EF-Hand Battle Royale: Hetero-ion Complexation in Lanmodulin

Seidel, Jeremy; Diep, Patrick; Dong, Ziye; Cotruvo, Joseph A.; Park, Dan M.

doi:10.1021/jacsau.4c00628

EF-Hand Battle Royale: Hetero-ion Complexation in Lanmodulin

Journal Article · Thu Sep 05 00:00:00 EDT 2024 · JACS Au

DOI:https://doi.org/10.1021/jacsau.4c00628· OSTI ID:2478758

Seidel, Jeremy ^[1]; ^[1]; ^[1]; ^[2]; ^[1]

Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Pennsylvania State University, University Park, PA (United States)

The lanmodulin (LanM) protein has emerged as an effective means for rare earth element (REE) extraction and separation from complex feedstocks without the use of organic solvents. Whereas the binding of LanM to individual REEs has been well characterized, little is known about the thermodynamics of mixed metal binding complexes (i.e., heterogeneous ion complexes), which limits the ability to accurately predict separation performance for a given metal ion mixture. In this paper, we employ the law of mass action to establish a theory of perfect cooperativity for LanM-REE complexation at the two highest-affinity binding sites. The theory is then used to derive an equation that explains the nonintuitive REE binding behavior of LanM, where separation factors for binary pairs of ions vary widely based on the ratio of ions in the aqueous phase, a phenomenon that is distinct from single-ion-binding chemical chelators. We then experimentally validate this theory and perform the first quantitative characterization of LanM complexation with heterogeneous ion pairs using resin-immobilized LanM. Importantly, the resulting homogeneous and heterogeneous constants enable accurate prediction of the equilibrium state of LanM in the presence of mixtures of up to 10 REEs, confirming that the perfect cooperativity model is an accurate mechanistic description of REE complexation by LanM. We further employ the model to simulate separation performance over a range of homogeneous and heterogeneous binding constants, revealing important insights into how mixed binding differentially impacts REE separations based on the relative positioning of the ion pairs within the lanthanide series. In addition to informing REE separation process optimization, these results provide mathematical and experimental insight into competition dynamics in other ubiquitous and medically relevant, cooperative binding proteins, such as calmodulin.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Energy Efficiency and Renewable Energy (EERE), Energy Efficiency Office. Advanced Materials & Manufacturing Technologies Office (AMMTO); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC52-07NA27344; SC0021007

OSTI ID:: 2478758

Alternate ID(s):: OSTI ID: 2478854

Journal Information:: JACS Au, Journal Name: JACS Au Journal Issue: 11 Vol. 4; ISSN 2691-3704

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (41)

