journal menu
research papers
 | STRUCTURAL CHEMISTRY |
accessCe, Gd and Yb accumulation in microalgae: an L-edge study
aCawthron Institute, 98 Halifax Street East, Nelson, 7010, New Zealand, bSchool of Food Technology and Natural Sciences, Massey University, Riddet Road, Palmerston North, 4410, New Zealand, and cAustralian Synchrotro, Australian Nuclear Science and Technology Organisation, 800 Blackburn Road, Melbourne, VIC, 3168, Australia
*Correspondence e-mail: [email protected]
The extraction and separation of rare earth elements (lanthanides) can be difficult due to their chemical similarities. Biological processes can have very selective activity towards different elements. We investigated the use of microalgae for this purpose by looking at the interaction of Ce, Gd and Yb with the microalga Chlamydomonas reinhardtii, which has been induced to form polyphosphate granules. X-ray absorption spectroscopy with XANES and EXAFS at the Ce L3-edge, Gd L3-edge and Yb L3-edge was used to characterize the interaction between the lanthanides and the phosphate-containing algae. All three of the lanthanides, added as the chloride salt to the algae, appeared to react to form phosphate compounds. These form both in the presence of phosphate granules or when there is only a low level of P present. CePO4 could be determined by XANES, but the structures of GdPO4 and YbPO4 were determined by analysis without reference to the spectra of the standard compounds. It is proposed that C. reinhardtii or other similar microalgae may be useful in the selective removal of rare earths from solution.
Keywords: crystal structure; lanthanide; XAFS; EXAFS; Gd L3-edge; Ce L3-edge; Yb L3-edge; rare earth removal.
1. Introduction
Rare earth elements (lanthanides) are important for many technological applications. These include phosphors for lighting and displays, batteries, magnets and catalysts (Hu et al., 2024
). Geopolitical considerations (Fan et al., 2023) and the limited range of high-grade ore deposits available (Zhao et al., 2023) provide incentives to find new sources of lanthanides that might include lower concentration deposits, by-product streams from other extraction processes and urban mining (Sedykh et al., 2022). New extraction methods may be needed for the lower concentration sources, including radioactive waste sources (Jun et al., 2023), and these methods could be greener, and more sustainable methods (Zapp et al., 2022) include biomining (Vo et al., 2023).
A possible method to extract lanthanides from solution could be adsorption or absorption by bacteria and algae (Birungi & Chirwa, 2014). For instance, the removal of La, Y, Sm, Nd and Eu from wastewater by bacteria was demonstrated by Sun et al. (2022) and Jacinto et al. (2018), and the removal of Y, Ce, Eu and Tb from solution by red algae has also been demonstrated (Iovinella et al., 2022). Cyanobacteria can absorb Ce from wastewater (Sadovsky et al., 2016). It has also been shown that Cd can accumulate in the microalga Chlamydomonas reinhardtii (Penen et al., 2017). These pieces of evidence suggest that biological methods could be a means to separate mixtures of lanthanides if the absorption is significantly different for different lanthanides (Plouviez et al., 2024b).
To enhance the absorption of lanthanides into algae, the presence of phosphate, including polyphosphate granules that can be generated in some microalgae (Plouviez et al., 2024b; Cliff et al., 2023; Plouviez & Brown, 2024), has been considered (Plouviez et al., 2024b). This is based on the strong affinity that many rare earths have for phosphate, where the main mineral forms are monazite and xenotine, which are lanthanide phosphates. The affinity for phosphate increases along the lanthanide series from La to Lu (Wilharm et al., 2021).
A suitable technique for studying the chemistry of lanthanides in the solid state is X-ray absorption spectroscopy, either the near-edge region with XANES (X-ray Absorption Near Edge Spectroscopy) to give chemical information or an examination of the crystal structure in the local environment of the element of interest using EXAFS (Extended X-ray Absorption Fine Structure). Both require similar data collection. For the rare earth elements, the X-ray absorption edges easily accessible include the K-edges and the L-edges. Specifically, the L3-edge has been shown to be more sensitive to changes in chemical environment (Asakura et al., 2015, 2021).
