Rare Earth Element-Induced Condensation of the Block V of the Repeats-in-Toxin Domain from CyaA from Bordetella pertussis for Separations

Ortuno Macias, Luis E.; Khoury, Farid; Bera, Mrinal K.; Bu, Wei; Lin, Binhua; Banta, Scott; Tu, Raymond S.

doi:10.1021/acs.langmuir.5c04148

Title: Rare Earth Element-Induced Condensation of the Block V of the Repeats-in-Toxin Domain from CyaA from Bordetella pertussis for Separations

Journal Article · Thu Dec 18 00:00:00 UTC 2025 · Langmuir

DOI: https://doi.org/10.1021/acs.langmuir.5c04148 · OSTI ID:3011362

^[1];

^[2];

^[3];

^[3]; Lin, Binhua ^[3]; Banta, Scott ^[2];

^[1]

City Univ. of New York (CUNY), NY (United States)
Columbia Univ., New York, NY (United States)
Univ. of Chicago, IL (United States)

Rare earth elements (REEs) are critical for the development of a range of new technologies. However, the current industrial separation processes of these metals from natural sources, recycled materials, and industrial effluents involve the large consumption of organic solvents, resulting in a sizable environmental footprint. We aim to exploit the high affinity of the block V peptide of the repeats-in-toxin (RTX) domain of the adenylate cyclase protein from Bordetella pertussis for the separation of REEs. This peptide selectively binds with lanthanide (Ln) cations and can undergo Ln-induced phase separation, which can be used in bioseparation processes. Here, we evaluated the self-assembling structures of complexes of the RTX domain peptide folded in the presence of Ln³⁺ cations. Size distribution and surface potential measurements of complexes were taken to understand the Ln-induced changes in the complexed peptide. Transmission electron microscopy imaging was used to explore the structures of complexes, while anomalous small-angle X-ray scattering measurements were used to determine the distribution of Ln³⁺ ions within the protein-based macrostructures. In the presence of excess Ln³⁺, we observed the formation of coral-like cylindrical structures comprised of Ln³⁺-RTX complexes, with approximately eight trivalent metals per peptide within the nanosized assemblies. These findings provide new insights into the structural organization of assembled RTX domains and their ability to coordinate with REEs, forming nanosized, metal-rich structures that naturally condense, providing a proof-of-concept for protein-based separation processes of these critical materials.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); Univ. of Pennsylvania, Philadelphia, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357; SC0022240

OSTI ID:: 3011362

Journal Information:: Langmuir, Journal Name: Langmuir Journal Issue: 51 Vol. 41; ISSN 0743-7463; ISSN 1520-5827

