Intravesicular Formation of Unstable Mineral Precursors Drives Biocalcification in Porcelaneous Foraminifera

Core Concepts

Foraminifera utilize intravesicular formation of unstable mineral precursors (Mg-rich amorphous calcium carbonates) supplied by endocytosed seawater to deposit calcite mesocrystals within the extracellular organic matrix, challenging the previous model of miliolid mineralization.

Abstract

The study examines the biomineralization process in the miliolid foraminifer Pseudolachlanella eburnea, challenging the widely accepted model of miliolid shell formation.
Key insights:

In vivo experiments using fluorescent dyes revealed the presence of seawater-containing vesicles and acidic vesicles within the cytosol, indicating the uptake of seawater via endocytosis and the potential role of pH regulation.
SEM-EDS analysis showed that the cytoplasm is enriched in Mg and Ca, while the shell is strongly enriched in Ca, suggesting the intravesicular formation of Mg-rich amorphous calcium carbonate (Mg-ACC) as a precursor for calcite precipitation.
The shell wall is formed by the accumulation and assembly of Mg-ACC particles within the extracellular organic matrix, rather than the agglutination of pre-formed calcite needles as previously proposed.
The gradual change in shell appearance from transparent to opaque during calcification is explained by the in situ precipitation of calcite mesocrystals within the organic matrix, rather than the deposition of pre-formed needles.
The results suggest that miliolid foraminifera utilize a biomineralization pathway similar to that of rotaliid foraminifera, involving the intravesicular formation of unstable mineral precursors and their subsequent deposition within the extracellular organic matrix.

Stats

Mg and Ca contents in the cytoplasm are much higher than in the shell, as detected by SEM-EDS analysis.
The newly formed chamber wall changes appearance from completely transparent to milky and opaque during calcification.

Quotes

"Our new FE-SEM data challenge the current understanding of the biomineralization of miliolid foraminifera and such a significant divergence of biomineralization pathways within the Foraminifera."
"Mesocrystalline chamber walls are therefore apparently 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."

Key Insights Distilled From

Biocalcification in porcelaneous foraminifera

by Dubicka,Z., ... at www.biorxiv.org 10-03-2023

https://www.biorxiv.org/content/10.1101/2023.10.02.560476v2

Deeper Inquiries

How do the biomineralization pathways in miliolid and rotaliid foraminifera differ in terms of the specific mechanisms and factors involved in the precipitation and transformation of the mineral precursors?

In miliolid foraminifera, the biomineralization pathway involves the intravesicular formation of unstable mineral precursors, specifically Mg-rich amorphous calcium carbonates (Mg-ACCs). These precursors are supplied by endocytosed seawater and deposited at the site of new wall formation within the organic matrix. The precipitation of high-Mg calcitic mesocrystals takes place in situ, forming a dense, chaotic meshwork of needle-like crystallites. On the other hand, in rotaliid foraminifera, the biomineralization pathway traditionally involved the mineralization of the extracellular matrix. However, recent studies have shown that rotaliids also utilize Mg-ACCs and follow a similar mechanism of intravesicular formation of mineral precursors as seen in miliolids. This challenges the previous understanding of distinct biomineralization pathways between these two groups of foraminifera.

What are the potential implications of the shared intravesicular formation of unstable mineral precursors for the evolutionary history and diversification of foraminifera?

The shared intravesicular formation of unstable mineral precursors, particularly Mg-ACCs, in both miliolid and rotaliid foraminifera suggests a common evolutionary origin or convergence in biomineralization strategies within the phylum Foraminifera. This shared mechanism implies that the utilization of Mg-ACCs for shell formation may have evolved early in the evolutionary history of foraminifera and has been conserved over time. The presence of similar biomineralization pathways in distantly related foraminiferal groups indicates the importance of this strategy in the success and diversification of foraminifera as efficient marine calcifiers. Understanding the evolutionary implications of shared biomineralization pathways can provide insights into the adaptive strategies that have contributed to the ecological success and radiation of foraminifera in marine environments.

Could the insights from foraminiferal biomineralization be applied to develop novel biomimetic materials or inform our understanding of other biomineralization processes in marine organisms?

The insights gained from studying foraminiferal biomineralization, particularly the formation of Mg-ACCs and mesocrystalline structures, have the potential to inspire the development of novel biomimetic materials with unique properties. By understanding the specific mechanisms and factors involved in foraminiferal shell formation, researchers can mimic these processes to create bioinspired materials for various applications, such as in biomedicine, materials science, and environmental engineering. Additionally, the study of foraminiferal biomineralization can inform our understanding of other biomineralization processes in marine organisms, shedding light on the diverse strategies employed by different species to produce mineralized structures. This comparative approach can enhance our knowledge of biomineralization across taxa and ecosystems, leading to valuable insights for biomimetic design and ecological research.