Repeated Recovery of Rare Earth Elements Using a Highly Selective and Thermo‐Responsive Genetically Encoded Polypeptide Hussain, Zohaib; Kim, Seoungkyun; Cho, Jinhwan Advanced Functional Materials, Vol. 32, Issue 13 https://doi.org/10.1002/adfm.202109158	journal	December 2021
Structural Origin of the High Affinity of a Chemically Evolved Lanthanide-Binding Peptide Nitz, Mark; Sherawat, Manashi; Franz, Katherine J. Angewandte Chemie International Edition, Vol. 43, Issue 28 https://doi.org/10.1002/anie.200460028	journal	July 2004
Lanthanide-Binding Tags as Versatile Protein Coexpression Probes Franz, Katherine J.; Nitz, Mark; Imperiali, Barbara ChemBioChem, Vol. 4, Issue 4 https://doi.org/10.1002/cbic.200390046	journal	March 2003
Biochemical and Structural Characterization of XoxG and XoxJ and Their Roles in Lanthanide‐Dependent Methanol Dehydrogenase Activity Featherston, Emily R.; Rose, Hannah R.; McBride, Molly J. ChemBioChem, Vol. 20, Issue 18 https://doi.org/10.1002/cbic.201900184	journal	July 2019
Assessing Lanthanide‐Dependent Methanol Dehydrogenase Activity: The Assay Matters Phi, Manh Tri; Singer, Helena; Zäh, Felix ChemBioChem, Vol. 25, Issue 5 https://doi.org/10.1002/cbic.202300811	journal	January 2024
Efficient Separation of Light Lanthanides(III) by Using Bis‐Lactam Phenanthroline Ligands Healy, Mary R.; Ivanov, Alexander S.; Karslyan, Yana Chemistry – A European Journal, Vol. 25, Issue 25 https://doi.org/10.1002/chem.201806443	journal	March 2019
The Rare Earth Elements Voncken, J. H. L. SpringerBriefs in Earth Sciences https://doi.org/10.1007/978-3-319-26809-5	book	January 2016
Surface complexation model of rare earth element adsorption onto bacterial surfaces with lanthanide binding tags Chang, Elliot; Brewer, Aaron W.; Park, Dan M. Applied Geochemistry, Vol. 112 https://doi.org/10.1016/j.apgeochem.2019.104478	journal	January 2020
The size of actinoid(III) ions – structural analysis vs. common misinterpretations Lundberg, Daniel; Persson, Ingmar Coordination Chemistry Reviews, Vol. 318 https://doi.org/10.1016/j.ccr.2016.04.003	journal	July 2016
Leaching behavior of rare earth elements in Fort Union lignite coals of North America Laudal, Daniel A.; Benson, Steven A.; Addleman, Raymond Shane International Journal of Coal Geology, Vol. 191 https://doi.org/10.1016/j.coal.2018.03.010	journal	April 2018
Preference for particular lanthanide species and thermal stability of XoxFs in Methylorubrum extorquens strain AM1 Wang, Lun; Hibino, Ayumi; Suganuma, Souya Enzyme and Microbial Technology, Vol. 136 https://doi.org/10.1016/j.enzmictec.2020.109518	journal	May 2020
Yttrium separation by phosphorylcarboxylic acid and the underlying tetrad effect along lanthanide unveiled from different microscopic interactions Zhang, Xuyi; Zhang, Xun; Zheng, Haifeng Fundamental Research https://doi.org/10.1016/j.fmre.2023.01.004	journal	January 2023
The evolution of mineral processing in extraction of rare earth elements using solid-liquid extraction over liquid-liquid extraction: A review Hidayah, Nur Nadiatul; Abidin, Sumaiya Zainal Minerals Engineering, Vol. 112 https://doi.org/10.1016/j.mineng.2017.07.014	journal	October 2017
Process development for the recovery of rare earth elements and critical metals from an acid mine leachate Zhang, Wencai; Honaker, Rick Minerals Engineering, Vol. 153 https://doi.org/10.1016/j.mineng.2020.106382	journal	July 2020
Protein-based approach for high-purity Sc, Y, and grouped lanthanide separation Dong, Ziye; Mattocks, Joseph A.; Seidel, Jeremy A. Separation and Purification Technology, Vol. 333 https://doi.org/10.1016/j.seppur.2023.125919	journal	April 2024