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

DNA condensation by multivalent cations Bloomfield, Victor A. Biopolymers, Vol. 44, Issue 3 https://doi.org/10.1002/(SICI)1097-0282(1997)44:3<269::AID-BIP6>3.0.CO;2-T	journal	January 1997
Lanmodulin‐Decorated Microbes for Efficient Lanthanide Recovery Gut, Melanie; Wilhelm, Tatum; Beniston, Olivia Advanced Materials, Vol. 37, Issue 10 https://doi.org/10.1002/adma.202412607	journal	January 2025
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
Accurate Determination of the Quantity and Spatial Distribution of Counterions around a Spherical Macroion Chen, Jiahui; Bera, Mrinal K.; Li, Hui Angewandte Chemie International Edition, Vol. 60, Issue 11 https://doi.org/10.1002/anie.202013806	journal	January 2021
Rare-Earth Metal Recovery for Green Technologies: Methods and Applications Jyothi, Rajesh Kumar https://doi.org/10.1007/978-3-030-38106-6	book	December 2019
Separation Hydrometallurgy of Rare Earth Elements Zhang, Jack; Zhao, Baodong; Schreiner, Bryan https://doi.org/10.1007/978-3-319-28235-0	book	December 2015
Determination of conformation and orientation of immobilized peptides and proteins at buried interfaces Shen, Lei; Ulrich, Nathan W.; Mello, Charlene M. Chemical Physics Letters, Vol. 619 https://doi.org/10.1016/j.cplett.2014.10.035	journal	January 2015
Tuning the properties of β-lactoglobulin nanofibrils with pH, NaCl and CaCl2 Loveday, S. M.; Wang, X. L.; Rao, M. A. International Dairy Journal, Vol. 20, Issue 9 https://doi.org/10.1016/j.idairyj.2010.02.014	journal	September 2010
β-Lactoglobulin nanofibrils: The long and the short of it Loveday, Simon M.; Anema, Skelte G.; Singh, Harjinder International Dairy Journal, Vol. 67 https://doi.org/10.1016/j.idairyj.2016.09.011	journal	April 2017
Enhanced rare earth element recovery with cross-linked glutaraldehyde-lanthanide binding peptides in foam-based separations Ortuno Macias, Luis E.; Zhang, Honghu; Ocko, Benjamin M. Journal of Colloid and Interface Science, Vol. 678 https://doi.org/10.1016/j.jcis.2024.08.225	journal	January 2025
Environmental life cycle assessment on the separation of rare earth oxides through solvent extraction Vahidi, Ehsan; Zhao, Fu Journal of Environmental Management, Vol. 203 https://doi.org/10.1016/j.jenvman.2017.07.076	journal	December 2017
Effectively auto-regulated adsorption and recovery of rare earth elements via an engineered E. coli Xie, Xiaoman; Tan, Xirui; Yu, Yiyan Journal of Hazardous Materials, Vol. 424 https://doi.org/10.1016/j.jhazmat.2021.127642	journal	February 2022
Functional and structural studies on different forms of the adenylate cyclase toxin of Bordetella pertussis Cheung, Gordon Y. C.; Kelly, Sharon M.; Jess, Thomas J. Microbial Pathogenesis, Vol. 46, Issue 1 https://doi.org/10.1016/j.micpath.2008.10.005	journal	January 2009
A Diversity of Assembly Mechanisms of a Generic Amyloid Fold Eichner, Timo; Radford, Sheena E. Molecular Cell, Vol. 43, Issue 1 https://doi.org/10.1016/j.molcel.2011.05.012	journal	July 2011
Calcium-Driven Folding of RTX Domain β-Rolls Ratchets Translocation of RTX Proteins through Type I Secretion Ducts Bumba, Ladislav; Masin, Jiri; Macek, Pavel Molecular Cell, Vol. 62, Issue 1 https://doi.org/10.1016/j.molcel.2016.03.018	journal	April 2016
Structure formation in polyelectrolytes induced by multivalent ions Jusufi, Arben; Borisov, Oleg; Ballauff, Matthias Polymer, Vol. 54, Issue 8 https://doi.org/10.1016/j.polymer.2012.12.030	journal	April 2013
Review and new life cycle assessment for rare earth production from bastnäsite, ion adsorption clays and lateritic monazite Bailey, Gwendolyn; Joyce, P. James; Schrijvers, Dieuwertje Resources, Conservation and Recycling, Vol. 155 https://doi.org/10.1016/j.resconrec.2019.104675	journal	April 2020
Engineering biomaterials for the recovery of rare earth elements Ye, Quanhui; Wang, Dong; Wei, Na Trends in Biotechnology, Vol. 42, Issue 5 https://doi.org/10.1016/j.tibtech.2023.10.011	journal	May 2024
Metal Binding of Alzheimer’s Amyloid-β and Its Effect on Peptide Self-Assembly Abelein, Axel Accounts of Chemical Research, Vol. 56, Issue 19 https://doi.org/10.1021/acs.accounts.3c00370	journal	September 2023
Lanmodulin-Functionalized Magnetic Nanoparticles as a Highly Selective Biosorbent for Recovery of Rare Earth Elements Ye, Quanhui; Jin, Xiuyu; Zhu, Baotong Environmental Science & Technology, Vol. 57, Issue 10 https://doi.org/10.1021/acs.est.2c08971	journal	February 2023