It has been shown previously that Ce and Gd could absorb onto and within C. reinhardtii when the algae contains granules of polyphosphates (Plouviez et al., 2024b). Here we investigate the chemistry of Ce, Gd and Yb when this absorption has occurred, to understand the changes that have occurred in the rare earths with the P-containing algae. This range of Ce, Gd and Yb was chosen to represent a light, medium and heavy rare earth, with variation in the filling of electronic shells which should result in some slight differences in chemical bonding. Because standard phosphate compounds were not available for Gd and Yb, data measurements from an EXAFS analysis were required to assess whether these compounds had formed.
2. Materials and methods
2.1. Cultures
Chlamydomonas reinhardtii (CC-1690) culture maintenance and cultivation were performed as described in Plouviez et al. (2021). Briefly, the microalga was sequentially cultivated on low-phosphorus (1 mg P l−1) minimal media. The day of the experiment, 25 ml of culture was used to analyze the initial dry weight, optical density, total phosphorus and dissolved phosphate, and also for microscopic observations (Plouviez et al., 2021).
Algal cultures were supplemented with a P dose equivalent to a final concentration of 10 mg P l−1, using a 1 M stock solution of potassium phosphate (46 g l−1 KH2PO4 and 115 g l−1 K2HPO4) and either CeCl3, GdCl3 or YbCl3 at a final concentration of 6, 10 or 11 mg l−1, respectively.
The cultures were harvested by centrifugation at 10000 g for 3.5 min (Sigma 6–16 centrifuge) in several batches. The pellets were rinsed with distilled water and centrifuged again before being mixed to make a composite sample and frozen at −80 °C. The algae pellets were finally freeze dried in a Buchi Lyovapor L-300 for 36 h at 0.2 mbar (1 bar = 105 Pa) with a temperature profile starting at −30 °C and finishing at 20 °C.
2.2. XAS/XANES
The information provided here follows recent guidelines for reporting data (Paripsa et al., 2024). XAS scans at the Ce, Gd and Yb L3-edges were recorded at the MEX1 beamline at the Australian Synchrotron, ANSTO.
The MEX1 beamline uses X-rays from a bending magnet source and was configured for harmonic rejection for the energies of interest using a vertically collimating mirror translated to its rhodium stripe before a water-cooled Si(111) double crystal monochromator on an azimuth angle of 0°, and a vertical and horizontal focusing mirror also translated to its flat rhodium stripe after the monochromator. Energy resolution for MEX is (ΔE/E) of 1.4 × 10−4. Solid samples were pressed into 7 mm pellets for analysis. Standard compounds were mixed with cellulose powder and pressed into pellets for analysis and measured in transmission mode using 15 cm Ionitech gridded ion chambers filled with nitrogen to an absolute pressure of 2 bar. Samples showing low concentrations (<2 wt%) of Ce, Gd and Yb were analysed in fluorescence mode using a four-element silicon drift detector. Samples were run using a beam size of 0.5 mm vertical × 3 mm horizontal, giving a photon flux of 3 × 1011 photons s−1. Ambient temperature (20 °C) and atmospheric pressure under helium were used as the sample environment. Beam energy was calibrated using Cr, Co and Cu metal foils for Ce, Gd and Yb, respectively, by aligning the peak of the first derivative of their respective K-edges to reference values.
Sample scans employed variable step sizes, with a large step for the pre-edge region, a very small step over the edge region, a larger step size for the post-edge (XANES) region, and a larger and variable step size increasing in proportion to k for the EXAFS region. The recorded energy range was expanded to include the edge energy of the reference metal foils with a small step size in the region of the reference metal edge. The energy range and step sizes used are listed in Table 1. This scanning was run in continuous scanning mode (not discrete steps).
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
ATHENA (Ravel & Newville, 2005) software was used to process the XAS spectra. ATHENA was used for background removal, with E0 unconstrained, and for spectra normalization.