The Hemoglobin System Adair, G. S.; Bock, A. V.; Field, H. Journal of Biological Chemistry, Vol. 63, Issue 2 https://doi.org/10.1016/s0021-9258(18)85018-9	journal	March 1925
Bioadsorption of Rare Earth Elements through Cell Surface Display of Lanthanide Binding Tags Park, Dan M.; Reed, David W.; Yung, Mimi C. Environmental Science & Technology, Vol. 50, Issue 5 https://doi.org/10.1021/acs.est.5b06129	journal	February 2016
Recovery of Rare Earth Elements from Low-Grade Feedstock Leachates Using Engineered Bacteria Park, Dan M.; Brewer, Aaron; Reed, David W. Environmental Science & Technology, Vol. 51, Issue 22 https://doi.org/10.1021/acs.est.7b02414	journal	November 2017
Selective and Efficient Biomacromolecular Extraction of Rare-Earth Elements using Lanmodulin Deblonde, Gauthier J. -P.; Mattocks, Joseph A.; Park, Dan M. Inorganic Chemistry, Vol. 59, Issue 17 https://doi.org/10.1021/acs.inorgchem.0c01303	journal	July 2020
Tuning the Separation of Light Lanthanides Using a Reverse-Size Selective Aqueous Complexant Thiele, Nikki A.; Fiszbein, David J.; Woods, Joshua J. Inorganic Chemistry, Vol. 59, Issue 22 https://doi.org/10.1021/acs.inorgchem.0c02413	journal	October 2020
Evidence for Participation of 4f and 5d Orbitals in Lanthanide Metal–Ligand Bonding and That Y(III) Has Less of This Complex-Stabilizing Ability. A Thermodynamic, Spectroscopic, and DFT Study of Their Complexation by the Nitrogen Donor Ligand TPEN Zanella, Brady S.; Jones, S. Bart; Lee, Hee-Seung Inorganic Chemistry, Vol. 61, Issue 11 https://doi.org/10.1021/acs.inorgchem.1c03443	journal	March 2022
Periodicity of the Affinity of Lanmodulin for Trivalent Lanthanides and Actinides: Structural and Electronic Insights from Quantum Chemical Calculations Prejanò, Mario; Toscano, Marirosa; Marino, Tiziana Inorganic Chemistry, Vol. 62, Issue 19 https://doi.org/10.1021/acs.inorgchem.3c00754	journal	May 2023
Bis-lactam-1,10-phenanthroline (BLPhen), a New Type of Preorganized Mixed N,O-Donor Ligand That Separates Am(III) over Eu(III) with Exceptionally High Efficiency Jansone-Popova, Santa; Ivanov, Alexander S.; Bryantsev, Vyacheslav S. Inorganic Chemistry, Vol. 56, Issue 10 https://doi.org/10.1021/acs.inorgchem.7b00555	journal	April 2017
Bridging Hydrometallurgy and Biochemistry: A Protein-Based Process for Recovery and Separation of Rare Earth Elements Dong, Ziye; Mattocks, Joseph A.; Deblonde, Gauthier J. -P. ACS Central Science, Vol. 7, Issue 11 https://doi.org/10.1021/acscentsci.1c00724	journal	October 2021
Binding Energy and Free Energy of Calcium Ion to Calmodulin EF-Hands with the Drude Polarizable Force Field Tan, Qiaozhu; Ding, Ye; Qiu, Zongyang ACS Physical Chemistry Au, Vol. 2, Issue 2 https://doi.org/10.1021/acsphyschemau.1c00039	journal	December 2021
Powdered Hierarchically Porous Silica Monoliths for the Selective Extraction of Scandium Brewer, Aaron; Reicher, Chloé; Manatschal, Olivia ACS Sustainable Chemistry & Engineering, Vol. 11, Issue 42 https://doi.org/10.1021/acssuschemeng.3c04672	journal	October 2023
The Second Ca²⁺-Binding Domain of NCX1 Binds Mg²⁺ with High Affinity Breukels, Vincent; Konijnenberg, Albert; Nabuurs, Sanne M. Biochemistry, Vol. 50, Issue 41 https://doi.org/10.1021/bi201134u	journal	September 2011
Battle for the EF-Hands: Magnesium−Calcium Interference in Calmodulin ^† Malmendal, Anders; Linse, Sara; Evenäs, Johan Biochemistry, Vol. 38, Issue 36 https://doi.org/10.1021/bi9909288	journal	September 1999
