Weaving of biomineralization framework in rotaliid foraminifera: Implications for paleoenvironmental reconstructions

Abstract

Abstract. Foraminifera are commonly used to reconstruct paleoenvironmental conditions based on the taxonomical composition, as well as elemental and/or isotopic signatures of their calcareous tests. A major problem, often referred to as the 'vital effect', is that such geochemical signatures stored in inorganic calcium carbonates differ greatly under the same environmental conditions. This effect was previously explained by proportional contributions from passive vs active ion 5 transport patterns, but their details are still investigated. In this study, the functional role of pseudopodial structures during chamber formation is elucidated by detailed observation of Ammonia beccarii (Linnaeus) using a time-lapse optical imaging system and high-resolution electron microscopy. For the first time, we document triple organic layers sandwiching carbonate precipitation sites. The three major organic layers (outer organic layer, primary organic sheet, and inner organic layer) are formed by an initial framework of pseudopodia overlaid with further layer-like pseudopodia. The POS seems to facilitate 10 early calcium carbonate nucleation, then entrapped by double precipitation sites. We further show that calcification starts when outer/inner organic layers still reveal tiny gaps (holes within the framework) that may serve as pathways for passive ion exchange (e.g., Mg 2+ ) between seawater and the confined precipitation space. Nevertheless, the majority of wall thickening occurs when the precipitation site is completely isolated from seawater that implicates of active ion exchange.This may explain the differences in Mg/Ca ratios in early and later stages of calcification observed in previous studies. Our 15 study resolves a key 'missing piece' in understanding foraminiferal calcification. The 'vital effect' is directly linked to spatio-temporal organization of the 'biomineralization sandwich' controlled by the three major organic layers. This study exemplifies the importance of culture experiments and in-depth observations of living organisms in order to interpret and calibrate biogeochemical proxies.

Form and function of F-actin during biomineralization revealed from live experiments on foraminifera

“…This interpretation agrees with observations of membrane probes labeling thin ectoplasmic layer that most likely isolated the crystals from the surrounding water during mineralization ( 32 ). Recent ultrastructural SEM investigations also document another globothalamean species ( Ammonia ) that revealed isolation of calcification sites by two external organic layers, i.e., inner and outer organic layers, entrapping the POS ( 41 , 42 ). These external layers, actively involved in calcification during the chamber formation, truly represent inner and outer lamellipodial structures identified in A. lessonii .…”

“…These external layers, actively involved in calcification during the chamber formation, truly represent inner and outer lamellipodial structures identified in A. lessonii . Authors suggest an early “leakage” of seawater through tiny holes of outer/inner organic layers at the onset of mineralization ( 42 ). Further research is required to investigate this phenomenon and its consequences.…”

Coupled Ca and inorganic carbon uptake suggested by magnesium and sulfur incorporation in foraminiferal calcite

“…leakage, initial seawater enclosed at the site of calcification or seawater endocytosis), while SO 4 2would not be transported by the Cachannels or -pumps. Only prior to or at the first stages of chamber formation, when the membrane is perhaps not fully closed (Nagai et al, 2018) and the fluid in the site of calcification (SOC) resembles seawater, SO 4 2is incorporated due to the relatively Biogeosciences Discuss., https://doi.org/10.5194/bg-2018-481 Manuscript under review for journal Biogeosciences Discussion started: 12 December 2018 c Author(s) 2018. CC BY 4.0 License.…”

“…In perforate hyaline species, studies have shown that the site of calcification is separated from the surrounding seawater by a protective envelope. Although observations for Ammonia suggest this envelope might not be closed at the start of calcification (Nagai et al, 2018), the carbonate chemistry at the site of calcification is proposed to be controlled by the foraminifer and e.g. characterized by a high internal and low external pH Toyofuku et al, 2017), as well as the chemistry of the calcification fluid itself .…”