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
Microbe Encapsulation for Selective Rare-Earth Recovery from Electronic Waste Leachates Brewer, Aaron; Dohnalkova, Alice; Shutthanandan, Vaithiyalingam Environmental Science & Technology, Vol. 53, Issue 23 https://doi.org/10.1021/acs.est.9b04608	journal	November 2019
Rare Earth Element Binding and Recovery by a Beta Roll-Forming RTX Domain Khoury, Farid; Su, Zihang; Banta, Scott Inorganic Chemistry, Vol. 63, Issue 29 https://doi.org/10.1021/acs.inorgchem.4c00420	journal	July 2024
Gravity-Driven Separation for Enrichment of Rare Earth Elements Using Lanthanide Binding Peptide-Immobilized Resin Sree, Hrishitha; Swarup, Gitanjali; Gupta, Sharad ACS Applied Bio Materials, Vol. 7, Issue 12 https://doi.org/10.1021/acsabm.3c01280	journal	April 2024
Investigation of Rare Earth Element Binding to a Surface-Bound Affinity Peptide Derived from EF-Hand Loop I of Lanmodulin Verma, Geeta; Hostert, Jacob; Summerville, Alex A. ACS Applied Materials & Interfaces, Vol. 16, Issue 13 https://doi.org/10.1021/acsami.3c17565	journal	March 2024
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
Quantitative Determination of Metal Ion Adsorption on Cellulose Nanocrystals Surfaces Paul, Harrison R.; Bera, Mrinal K.; Macke, Nicholas ACS Nano, Vol. 18, Issue 3 https://doi.org/10.1021/acsnano.3c06140	journal	January 2024
Supramolecular Assembly of Lanthanide-Binding Tag Peptides for Aqueous Separation of Rare Earth Elements Ortuno Macias, Luis E.; Jiménez-Ángeles, Felipe; Kt, Surabh S. ACS Nano, Vol. 19, Issue 41 https://doi.org/10.1021/acsnano.5c05056	journal	October 2025
Catch and Release: Engineered Allosterically Regulated β-Roll Peptides Enable On/Off Biomolecular Recognition Bulutoglu, Beyza; Dooley, Kevin; Szilvay, Géza ACS Synthetic Biology, Vol. 6, Issue 9 https://doi.org/10.1021/acssynbio.7b00089	journal	May 2017
Binding of lanthanide ions to troponin C Wang, Chih-Lueh A.; Leavis, Paul C.; Horrocks, W. Dew Biochemistry, Vol. 20, Issue 9 https://doi.org/10.1021/bi00512a012	journal	April 1981
Tuning the Affinity for Lanthanides of Calcium Binding Proteins Bertini, Ivano; Gelis, Ioannis; Katsaros, Nikolaos Biochemistry, Vol. 42, Issue 26 https://doi.org/10.1021/bi034494z	journal	June 2003
Inducible Polymerization and Two-Dimensional Assembly of the Repeats-in-Toxin (RTX) Domain from thePseudomonas aeruginosaAlkaline Protease Zhang, Liang; Franks, Jonathon; Stolz, Donna B. Biochemistry, Vol. 53, Issue 41 https://doi.org/10.1021/bi5007546	journal	October 2014
A FRET-Based Method for Probing the Conformational Behavior of an Intrinsically Disordered Repeat Domain fromBordetella pertussisAdenylate Cyclase Szilvay, Géza R.; Blenner, Mark A.; Shur, Oren Biochemistry, Vol. 48, Issue 47 https://doi.org/10.1021/bi901447j	journal	November 2009
Characterization of Lanthanide Ion Binding to the EF-Hand Protein S100β by Luminescence Spectroscopy Chaudhuri, Dipankar; Horrocks, William DeW.; Amburgey, Judith C. Biochemistry, Vol. 36, Issue 32 https://doi.org/10.1021/bi9704358	journal	August 1997
Role of Metal Ions in the Self-assembly of the Alzheimer’s Amyloid-β Peptide Faller, Peter; Hureau, Christelle; Berthoumieu, Olivia Inorganic Chemistry, Vol. 52, Issue 21 https://doi.org/10.1021/ic4003059	journal	April 2013
Paramagnetically Induced Residual Dipolar Couplings for Solution Structure Determination of Lanthanide Binding Proteins Barbieri, Renato; Bertini, Ivano; Cavallaro, Gabriele Journal of the American Chemical Society, Vol. 124, Issue 19 https://doi.org/10.1021/ja025528d	journal	April 2002
Interaction of α-Synuclein with Divalent Metal Ions Reveals Key Differences: A Link between Structure, Binding Specificity and Fibrillation Enhancement Binolfi, Andrés; Rasia, Rodolfo M.; Bertoncini, Carlos W. Journal of the American Chemical Society, Vol. 128, Issue 30 https://doi.org/10.1021/ja0618649	journal	August 2006
Polyelectrolytes in Multivalent Salt Solutions: Monomolecular versus Multimolecular Aggregation Huang, Ching-I; Olvera de la Cruz, Monica Macromolecules, Vol. 35, Issue 3 https://doi.org/10.1021/ma010717m	journal	January 2002
Extent of N-terminus exposure of monomeric alpha-synuclein determines its aggregation propensity Stephens, Amberley D.; Zacharopoulou, Maria; Moons, Rani Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16564-3	journal	June 2020