Probing Lanmodulin’s Lanthanide Recognition via Sensitized Luminescence Yields a Platform for Quantification of Terbium in Acid Mine Drainage Featherston, Emily R.; Issertell, Edward J.; Cotruvo, Joseph A. Journal of the American Chemical Society, Vol. 143, Issue 35 https://doi.org/10.1021/jacs.1c06360	journal	August 2021
Lanmodulin: A Highly Selective Lanthanide-Binding Protein from a Lanthanide-Utilizing Bacterium Cotruvo, Joseph A.; Featherston, Emily R.; Mattocks, Joseph A. Journal of the American Chemical Society, Vol. 140, Issue 44 https://doi.org/10.1021/jacs.8b09842	journal	October 2018
Size Selective Ligand Tug of War Strategy to Separate Rare Earth Elements Johnson, Katherine R.; Driscoll, Darren M.; Damron, Joshua T. JACS Au, Vol. 3, Issue 2 https://doi.org/10.1021/jacsau.2c00671	journal	January 2023
Enhanced rare-earth separation with a metal-sensitive lanmodulin dimer Mattocks, Joseph A.; Jung, Jonathan J.; Lin, Chi-Yun Nature, Vol. 618, Issue 7963 https://doi.org/10.1038/s41586-023-05945-5	journal	May 2023
Observation of a promethium complex in solution Driscoll, Darren M.; White, Frankie D.; Pramanik, Subhamay Nature, Vol. 629, Issue 8013 https://doi.org/10.1038/s41586-024-07267-6	journal	May 2024
Engineering lanmodulin's selectivity for actinides over lanthanides by controlling solvent coordination and second-sphere interactions Mattocks, Joseph A.; Cotruvo, Joseph A.; Deblonde, Gauthier J. -P. Chemical Science, Vol. 13, Issue 20 https://doi.org/10.1039/d2sc01261h	journal	January 2022
Modulating metal-centered dimerization of a lanthanide chaperone protein for separation of light lanthanides Larrinaga, Wyatt B.; Jung, Jonathan J.; Lin, Chi-Yun Proceedings of the National Academy of Sciences, Vol. 121, Issue 45 https://doi.org/10.1073/pnas.2410926121	journal	October 2024
Calcium Binding to Calmodulin. Cooperativity of the Calcium-Binding Sites Iida, Shozo; Potter, James D. The Journal of Biochemistry, Vol. 99, Issue 6 https://doi.org/10.1093/oxfordjournals.jbchem.a135654	journal	January 1986
Global Rare Earth In-Use Stocks in NdFeB Permanent Magnets Du, Xiaoyue; Graedel, T. E. Journal of Industrial Ecology, Vol. 15, Issue 6 https://doi.org/10.1111/j.1530-9290.2011.00362.x	journal	July 2011
Positive Cooperativity of Acetylcholine and Other Agonists with Allosteric Ligands on Muscarinic Acetylcholine Receptors Jakubík, Jan; Bačáková, Lucie; El-Fakahany, Esam E. Molecular Pharmacology, Vol. 52, Issue 1 https://doi.org/10.1124/mol.52.1.172	journal	July 1997
Lanthanide-Dependent Regulation of Methanol Oxidation Systems in Methylobacterium extorquens AM1 and Their Contribution to Methanol Growth Vu, Huong N.; Subuyuj, Gabriel A.; Vijayakumar, Srividhya Journal of Bacteriology, Vol. 198, Issue 8 https://doi.org/10.1128/jb.00937-15	journal	February 2016
Extractive metallurgy of rare earths Gupta, C. K.; Krishnamurthy, N. International Materials Reviews, Vol. 37, Issue 1 https://doi.org/10.1179/imr.1992.37.1.197	journal	January 1992
Lanthanide-Dependent Methanol Dehydrogenases of XoxF4 and XoxF5 Clades Are Differentially Distributed Among Methylotrophic Bacteria and They Reveal Different Biochemical Properties Huang, Jing; Yu, Zheng; Chistoserdova, Ludmila Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01366	journal	June 2018

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
REE separation
complexation
equilibrium constant
ions
lanmodulin
lanmodulin reaction network
lanthanides
mixed binding
mixed metal binding
poly-ion model
rare earths
selectivity
separation factor

EF-Hand Battle Royale: Hetero-ion Complexation in Lanmodulin

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