2.3. EXAFS
Data for was recorded over a k of 10.6 Å−1 for Ce, 11.95 Å−1 for Gd and 11.8 Å−1 for Yb. Data processing and fitting used only a portion of this data range, as detailed in Table 2. Bond lengths were calculated using ATOMS and FEFF6 (within ARTEMIS) (Ravel & Newville, 2005), with CIF data taken from the Crystallographic Open Database (COD) (Gražulis et al., 2009). ARTEMIS was used to fit spectroscopic data to data. Where we had not been able to measure the spectra of the reference compounds of interest (GaPO4 and YbPO4), we calculated the EXAFS spectra from the CIF data taken from the COD (Table 2), and these are also available on the Materials Project, where a compilation of many FEFF files are also available (Jain et al., 2013; Mathew et al., 2018).
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
2.4. Inductively coupled plasma mass spectrometry (ICP–MS)
The samples were prepared by the following method. The sample (1.0 ml) was added to a 15 ml centrifuge tube and 1.5 ml 69% HNO3 (Tracepur, Merck) and 0.5 ml 37% HCl (Tracepur, Merck) were added. The vessels were sealed and placed in a 100 °C water bath for 30 min. The digest was diluted with 13 ml Type-1 water to a 15 ml final volume. The solutions were quantitatively analysed for desired elements on an Agilent 7700 ICP–MS in He mode to reduce polyatomic interferences. Calibration standards were prepared in a matrix matched solution from 1000 ppm single element standards (CPI International, USA). A 20 ppb solution of Y was used to monitor drift and matrix effects. All results are in µg g−1 and have been back calculated to the original sample.
3. Results
3.1. P, Ce, Gd and Yb accumulation in C. reinhardtii samples
The transition from P deplete to P replete conditions in the absence of added rare earths triggered P accumulation in C. reinhardtii up to (2.50 ± 0.42)% P in the dry weight of algae. Similar concentrations were measured for the cultures supplemented with P and the rare earths with (2.40 ± 0.31)% P, (2.60 ± 0.01)% P and (2.32 ± 0.15)% P for the samples supplemented with Ce, Gd and Yb, respectively. ICP–MS analysis of dried C. reinhardtii samples showed that the microalgae supplemented by both P and either Ce or Gd accumulated Ce at 0.57 ± 0.54% Ce and Gd at 1.5 ± 0.9% Gd. This absorption amounts to 17% of the Ce and 27% of the Gd available from solution.
A large shift (3.4 eV) is observed in E0 (the energy) in the XANES spectra with with CeIVO2 at 5729.0 eV and CeIIICl3 and CeIIIPO4 at 5725.3 and 5725.5 eV, respectively. With algae, the of Ce, based on E0, is clearly III at 5724.6 eV with higher P level and 5724.9 eV with only low levels of P, which is not a significant shift. In the near-edge region [Fig. 1(b)], the difference between the algae with or without extra P and between CeCl3 and CePO4 are subtle and not helpful in identifying differences in structure. In the k plots [Fig. 1(c)], the structure of CeCl3 is clearly differentiated. It is then apparent that the C. reinhardtii samples do not contain CeCl3, but compounds much closer to CePO4. This is also supported by the R plot [Fig. 1(d)], where the different bond lengths of CeCl3 than CePO4 are apparent.
![[Figure 1]](vx3014fig1thm.gif) | Figure 1 Ce L3-edge XAS for C. reinhardtii and standard compounds. (a) XANES, (b) near-edge region, (c) EXAFS function k2χ(k) and (d) Fourier transform moduli of the EXAFS spectra. |
3.2. XAS Ce
The bond lengths determined from an analysis shown in Fig. 1(d) clearly differentiate between the different reference compounds and identify that CePO4 is the dominant form of Ce in the algae. The most intense scattering peaks determined from FEFF6 calculations from published structures for these compounds are given in Table 3. The shortening of the Ce—O bond at higher oxidation state is clearly visible in the data recorded here. The distinctive Ce—P bonds at 3.2–3.3 Å are a clear characteristic of CePO4 which is visible in the R plots.
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
From the bond lengths it is apparent that the C. reinhardtii samples do not contain CeCl3, but rather contain CePO4, corroborating the XANES E0 data discussed above. There appear to be no difference in the structure of the Ce compounds in C. reinhardtii with or without P. Clearly, CePO4 forms with the algae in both cases, and that there is enough P present for this under P-limited conditions for normal cell growth. No significant portion of Ce remains as CeCl3, the form in which it was added.
