Adhesive gland transcriptomics uncovers a diversity of genes involved in glue formation in marine tube-building polychaetes.

Tube-building sabellariid polychaetes are hermatypic organisms capable of forming vast reefs in highly turbulent marine habitats. Sabellariid worms assemble their tube by gluing together siliceous and calcareous clastic particles using a polyelectrolytic biocement. Here, we performed transcriptomic analyses to investigate the genes that are differentially expressed in the parathorax region, which contains the adhesive gland and tissues, from the rest of the body. We found a large number of candidate genes to be involved in the composition and formation of biocement in two species: Sabellaria alveolata and Phragmatopoma caudata. Our results indicate that the glue is likely to be composed by a large diversity of cement-related proteins, including Poly(S), GY-rich, H-repeat and miscellaneous categories. However, sequences divergence and differences in expression profiles between S. alveolata and P. caudata of cement-related proteins may reflect adaptation to the type of substratum used to build their tube, and/or to their habitat (temperate vs tropical, amplitude of pH, salinity …). Related to the L-DOPA metabolic pathways and linked with the genes that were differentially expressed in the parathorax region, we found that tyrosinase and peroxidase gene families may have undergone independent expansion in the two Sabellariidae species investigated. Our data also reinforce the importance of protein modifications in cement formation. Altogether these new genomic resources help to identify novel transcripts encoding for cement-related proteins, but also important enzymes putatively involved in the chemistry of the adhesion process, such as kinases, and may correspond to new targets to develop biomimetic approaches. STATEMENTS OF SIGNIFICANCE: The diversity of bioadhesives elaborated by marine invertebrates is a tremendous source of inspiration to develop biomimetic approaches for biomedical and technical applications. Recent studies on the adhesion system of mussel, barnacle and sea star had highlighted the usefulness of high-throughput RNA sequencing in accelerating the development of biomimetic adhesives. Adhesion in sandcastle worms, which involves catechol and phosphate chemistries, polyelectrolyte complexes, supramolecular architectures, and a coacervation process, is a useful model to develop multipurpose wet adhesives. Using transcriptomic tools, we have explored the diversity of genes encoding for structural and catalytic proteins involved in cement formation of two sandcastle worm species, Sabellaria alveolata and Phragmatopoma caudata. The important genomic resource generated should help to design novel "blue" adhesives.