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Manganese incorporation into mussel shells elucidated using X-ray emission spectroscopy


The carbonate shell of freshwater bivalves records changes in the surrounding water as it grows. In this way, bivalves created an archive of environmental changes during periods that predate our instrumental data records. A team of scientists from Argentina, Australia, Austria and the ESRF used state-of-the-art X-ray emission spectroscopy to study the chemical state of manganese in freshwater mussel shells and found an unusual structure that provides insight into the biogenic incorporation of manganese into shells.

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Climate change is a complex issue that is important for the fate of mankind. To better understand the behaviour of the Earth’s atmosphere and oceans, paleoclimatologists investigate the climate of the past using proxies such as the annual changes in ice cores, tree rings, lake sediments and animal skeletons. Mollusc shells archive information about the paleoclimate by incorporation of elements such as strontium, magnesium, barium and manganese. Manganese is at the centre of photocatalytic water oxidation in algae and its presence can thus be directly related to the chlorophyll concentration in freshwater bodies. However, debate continues as to what degree the Mn concentration in bivalve shells reflects the chlorophyll concentration of the surrounding water, because the mechanism of manganese incorporation into the shell is under debate. An important prerequisite to decode the bivalve-proxy archive is therefore to understand thoroughly how these animals form their carbonate shells. This biomineralisation process, however, turns out to be surprisingly complex.

Uptake of Mn may vary significantly depending on the atomic structure of the carbonate. There are two important structural modifications in this context, aragonite and calcite, which are illustrated in Figure 1. In aragonite, the central Ca site is nine-fold coordinated by oxygen whereas it is octahedrally coordinated in calcite.

Schematic crystal structure of the CaCO3 polymorphs aragonite and calcite.

Figure 1. Schematic crystal structure of the CaCO3 polymorphs aragonite and calcite. Aragonite (a) has a crystal structure with orthorhombic symmetry (space group Pnma) where the Ca (green) site is nine-fold coordinated by O with site symmetry m, as shown in (b). In contrast, the crystal structure of calcite (c) is trigonal, space group R-3c. In this case, calcium is octahedrally coordinated by O with site symmetry 32 (d).

The difference in local coordination is important because Mn is taken up into these crystal structures by replacing Ca. While this can be readily achieved for calcite, it is virtually impossible for aragonite. Yet bivalves with aragonitic shells manage to incorporate Mn in concentrations that are orders of magnitude larger than those achievable in non-biogenic counterparts.

To clarify the configuration of the Mn 3d valence shell in the bivalve shell aragonite [1], spin-resolved X-ray absorption (XAS) and X-ray emission spectroscopy (XES) were performed at beamline ID26 and results were compared with those of calcite. These two spectroscopic methods are sensitive probes for the valence shell configuration of manganese as they depend strongly on the oxidation state and the occupation of the different valence orbitals. For the bivalve shells, the spin-resolved XAS and the Mn Kβ-main lines were all found to be identical within experimental error, identifying Mn2+ in a 3d5 high-spin state [2].

The valence-to-core XES line shapes of all of the shell materials studied also coincide within experimental error (Figure 2a). This implies that the chemical environment of Mn, i.e. the coordination symmetry and the type of ligand, in the samples is the same. The key result of the present study is presented in Figure 2b, which further reveals that the valence-to-core line shapes of the bivalve materials are identical to the calcite and rhodochrosite (MnCO3 with calcite coordination, Figure 1, c and d) reference samples within experimental error. Manganese in the aragonitic biominerals formed by freshwater bivalves is therefore, in all cases studied, coordinated locally by an octahedron of six oxygen atoms belonging to six different CO3 groups. The global aragonite structure of the biominerals (where the Ca2+ is surrounded by nine nearest-neighbour oxygen atoms) is therefore altered locally around the Mn-sites in such a way that a calcite-like octahedral coordination is established (cf. Figure 1).

Mn valence-to-core X-ray emission.

Figure 2. Mn valence-to-core X-ray emission. (a) Extended view of the bivalve Kβ X-ray emission, including the weak valence emission satellite at high emission energies (inset). Comparison of the bivalve data (averaged) to different Mn-bearing carbonate (b) and oxide (c) reference samples. The lineshape of the bivalve average spectrum is identical to that of Mn-doped calcite and rhodochrosite (MoCO3).

Hence, our results show that, although the global structure of the shell material corresponds to aragonite, the local structure around Mn is altered to an octahedral coordination by the oxygen ligands.

While the formation of the carbonate shell was presumed similar to carbonates crystallised by an inorganic chemical process, it has become increasingly clear that calcifying organisms use a different strategy to build their shells. This strategy employs a transient precursor crystallisation pathway, where an amorphous calcium carbonate phase is formed initially. The amorphous precursor phase is able to incorporate orders of magnitude more Mn than would be possible by non-biogenic aragonite. This crystallisation pathway, which involves particle attachment and stepwise crystallisation via metastable phases such as amorphous calcium carbonate and vaterite, is an energetically more favourable route as opposed to classical ion-by-ion crystallisation from solution. Upon crystallisation of the aragonitic shell, the chemical stability of Mn in octahedral coordination may drive the formation of calcite domains, which accommodate the Mn impurities in the aragonite host structure. In contrast to ion-by-ion crystal growth in inorganic processes, the transient precursor pathway in bivalves therefore seems to enable the incorporation of large Mn concentrations into the aragonite host lattice by changing the local symmetry around Mn at the atomic scale. This study thus provides insight into of one of the so-called “vital effects” of physiology on mineralogy and chemistry that so often complicate the deciphering of biogenic proxy archives.


Principal publication and authors
Element substitution by living organisms: the case of manganese in mollusc shell aragonite, A.L. Soldati (a), D.E. Jacob (b) , P. Glatzel (c), J.C. Swarbrick (c), J. Geck (d), Scientific Reports 6, 22514 EP (2016); doi: 10.1038/srep22514.
(a) Institut für Geowissenschaften, Johannes Gutenberg-Universität, Mainz (Germany)
(b) Department of Earth and Planetary Sciences, Macquarie University, Sydney (Australia)
(c) ESRF
(d) Chemistry and Physics of Materials, Paris Lodron University Salzburg, Salzburg (Austria)


[1] A.L. Soldati, D.E. Jacob, B.R. Schöne, M.M. Bianchi & A. Hajduk, J. Molluscan Studies 75, 75–85 (2009).
[2] P. Glatzel, & U. Bergmann, Coordination Chemistry Reviews 249, 65–95 (2005).


Top image: Mussels incorporate manganese into their carbonate shells and are a proxy archive for the interpretation of past climate changes.