3.3. XAS Gd
For the Gd analysis, no Gd phosphate standard was available for comparison. We therefore relied on analysis of the bond lengths, and a comparison with calculated from available data, for a full interpretation. analyses of GdPO4 measured at the L3-edge have been reported previously (George et al., 2010; Morss et al., 1996; Yoon et al., 2002).
In the near-edge region, the difference between the algae with or without extra P and between GdCl3 and Gd acetylacetonate are subtle and not helpful in identifying differences in structure, although Gd2O3 is clearly different and not similar to the algae samples or the other standards. In the near-edge region, the Gd in C. reinhardtii looks the same with and without extra P (Fig. 2).
![[Figure 2]](vx3014fig2thm.gif) | Figure 2 Gd L3-edge XAS for C. reinhardtii and standard compounds. (a) XANES, (b) near-edge region, (c) EXAFS function k2χ(k) and (d) Fourier transform moduli of the EXAFS spectra. GdPO4 in parts (c) and (d) are derived spectra from literature crystal structures. |
However, in the k plot, there are clear differences between Gd in C. reinhardtii and the standards GdCl3 and Gd acetylacetonate in the range 8.5–10.5 Å−1. The differences are also pronounced in the R plot, where the peaks at 3.2 and 4.1 Å in the algae samples are not present in the standards (Fig. 2).
The bond lengths determined from an EXAFS analysis clearly differentiate between the different reference compounds and identify that GdPO4 is the dominant form of Gd in the algae. The most intense scattering peaks determined from FEFF6 calculations from published structures for these compounds are given in Table 4. The bond lengths of 3.2 and 4.1 Å corresponding to Gd—P and Gd—Gd provide strong evidence of the presence of GdPO4 in the algae samples, both with extra P and with low levels of P. To confirm this, a full fitting of the of GdPO4 to the data for the C. reinhardtii with P granules was performed (using ARTEMIS running FEFF6) (Fig. 2). This provided an adequate fit to the structure.
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
3.4. XAS Yb
For the Yb analysis, we also did not have a Yb phosphate standard for comparison. We therefore again relied on analysis of the bond lengths, and a comparison with calculated from available data, for a full interpretation. An analysis of YbPO4 measured at the L3-edge has been reported previously (Louvel et al., 2015), as well as a Raman spectroscopy analysis (Becker et al., 1992).
In the near-edge region, the difference between the algae with or without extra P and between YbCl3 and Yb in C. reinhardtii are subtle but, based on the experience with Ce and Gd, we do not expect this to be definitive in identifying differences in structure, although Yb2O3 is clearly different and not similar to the algae samples or YbCl3. In the near-edge region, the Yb in C. reinhardtii looks the same with and without extra P.
However, in the R plot, the differences are pronounced, where the peak at 3.0 Å in the algae samples is not present in the standards (Fig. 3). Also apparent in the R plot is the longer radial distance for the Yb—Cl bond length, forming the dominant low radial distance peak, compared with the Yb—O bond length in YbPO4 or Yb2O3. From this, the YbCl3 structure is easily able to be ruled out as a possible structure in C. reinhardtii.
![[Figure 3]](vx3014fig3thm.gif) | Figure 3 Yb L3-edge XAS for C. reinhardtii and standard compounds. (a) XANES, (b) near-edge region, (c) EXAFS function k2χ(k) and (d) Fourier transform moduli of the EXAFS spectra. k data is smoothed (11 point average). YbPO4 in parts (c) and (d) are derived spectra from literature crystal structures. |
The bond lengths determined from an analysis clearly differentiate between the different reference compounds and identify that YbPO4 is the dominant form of Yb in the algae. The most intense scattering peaks determined from FEFF6 calculations from published structures for these compounds are given in Table 5. We were not able to get convergence of a fit of the data for Yb in C. reinhardtii to YbCl3.
