Biomineralization of CaCO3 in the oceans: Seawater is the calcifying fluid

Abstract

Calcium carbonate precipitation in the ocean is a major process of the global carbon cycle controlling atmospheric CO2 and climate. Almost all the CaCO3 precipitation in the today’s ocean is biological and most organisms that calcify in the ocean bring seawater directly into their privileged space where skeletal precipitation of CaCO3 occurs. The only significant exception to these observations (to the best of our knowledge) are the photosynthetic coccolithophores that transport calcium and bicarbonate ions and calcify intracellularly, also referred to as the transmembrane transport model. All other calcifying invertebrates that were examined: foraminifera, corals, echinoderms, mollusks, sponges and other minor groups, regardless of their mineralogy, precipitate their skeleton directly from seawater. These organisms bring bulk seawater directly to their calcification site with slight modifications to form their calcifying fluid. Seawater contains high concentration of Ca2+ (>10 mM) and considerable concentration of dissolved inorganic carbon (DIC, 2 mM) and is supersaturated for both calcite and aragonite. The seawater calcifying fluid hypothesis is supported by different lines of evidence: 1. The most obvious one is the incorporation of membrane-impermeable fluorescent dyes (calcein and FITC-Dextran) into the skeletons of all these organisms. 2. The skeletons of these marine organisms contain most of the major, minor and trace elements found in seawater including their stable isotopes, with only slight deviations compared to inorganic precipitation of CaCO3 from seawater. 3. Direct in vivo microscopic observations at the calcifying site of corals, foraminifera and echinoderms using cell impermeable fluorescent dyes that show the presence of seawater at the calcification sites. Furthermore, pulse-chase experiments with calcein in these organisms demonstrate the dynamics of seawater supply for calcification is fast enough to support the observed calcification rates (corals and foraminifera). Calcification in marine organisms that transport seawater have excess Ca2+ over CO32- and hence the main modifications of the calcifying seawater are pH and DIC elevation. This is achieved by continuous alkalinity transport into the calcifying seawater in exchange for protons followed by CO2 diffusion into the alkaline calcifying fluid thus building an internal carbon pool. The transporters responsible for the alkalinity increase are most likely Na and K ATPases, while other trace elements (e.g. Li) are leaking through these transporters. Recent experimental studies on the partition of elements in coral and foraminifera skeletons under variable Ca2+ concentrations show clear Rayleigh distillation behavior with increased CO32- concentrations that support the seawater model as opposed to the trans-membrane alternative. Our model explains well why foraminifera and corals are excellent archives for reconstructing past seawater chemistry, improve the reliability of existing proxies and introduce new ones.