The Lingula genome provides insights into brachiopod evolution and the origin of phosphate biomineralization

Abstract

The evolutionary origins of lingulid brachiopods and their calcium phosphate shells have been obscure. Here we decode the 425-Mb genome of Lingula anatina to gain insights into brachiopod evolution. Comprehensive phylogenomic analyses place Lingula close to molluscs, but distant from annelids. The Lingula gene number has increased to ∼34,000 by extensive expansion of gene families. Although Lingula and vertebrates have superficially similar hard tissue components, our genomic, transcriptomic and proteomic analyses show that Lingula lacks genes involved in bone formation, indicating an independent origin of their phosphate biominerals. Several genes involved in Lingula shell formation are shared by molluscs. However, Lingula has independently undergone domain combinations to produce shell matrix collagens with EGF domains and carries lineage-specific shell matrix proteins. Gene family expansion, domain shuffling and co-option of genes appear to be the genomic background of Lingula's unique biomineralization. This Lingula genome provides resources for further studies of lophotrochozoan evolution.

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Its compact size is related to short intergenic regions and introns, comparable to the situation observed in vertebrate Hox clusters (23). The order and orientation of the Hox genes in T. transversa are preserved and more organized compared with the Hox cluster reported for the brachiopod L. anatina, which exhibits a genomic rearrangement that places a portion of the cluster upstream of lab and in reverse orientation (69). Indeed, the split Hox clusters reported so far in lophotrochozoan taxa exhibit multiple different conformations, indicating that lineage-specific genomic events have shaped Hox gene clusters in Spiralia.…”

“…A degenerate-primer screening for Hox genes reported the presence of Lox2 and Lox4 in L. anatina (15). Blastn searches against the sequenced L. anatina genome only confirmed the presence of Lox4, in the same scaffold as Post1 and Post2, although genome annotation pipelines failed to predict this gene (69). The low contiguity of the draft genome assembly of N. anomala hampered the recovery of genomic linkages between the identified Hox genes.…”

“…In H. asinina, lab and Post2 also are related to shell formation (49). In brachiopods, Dfd is associated with the adult shell in L. anatina (69); however, during embryogenesis of T. transversa and N. anomala, only Scr and Antp are expressed in the shell fields, and lab and Post1 are not; here lab and Post1 are expressed in the chaetae sacs. These properties could support the homology of the chitin network formed at the onset of brachiopod and mollusk shell fields.…”

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

“…The brachiopod shell proteomes, retrieved from the CaCO 3 shell of Magellania venosa [58] and the CaPO 3 one of Lingula anatina [59], respectively, exhibit many similarities to those of molluscs in their respective protein and functional domain compositions. The list of shared domains comprises potentially key contributors of shell formation processes, such as D-, A-and G-rich, VWA, EGF, CCP, peroxidase, tyrosinase, chitinase, CA, KU, A2M and CBD2.…”

“…The list of shared domains comprises potentially key contributors of shell formation processes, such as D-, A-and G-rich, VWA, EGF, CCP, peroxidase, tyrosinase, chitinase, CA, KU, A2M and CBD2. Furthermore, Luo and co-workers [59] noticed also that genes shared between Lingula and molluscs, such as calcium-dependent protein kinase and chitin synthase, exhibit high expression in larvae and mantle, indicating that they may also be involved in brachiopod shell formation. Taken together, these results indicate that a conserved molecular machinery exists for shell biomineralization in brachiopods and molluscs.…”