with other sabellariid polychaetes, it exhibits an almost frenzied diligence in the collection, sorting and placement of sand grains for the construction and repair of its tubular home.3 Although each worm builds primarily the tube in which it resides, a colony of worms can coordinate its efforts to erect massive boulder-like concretions that play a pivotal role in reef ecology (3, 4). The cement used by Phragmatopoma and related sabellariids to bind together grains of sand has been of interest for some time in that it adheres irreversibly to wet mineral surfaces and is used with extraordinary speed and economy. Perhaps 4 -7 "spot welds," each about 100 m in diameter, are used to hold each sand grain (diameter 500 m) in place in the natural concrete (3,5).Phragmatopoma cement consists of proteins and significant levels of phosphate, calcium, and magnesium (6, 7). Two of the cement proteins, Pc-1 and Pc-2, 4 known from an earlier partial characterization (8),resemble the byssal adhesives of mussels (9) in that they are basic and contain 3,4-dihydroxyphenyl-L-alanine (Dopa) (5,7,8). Surprisingly, the abundant phosphate was not found to be associated with mineral but rather with serine residues in the cement (7). Indeed, the cement is dominated by phosphoserine and glycine, which together account for nearly 60 mol % of all the residues detected post-hydrolysis. Since the serine content of Pc-1 and -2 is negligible (8), the existence of a third serine-rich precursor is postulated. The aim of the present research was to identify the serine-rich protein, to obtain full-length sequences of Pc-1 and Pc-2, and to gain some insights into the mechanism of cement solidification. MATERIALS AND METHODSWorm Maintenance for Tub...

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