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Abstract
Minerals are formed by organisms in all of the kingdoms of life. Mineral formation pathways all involve uptake of ions from the environment, transport of ions by cells, sometimes temporary storage, and ultimately deposition in or outside of the cells. Even though the details of how all this is achieved vary enormously, all pathways need to respect both the chemical limitations of ion manipulation, as well as the many "housekeeping" roles of ions in cell functioning. Here we provide a chemical perspective on the biological pathways of biomineralization. Our approach is to compare and contrast the ion pathways involving calcium, phosphate, and carbonate in three very different organisms: the enormously abundant unicellular marine coccolithophores, the well investigated sea urchin larval model for single crystal formation, and the complex pathways used by vertebrates to form their bones. The comparison highlights both common and unique processes. Significantly, phosphate is involved in regulating calcium carbonate deposition and carbonate is involved in regulating calcium phosphate deposition. One often overlooked commonality is that, from uptake to deposition, the solutions involved are usually supersaturated. This therefore requires not only avoiding mineral deposition where it is not needed but also exploiting this saturated state to produce unstable mineral precursors that can be conveniently stored, redissolved, and manipulated into diverse shapes and upon deposition transformed into more ordered and hence often functional final deposits.
Figure 1. Formation of
coccoliths. (A,B) SEM images of Coccolithus
braarudii coccoliths. The diploid life stage forms intricate
crystal morphologies (A), while the haploid stage forms simple rhombohedral
crystals (B). (C–F) Cellular anatomy of Pleurochrysis
carterae. (C, D) Sections in fixed cells show in (C) the
various cell organelles (Chl., chloroplast; Nu., nucleus; magenta
arrowheads indicate coccolith vesicles), and a high magnification
image shows in (D) a coccolith vesicle (blue arrowheads indicate the
crystals, yellow arrowhead indicates the organic base plate). Reprinted
with permission from ref (22). Copyright 2020 Elsevier. (E) 3D rendering of a cryo-fixed
cell. The inset shows the vacuole (light brown) filled with Ca–P-rich
bodies (red) and coccoliths (blue). (F) 3D rendering of a live cell
using confocal microscopy, showing several dense intracellular pools
stained with DAPI (red); chloroplasts are in green. Reprinted with
permission from ref (18). Copyright 2021 Wiley-VCH GmbH.
Figure 2. Mineral deposition process
in sea urchin larvae. (A) Light micrographs
of a live larva of the sea urchin Paracentrotus lividus taken 41 h after fertilization (hpf) (top image); image at the bottom:
the same larva observed under polarized light, showing the crystalline
nature of the spicules. (B) SEM micrograph of an isolated spicule
from Litechinus pictus larva. The spicule is pseudocolored
yellow to facilitate observation. (C) Confocal fluorescence image
of a 46hpf larva developed continuously in calcein-labeled seawater.
Note that the spicule (S) is fully labeled. Many intracellular vesicles
are also fluorescent, indicating uptake by endocytosis of seawater.
(D) Cryo-FIB-SEM micrograph of a high-pressure frozen 40hpf larva.
The cyan vesicle is open toward the body cavity (blastocoel), which
is filled with a seawater-like solution. BF, blastocoel fluid; CM,
cell membrane; N, nucleus. (E) Segmentation of cryo-FIB-SEM serial
milling and block face imaging stack acquired from 40hpf high-pressure
frozen larva. The segmentation shows the syncytium enveloping the
spicule. A vesicle (green arrow) is depositing onto the growing spicule.
Reprinted and modified with permission from (41). Copyright 2016 Elsevier.
(F) Segmentation of cryo-soft X-ray tomography of a PMC taken from
36hpf larva. The colored particles are Ca-rich particles. Cytoplasm
and other cellular vesicles and organelles are gray.
Figure 3. (A) SEM image
of fractured baboon tibia after removal of the organic
matrix using sodium hypochlorite. Note the plate-shaped crystals organized
in layers. (B) TEM image of an isolated mineralized collagen fibril
extracted mechanically from turkey tendon. The banding is due to the
presence of more plate-shaped crystals in the gap region of the collagen
fibril as compared to the overlap region. (C) Cryo-SEM image of the
fracture surface of an embryonic chicken bone showing in green the
distribution of mineral (based on the BSE image of the same area).
Note the presence of vesicles containing mineral particles inside
the cell (arrows).
Figure 4. Schematic illustration showing the three common processes that
make up ion pathways in the biomineralization of coccolithophores,
sea urchin larvae, and vertebrate bone. These pathways involve ion
uptake, cellular manipulation and deposition of the mature mineral
phase. The Y-axis shows the approximate calcium concentration
ranges in which these three processes operate. The solid lines indicate
known processes and dotted lines indicate putative ones. Question
marks highlight yet uncharacterized stages in the pathway. Note the
enormous calcium concentration range for mineralizing cells. Irrespective
of whether the mature mineral phase is a carbonate or phosphate mineral,
the ion pathways all involve calcium, carbonate and phosphate as is
schematically illustrated by the blend of colors for the different
ions.