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
The bond length of 3.0 Å corresponding to Yb—P provides evidence of the presence of YbPO4 in the algae samples, both with extra P and with low levels of P. To confirm this, a full fitting of the of YbPO4 to the data for the C. reinhardtii with P granules was performed (using ARTEMIS running FEFF6) (Table 5). The fit to the structure of YbPO4 was poor, but is probably adequate for the noisy quality of the data. The data did not require smoothing prior to fitting, because of the nature of using a Fourier transform for this fitting, which separates the high-frequency noise; however, for the purposes of displaying the experimental data, an 11-point moving average was used.
4. Discussion and conclusions
Previously, we have shown that phosphate granules that form in C. reinhardtii are composed of polyphosphates, some in the form of inositol phosphate (otherwise known as phytate) (Plouviez et al., 2024a). We then showed with scanning transmission X-ray microscopy that the addition of Gd to these algae results in an association of Gd with P, including with the polyphosphate granules inside the algae (Plouviez et al., 2024b). With Ce there was an association of Ce with P but not within the algae. That previous work did not investigate the interactions of Yb.
P K-edge XANES on the Gd- and Ce-doped algae with extra phosphate showed some change in the chemistry of P, suggesting that there is a chemical interaction between the rare earths and phosphate (Plouviez et al., 2024b). However, the P atom is interacting only at a distance, via the O atom bonded to phosphorus, and therefore the chemical changes observed at the P atom are not large. A more sensitive measure of that interaction is the work described here, where this same interaction is observed from the rare earth atom. The change is one that is more direct, with the lanthanide interacting not with a chloride ion in the compound added, but with a phosphate ion, a larger difference in electronic interaction. It is an interaction specific to the lanthanide ion – so that if the phosphate is in a variety of states, with some bonded to lanthanide and some not, this will not confound the results, unlike with P K-edge XAS.
In this work, we have found that XANES was very useful in identifying the chemical structures present for Ce. There were significant differences in the near-edge spectra for the different Ce compounds and we had a spectrum of CePO4 for comparison which provided a good match. For Gd and Yb we were not able to record spectra of the phosphate compounds from standards, so we had to rely on analysis of the Fortunately, crystal structures of Gd and Yb phosphates are available in the literature, so it was possible to model the spectrum from these structures to fit with the data recorded in this work and find a good match to GdPO4 and a reasonable match to YbPO4.
The L3-edge for Ce, Gd and Yb provided sufficient sensitivity to chemical changes to be useful for analytical purposes. Other studies have investigated this sensitivity in more detail for each of the elements at the X-ray edge (Asakura et al., 2015, 2021), with many studies on Ce and some specifically on Gd (George et al., 2010; Morss et al., 1996; Yoon et al., 2002) and Yb (Louvel et al., 2015).
This study suggests that microalgae with phosphate may be a useful method of capturing rare earths from solutions. These are living organisms so the tolerance of these organisms to the presence of lanthanides also needs to be considered if this is to be a viable extraction technique. This was not directly addressed in the work presented here. However, other studies have investigated aspects of tolerance to lanthanides. In Chlorella sp., Ce3+ slightly boosted biomass production in concentrations up to 7 µM, but in C. reinhardtii, Ce has been found to decrease photosynthetic yield at concentrations of 1–200 µM (Röhder et al., 2014). Although it has also been found that in C. reinhardtii, Ce3+ does not inhibit cell growth when the Ce is stabilized by phosphate (Röhder et al., 2014). The protective effect of polyphosphate accumulation has also been observed with uranium, where it increases tolerance for the cyanobacterium Anabaena torulosa (Chandwadkar & Acharya, 2023).
The extraction and separation of rare earth elements (lanthanides) can be difficult due to their chemical similarities (Baldwin et al., 2018). Biological processes can have very selective activity towards different elements. However, all three of the lanthanides added to the algae as chloride reacted to form phosphate compounds. These formed both in the presence of polyphosphate granules or when there was only a low level of P present. Nevertheless, C. reinhardtii or other similar microalgae may be useful in the removal of rare earths from solution, with the selectivity to different lanthanides yet to be determined.
Acknowledgements
The authors thank Stuart Morrow, School of Chemical Sciences, The University of Auckland, for the ICP–MS analysis. Open access publishing facilitated by Massey University, as part of the Wiley–Massey University agreement via the Council of Australian University Librarians.
