Integrative Transcriptome and Proteome Analysis of the Tube Foot and Adhesive Secretions of the Sea Urchin Paracentrotus lividus

Abstract

Echinoderms, such as the rock-boring sea urchin Paracentrotus lividus, attach temporarily to surfaces during locomotion using their tube feet. They can attach firmly to any substrate and release from it within seconds through the secretion of unknown molecules. The composition of the adhesive, as well as the releasing secretion, remains largely unknown. This study re-analyzed a differential proteome dataset from Lebesgue et al. by mapping mass spectrometry-derived peptides to a P. lividus de novo transcriptome generated in this study. This resulted in a drastic increase in mapped proteins in comparison to the previous publication. The data were subsequently combined with a differential RNAseq approach to identify potential adhesion candidate genes. A gene expression analysis of 59 transcripts using whole mount in situ hybridization led to the identification of 16 transcripts potentially involved in bioadhesion. In the future these data could be useful for the production of synthetic reversible adhesives for industrial and medical purposes.

Omics‐based molecular analyses of adhesion by aquatic invertebrates

“…Recently, it was confirmed that attachment of M. lignano relies on two large proteins expressed in the adhesive glands (Mlig-ap1 and Mlig-ap2; Wunderer et al, 2019). Similar transcriptomics, proteomics and expression analyses were also applied to the proseriate flatworm Minona ileanae, where nine transcripts specific to the adhesive organs were identified (Pjeta et al, 2019). Six transcripts had similar conserved domain architecture and were rich in repetitive motifs previously observed in adhesive proteins Mlig-ap1 and Mlig-ap2 of M. lignano.…”

“…This 108 kDa protein presents phosphorylated and glycosylated isoforms and contains six discoidin domains (similar to Sfp1) that can bind molecules bearing galactose and N-acetylglucosamine residues (Santos et al, 2013;Lebesgue et al, 2016;Toubarro et al, 2016). Recently, these proteomic data were re-mapped to a new P. lividus tube foot transcriptome (Pjeta et al, 2020). This resulted in a 60% increase in the mapped disc and stem peptides, accompanied by a 71% increase in the number of identified proteins.…”

“…Wholemount in situ hybridisation (WISH) was performed for 59 selected transcripts, pinpointing 16 transcripts potentially involved in sea urchin adhesion. Of these, six transcripts were identified as nectin, alpha-tectorin, uncharacterised protein, myeloperoxidase, neurogenic locus notch homolog protein and alpha-macroglobulin, but simultaneously shared orthology with putative adhesion-related genes from sea stars (Lengerer et al, 2019;Pjeta et al, 2020). The advantages of 'omics and, more specifically, the advantages of bespoke, comparative 'omics analyses (Fig.…”

“…Interestingly, a region comprising tandem repeats of a glycine, arginine and lysine low-complexity motif, which encompassed about twothirds of M. lignano Mlig-ap1, was identified in a M. ileanae adhesive protein (Mile-ap3). Long-read genomic DNA sequencing using Oxford Nanopore Technology identified that four of these nine transcripts were part of two larger genes (Pjeta et al, 2019).…”

Sea stars generate downforce to stay attached to surfaces

“…The preceding discussion suggests that the pentaradial body shape and morphological plasticity exhibited by sea stars enable them to better resist hydrodynamic loads. Sea urchins are often found in the same environment as sea stars and have a comparable biological adhesion mechanism 25 – 27 . Yet it is unlikely that the spiny spheroidal geometry typical of sea urchins leads to downforce generation.…”