Biomineralization: Integrating mechanism and evolutionary history

Abstract

Calcium carbonate (CaCO 3 ) biomineralizing organisms have played major roles in the history of life and the global carbon cycle during the past 541 Ma. Both marine diversification and mass extinctions reflect physiological responses to environmental changes through time. An integrated understanding of carbonate biomineralization is necessary to illuminate this evolutionary record and to understand how modern organisms will respond to 21st century global change. Biomineralization evolved independently but convergently across phyla, suggesting a unity of mechanism that transcends biological differences. In this review, we combine CaCO 3 skeleton formation mechanisms with constraints from evolutionary history, omics, and a meta-analysis of isotopic data to develop a plausible model for CaCO 3 biomineralization applicable to all phyla. The model provides a framework for understanding the environmental sensitivity of marine calcifiers, past mass extinctions, and resilience in 21st century acidifying oceans. Thus, it frames questions about the past, present, and future of CaCO 3 biomineralizing organisms.

Proteomic Profiling of Black Coral (Antipatharia) Skeleton Reveals Hundreds of Skeleton-Associated Proteins Across Two Taxa

“…Further, an acidic chitin binding protein appears to be involved in the precipitation of calcium phosphate and then calcium carbonate in crustacean teeth (Tynyakov et al, 2015). Our results suggest that acidic proteins may be involved in black coral chitinous skeleton development; however, despite likely sharing conserved biomineralizationrelated genes with stony corals (review by Gilbert et al, 2022), black coral acidic proteins are perhaps not as central to the process as they appear to be in allowing stony corals biomineralize (Mass et al, 2013) and to counter the effects of ocean acidification (e.g., Drake et al, 2017).…”

Stylasterid corals build aragonite skeletons in undersaturated water despite low pH at the site of calcification

“…( 4 ); Methods; e.g. 16 , 17 ), these δ 11 B results suggest no modification of internal seawater pH in stylasterids. Furthermore, application of a physiochemical biocalcification model based on scleractinian corals by DeCarlo et al 37 (Methods), the high B/Ca values in our aragonitic stylasterids imply low [CO 3 2− ] in the CF (average 110 µmol/kg excluding S. ibericus ) similar to external seawater (average 90 µmol/kg).…”

“… 13 – 15 ). Skeletal geochemistry is therefore the go-to approach for understanding the mineralisation process, with the boron isotopic composition (δ 11 B; 11 B/ 10 B ratio relative to the standard NIST SRM 951 in ‰) of marine carbonates shown to be a powerful tool to assess pH at the site of calcification 16 , 17 .…”

Brachiopod and mollusc biomineralisation is a conserved process that was lost in the phoronid-bryozoan stem lineage

“…Figs. [1][2][3][4][5][6] were used to assess orthology of the lophophorate genes of interest. New sequences obtained and identified in this study were uploaded to GenBank (accession numbers ON868422 to ON868458).…”

“…While the last common ancestor of the two groups was likely weakly mineralised at most [8], mollusc shell formation does have similarities to that of brachiopods [40,42,47,48], and mounting evidence suggests that the two groups may share some of the underlying genetic architecture required for biomineralisation [48][49][50][51][52][53]. A conserved 'biomineralisation toolkit' has been proposed by several authors [1,8,27,[54][55][56][57][58][59], possibly encompassing not only molluscs, brachiopods and other lophotrochozoans but all bilaterians. This idea implies that while structurally analogous, the formation of shells in brachiopods and molluscs builds on a complement of orthologous genes, and has support from genomics- [49,51,57] and proteomicsbased studies [53].…”