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Data availability
Raw data and fitted data are available on request.
Funding information
Funding for this research was provided by: Australian Nuclear Science and Technology Organization (grant No. M20433); New Zealand Synchrotron Group; French Embassy of New Zealand, Pacific Fund (grant No. 2337); Ministry of Business, Innovation and Employment (grant No. MAUX2302).
References
Asakura, H., Hosokawa, S., Teramura, K. & Tanaka, T. (2021). Inorg. Chem. 60, 9359–9367. CrossRef PubMed Google Scholar
Asakura, H., Shishido, T., Teramura, K. & Tanaka, T. (2015). J. Phys. Chem. C 119, 8070–8077. CrossRef Google Scholar
Baldwin, A. G., Ivanov, A. S., Williams, N. J., Ellis, R. J., Moyer, B. A., Bryantsev, V. S. & Shafer, J. C. (2018). ACS Cent. Sci. 4, 739–747. CrossRef PubMed Google Scholar
Becker, P., Williams, G., Edelstein, N., Koningstein, J., Boatner, L. & Abraham, M. (1992). Phys. Rev. B 45, 5027–5030. CrossRef Google Scholar
Birungi, Z. S. & Chirwa, E. M. N. (2014). Bioresour. Technol. 160, 43–51. CrossRef PubMed Google Scholar
Chandwadkar, P. & Acharya, C. (2023). J. Environ. Radioact. 263, 107185. CrossRef PubMed Google Scholar
Cliff, A., Guieysse, B., Brown, N., Lockhart, P., Dubreucq, E. & Plouviez, M. (2023). Algal Res. 73, 103161. CrossRef Google Scholar
Fan, J. H., Omura, A. & Roca, E. (2023). Eur. J. Polit. Econ. 78, 102356. CrossRef Google Scholar
George, S. J., Webb, S. M., Abraham, J. L. & Cramer, J. L. (2010). Br. J. Dermatol. 163, 1077–1081. CrossRef PubMed Google Scholar
Gražulis, S., Chateigner, D., Downs, R. T., Yokochi, A. F. T., Quirós, M., Lutterotti, L., Manakova, E., Butkus, J., Moeck, P. & Le Bail, A. (2009). J. Appl. Cryst. 42, 726–729. Web of Science CrossRef IUCr Journals Google Scholar
Hu, Z., Yu, B., Liu, L. C. & Wei, Y. M. (2024). Sci. Total Environ. 912, 168634. CrossRef PubMed Google Scholar
Iovinella, M., Lombardo, F., Ciniglia, C., Palmieri, M., di Cicco, M. R., Trifuoggi, M., Race, M., Manfredi, C., Lubritto, C., Fabbricino, M., De Stefano, M. & Davis, S. J. (2022). Plants 11, 1376. CrossRef PubMed Google Scholar
Jacinto, J., Henriques, B., Duarte, A., Vale, C. & Pereira, E. (2018). J. Hazard. Mater. 344, 531–538. CrossRef PubMed Google Scholar
Jain, A., Ong, S. P., Hautier, G., Chen, W., Richards, W. D., Dacek, S., Cholia, S., Gunter, D., Skinner, D., Ceder, G. & Persson, K. A. (2013). APL Mater. 1, 011002. Google Scholar
Jun, B.-M., Kim, H.-H., Rho, H., Seo, J., Jeon, J.-W., Nam, S.-N., Min Park, C. & Yoon, Y. (2023). Chem. Eng. J. 475, 146222. CrossRef Google Scholar
Louvel, M., Bordage, A., Testemale, D., Zhou, L. & Mavrogenes, J. (2015). Chem. Geol. 417, 228–237. CrossRef Google Scholar
Mathew, K., Zheng, C., Winston, D., Chen, C., Dozier, A., Rehr, J. J., Ong, S. P. & Persson, K. A. (2018). Sci. Data 5, 180151. CrossRef PubMed Google Scholar
