Rapid evolution of pearl oyster shell matrix proteins with repetitive, low-complexity domains

Abstract

The lysine (K)-rich mantle protein (KRMP) and shematrin protein families are unique to the organic matrices of pearl oyster shells. Similar to other proteins that are constituents of tough, extracellular structures, such as spider silk, shematrins and KRMPs, contain repetitive, low-complexity domains (RLCDs). Comprehensive analysis of available gene sequences in three species of pearl oyster using BLAST and hidden Markov models reveal that both gene families have large memberships in these species. The shematrin gene family expanded before the speciation of these oysters, leading to a minimum of eight orthology groups. By contrast, KRMPs expanded primarily after speciation leading to species-specific gene repertoires. Regardless of their evolutionary history, the rapid evolution of shematrins and KRMPs appears to be the result of the intrinsic instability of repetitive sequences encoding the RLCDs, and the gain, loss and shuffling of other motifs. This mode of molecular evolution is likely to contribute to structural characteristics and evolvability of the pearl oyster shell. Based on these observations, we infer that analogous RLCD proteins throughout the animal kingdom also have the capacity to rapidly evolve and as a result change their structural properties.

Deep conservation of bivalve nacre proteins highlighted by shell matrix proteomics of the Unionoida Elliptio complanata and Villosa lienosa

“…In the present case, in spite of overall sequence similarities observed within these several RLCD protein categories identified in different models, it remains difficult to clearly outline whether they are true homologues considering the limitation of standard Blastp tools for low-complexity sequences, the fast rate of evolution of these domains [41,43] and that fortuitous low-complexity sequence similarities can be obtained between non-homologous SMPs that have evolved completely independently.…”

Investigation of gene family evolution and the molecular basis of shell formation in molluscs

“…By directly comparing the transcriptome of nacre-forming cells in a bivalve and gastropod, it has been revealed that there are tremendous differences in these secretomes, with less than 15% of secreted SMPs being shared (Jackson et al 2010). These differences also extend to comparisons between nacre-and prism-associated SMPs of two closely related pearl oyster species (P. maxima and P. margaritifera), and to comparisons within biomineralising gene families (shematrin and KRMP) across Pinctada species (Marie et al 2012b, McDougall et al 2013a, lending support to the supposition that mollusc shell formation is primarily controlled by rapidly evolving genes (Jackson et al 2006). …”

“…However, the true function of these RLCD-containing proteins in molluscan biomineralisation is still unknown because the behaviour of these motifs in vivo is likely to be affected by multiple factors and in vitro studies cannot inform us about the processes that occur within the complex shell environment. Nevertheless, given the high proportion of RLCD-containing proteins present in a wide range of shell-forming proteomes and transcriptomes (Jackson et al 2010, Marie et al 2010a, McDougall et al 2013a, Werner et al 2013, it is clear that these proteins are important shell components.…”

“…These domains exhibit little diversity in their amino acid composition, comprising few different residues or just one, and are either loosely clustered, irregularly spaced, or periodic (Miyamoto et al 1996, Shen et al 1997, Sudo et al 1997, Sarashina and Endo 1998, Samata et al 1999, Yano et al 2006, Zhang et al 2006b, Suzuki et al 2009, Jackson et al 2010, Marie et al 2010a, Montagnani et al 2011, Fang et al 2012, Marie et al 2012a, McDougall et al 2013a, Werner et al 2013. Often RLCDs are found in the terminal regions of SMPs and are thought to be structurally unstable and intrinsically disordered domains able to adopt a specific structure only upon binding to a ligand, such as crystal surface (Tompa 2002, Evans 2008, Tompa 2012).…”

“…Although hundreds of SMPs are expected to contribute to shell formation, little is known about their evolutionary histories, with only few studies conducted on metazoan biomineralisation-related genes (Sarashina et al 2006, Jackson et al 2010, Marie et al 2011a, Miyamoto 2012, Werner et al 2013) and molluscan-specific gene families (Isowa et al 2012, McDougall et al 2013a, Song et al 2014 Despite these difficulties, studies have revealed that SMP gene families, such as the shematrins and KRMPs, have undergone rapid and independent lineage-specific gene expansions and extensive sequence divergence and speciation events (McDougall et al 2013a), supporting the proposition that SMPs are fast evolving (Jackson et al 2006). …”