Species-specific shells: Chitin synthases and cell mechanics in molluscs

Abstract

Abstract. The size, morphology and species-specific texture of mollusc shell biominerals is one of the unresolved questions in nature. In search of molecular control principles, chitin has been identified by Weiner and Traub (FEBS Lett. 1980, 111 : 311-316) as one of the organic compounds with a defined co-organization with mineral phases. Chitin fibers can be aligned with certain mineralogical axes of crystalline calcium carbonate in a speciesspecific manner. These original observations motivated the functional characterization of chitin forming enzymes in molluscs. The full-length cDNA cloning of mollusc chitin synthases identified unique myosin domains as part of the biological control system. The potential impact of molecular motors and other conserved domains of these complex transmembrane enzymes on the evolution of shell biomineralization is investigated and discussed in this article. Chitin in organisms Chitin in extracellular matrices of cellsIn the end of the 19th century, there was a hot debate regarding the chemical nature of chitin. It lasted until acetylated glucosamine was found in alkaline melts of the carapace of diverse arthropods in contrast to tunicate cellulose [1], and "mycosin" of fungi in contrast to "fungal cellulose" (reviewed by [2]). Today, fungi are well accepted as one of the most prominent groups of eukaryotic organisms which contain chitin as part of their extracellular matrix [3]. Since chitin is usually associated with proteins, complex carbohydrates and sometimes mineral phases, it remains a challenge until today to characterize the diversity of cell walls and integuments in both, uni-and multicellular organisms [4][5][6][7][8][9]. One of the best examples for naturally pure chitin are cell wall appendices of diatoms [10,11], and some enzymes involved in their formation have recently been identified [12,13]. As originally determined by fiber diffraction studies [14-17], three major modifications of chitin are distinguished: a-, b-, and g-chitin [18,19], which differ from each other by the arrangement and molar fractions of differently oriented poly-N-acetylated linear b(1!4) glucosamine (i.e. chitobiose homopolymer, Fig. 1) backbones. They assemble into fiber crystals which are stabilized by H-bonds in either two or three dimensions [4,20,21]. Squids such as the European Squid Loligo vulgaris or the Humboldt squid Dosidicus gigas, which are members of the molluscan class Cephalopoda, perform the biosynthesis of different chitin polymorphs in a tissuespecific manner. The chitinous organs are associated with different sets of proteins [22]. The N-acetyl-glucosamine (GlcNAc) chains are assembled into fibrils and hierarchical structures in order to accomodate specific functions such as mechanical stiffness and strength [23,24]. This is important for the functional design, e.g. of insect exoskeletons and additional functions such as structural colours and adhesive micro-pillar appendages [25,26].A major achievement is the abundant information regarding primary structures of enzyme...

Mimivirus Fibrils Are Important for Viral Attachment to the Microbial World by a Diverse Glycoside Interaction Repertoire

“…Chitin is present in the cell walls of fungi, forming a thin structure covered by a dense mannose layer (22). Several invertebrates have chitin in their structures, such as the exoskeletons of arthropods (23) and mollusk shells (24). It was verified that mimivirus indeed has an attraction for both of these polymers, similar to its attraction for the monomers making up the polymers.…”

Negative Curvature and Control of Excitable Biological Media

“…Conclusively we can say that mechano-sensory response phenomena are shared by other biological systems, where similar or even more pronounced functional dependencies can be found, as the stress sensitivity to the extracellular matrix guides developmental processes of single cells and tissues [43,44,[128][129][130]]. An interesting example, which is still not well understood, is the biomineralization process of calcium carbonates, as found in many invertebrate biominerals such as alveolar plates of ciliates (single-cell eukaryotic micro-organism) [131] and mollusk shells.…”

“…The latter in particular is still not understood in terms of mechano-sensory response to the extremely hard shell (∼GPa). A soft tissue (∼kPa) controls the formation of a fine textured 3D structure (polysaccharide-containing ECM) into which mineral is deposited [130], mediated by local transmembrane proteins and myosin motor domains [129]. Mechanical sensing has been suggested to include a myosin chitin synthase with direct cytoskeletal interaction [132], similar as actin-myosin mechanosensing feedback found in vertebrate cardiac cells.…”

Real-time monitoring of calcium carbonate and cationic peptide deposition on carboxylate-SAM using a microfluidic SAW biosensor

“…Molecular and phylogenetic investigations report that the differences between the assemblies of shell proteins from one species to another species can be tremendous [14–16]. This observation suggests that multiple interactions between the proteins are fine-tuned in relationship to the forming mineral phases [17–20]. …”

“…We also investigated the two cationic peptides ES9 (sequence, N→C: EEKKKKKES) and AS8 (sequence, N→C: AKKKKKAS) [46]. The ES9 peptide is derived from E22, one of four major extracellular loops of an enzyme involved in biomineralization [20,47]. Previous experiments suggest that self-assembly of E22 is fine-tuned in accordance with pH changes that may occur as a function of the mineral precipitation and dissolution [48].…”