Morss, L. R., Schmidt, M. A., Nash, K. L., Allen, P. G., Bucher, J. J., Edelstein, N., Shuh, D. K., Denecke, M. A., Nitsche, H. & Reich, T. (1996). In EXAFS studies of lanthanide coordination in crystalline phosphates and amorphous phytates. Berlin: Springer. Google Scholar
Paripsa, S., Gaur, A., Förste, F., Doronkin, D. E., Malzer, W., Schlesiger, C., Kanngiesser, B., Welter, E., Grunwaldt, J.-D. & Lützenkirchen-Hecht, D. (2024). J. Synchrotron Rad. 31, 1105–1117. CrossRef IUCr Journals Google Scholar
Penen, F., Isaure, M., Dobritzsch, D., Bertalan, I., Castillo-Michel, H., Proux, O., Gontier, E., Le Coustumer, P. & Schaumlöffel, D. (2017). Metallomics 9, 910–923. CrossRef PubMed Google Scholar
Plouviez, M. & Brown, N. (2024). Curr. Opin. Biotechnol. 90, 103207. CrossRef PubMed Google Scholar
Plouviez, M., Fernández, E., Grossman, A. R., Sanz–Luque, E., Sells, M., Wheeler, D. & Guieysse, B. (2021). J. Phycol. 57, 988–1003. CrossRef PubMed Google Scholar
Plouviez, M., Guieysse, B., Buwalda, O., Wolmarans, K., Thånell, K., Beinik, I., Tuyishime, J. R. M., Mitchell, V., Kappen, P. & Haverkamp, R. G. (2024a). ACS Sustain. Res. Manag. 1, 1270–1278. Google Scholar
Plouviez, M., Guieysse, B., Wolmarans, K., Matinong, A. M. E., Buwalda, O., Thånell, K., Beinik, I., Tuyishime, J. R. M., Mitchell, V., Kappen, P., Flynn, D., Jauffrais, T. & Haverkamp, R. G. (2024b). ACS Sustain. Res. Manag. 1, 2225–2233. Google Scholar
Ravel, B. & Newville, M. (2005). J. Synchrotron Rad. 12, 537–541. Web of Science CrossRef CAS IUCr Journals Google Scholar
Röhder, L. A., Brandt, T., Sigg, L. & Behra, R. (2014). Aquat. Toxicol. 152, 121–130. PubMed Google Scholar
Sadovsky, D., Brenner, A., Astrachan, B., Asaf, B. & Gonen, R. (2016). J. Rare Earths 34, 644–652. CrossRef Google Scholar
Sedykh, A. E., Pflug, J. J., Schäfer, T. C., Bissert, R., Kurth, D. G. & Müller-Buschbaum, K. (2022). ACS Sustainable Chem. Eng. 10, 5101–5109. CrossRef Google Scholar
Sun, Y., Lu, T., Pan, Y., Shi, M., Ding, D., Ma, Z., Liu, J., Yuan, Y., Fei, L. & Sun, Y. (2022). Environ. Sci. Ecotech. 12, 100204. Google Scholar
Vo, P. H., Danaee, S., Hai, H. T. N., Huy, L. N., Nguyen, T. A., Nguyen, H. T., Kuzhiumparambil, U., Kim, M., Nghiem, L. D. & Ralph, P. J. (2023). Sci. Total Environ. 908, 168210. CrossRef PubMed Google Scholar
Wilharm, R. K., Huang, S.-Y., Gugger, I. J. & Pierre, V. C. (2021). Inorg. Chem. 60, 15808–15817. CrossRef PubMed Google Scholar
Yoon, S., Helmke, P. A., Amonette, J. E. & Bleam, W. F. (2002). Langmuir 18, 10128–10136. CrossRef Google Scholar
Zapp, P., Schreiber, A., Marx, J. & Kuckshinrichs, W. (2022). MRS Bull. 47, 267–275. CrossRef PubMed Google Scholar
Zhao, S., Wang, P., Chen, W., Wang, L., Wang, Q.-C. & Chen, W.-Q. (2023). Resour. Conserv. Recycl. 199, 107254. CrossRef Google Scholar
This is an open-access article distributed under the terms of the Creative Commons Attribution (CC-BY) Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are cited.
| STRUCTURAL CHEMISTRY |
access
