Biocalcification in porcelaneous foraminifera

Abstract

Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as the only exception. This phylum has been commonly thought to follow two contrasting models of either “extracellular in situ matrix mineralization” attributed to hyaline rotaliid shells, or “intracellular vesicle crystallization” attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We found that both groups produced calcareous shells via the intravesicular formation of unstable mineral precursors (Mg-rich amorphous calcium carbonate) supplied by endocytosed seawater and deposited in situ as mesocrystals formed at the site of new wall formation within the organic matrix. We did not observe calcification of the needles within the transported vesicles, which challenges the previous model of miliolid mineralization. Hence, Foraminifera utilize less divergent crystallization pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls are therefore created by accumulating and assembling particles of pre-formed liquid amorphous mineral phase within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well-conserved in two clades that represent different chamber formation modes.