Unveiling the solution structure of a DNA duplex with continuous silver-modified Watson-Crick base pairs Javornik, Uroš; Pérez-Romero, Antonio; López-Chamorro, Carmen Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-51876-8	journal	September 2024
The origins of binding specificity of a lanthanide ion binding peptide Hatanaka, Takaaki; Kikkawa, Nobuaki; Matsugami, Akimasa Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-76527-y	journal	November 2020
Structural models of intrinsically disordered and calcium-bound folded states of a protein adapted for secretion O’Brien, Darragh P.; Hernandez, Belen; Durand, Dominique Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14223	journal	September 2015
Evidence for Intramolecular Antiparallel Beta-Sheet Structure in Alpha-Synuclein Fibrils from a Combination of Two-Dimensional Infrared Spectroscopy and Atomic Force Microscopy Roeters, Steven J.; Iyer, Aditya; Pletikapić, Galja Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep41051	journal	January 2017
Stability, structural and functional properties of a monomeric, calcium–loaded adenylate cyclase toxin, CyaA, from Bordetella pertussis Cannella, Sara E.; Ntsogo Enguéné, Véronique Yvette; Davi, Marilyne Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42065	journal	February 2017
Trivalent cation-induced phase separation in proteins: ion specific contribution in hydration also counts Saha, Ria; Mitra, Rajib Kumar Physical Chemistry Chemical Physics, Vol. 24, Issue 38 https://doi.org/10.1039/D2CP01061E	journal	January 2022
Sequence-defined structural transitions by calcium-responsive proteins Chang, Marina P.; Huang, Winnie; Shambharkar, Gatha M. Polymer Chemistry, Vol. 15, Issue 47 https://doi.org/10.1039/D4PY00907J	journal	January 2024
Lanthanides compete with calcium for binding to cadherins and inhibit cadherin-mediated cell adhesion Brayshaw, Lewis L.; Smith, Rosanna C. G.; Badaoui, Magd Metallomics, Vol. 11, Issue 5 https://doi.org/10.1039/c8mt00317c	journal	January 2019
Metal-ion binding to parvalbumin. A 113Cd-n.m.r. study of the binding of different lanthanide ions Drakenberg, T.; Swärd, M.; Cavé, A. Biochemical Journal, Vol. 227, Issue 3 https://doi.org/10.1042/bj2270711	journal	May 1985
Copper(II)-induced self-oligomerization of α-synuclein Paik, Seung R.; Shin, Hyun-Ju; Lee, Ju-Hyun Biochemical Journal, Vol. 340, Issue 3 https://doi.org/10.1042/bj3400821	journal	June 1999
Coordination to lanthanide ions distorts binding site conformation in calmodulin Edington, Sean C.; Gonzalez, Andrea; Middendorf, Thomas R. Proceedings of the National Academy of Sciences, Vol. 115, Issue 14 https://doi.org/10.1073/pnas.1722042115	journal	March 2018
Amyloid β 42 fibril structure based on small-angle scattering Lattanzi, Veronica; André, Ingemar; Gasser, Urs Proceedings of the National Academy of Sciences, Vol. 118, Issue 48 https://doi.org/10.1073/pnas.2112783118	journal	November 2021
Lanthanide binding peptide surfactants at air–aqueous interfaces for interfacial separation of rare earth elements Ortuno Macias, Luis E.; Jiménez-Ángeles, Felipe; Marmorstein, Jason G. Proceedings of the National Academy of Sciences, Vol. 121, Issue 52 https://doi.org/10.1073/pnas.2411763121	journal	December 2024
RTX Calcium Binding Motifs Are Intrinsically Disordered in the Absence of Calcium: IMPLICATION FOR PROTEIN SECRETION Chenal, Alexandre; Guijarro, J. Iñaki; Raynal, Bertrand Journal of Biological Chemistry, Vol. 284, Issue 3 https://doi.org/10.1074/jbc.M807312200	journal	November 2008
Extractive Metallurgy of Rare Earths Krishnamurthy, Nagaiyar; Gupta, Chiranjib Kumar https://doi.org/10.1201/b19055	book	December 2015
Interdomain Contacts and the Stability of Serralysin Protease from Serratia marcescens Zhang, Liang; Morrison, Anneliese J.; Thibodeau, Patrick H. PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0138419	journal	September 2015
Handbook of Rare Earth Elements: Analytics Golloch, Alfred https://doi.org/10.1515/9783110365085	book	April 2017
Comparing α-Synuclein Fibrils Formed in the Absence and Presence of a Model Lipid Membrane: A Small and Wide-Angle X-Ray Scattering Study Dubackic, Marija; Linse, Sara; Sparr, Emma Frontiers in Soft Matter, Vol. 1 https://doi.org/10.3389/frsfm.2021.741996	journal	January 2022

Similar Records

Supramolecular Assembly of Lanthanide-Binding Tag Peptides for Aqueous Separation of Rare Earth Elements

Journal Article · Mon Oct 06 00:00:00 UTC 2025 · ACS Nano · OSTI ID:3000240

Ortuno Macias, Luis E.; Jiménez-Ángeles, Felipe; KT, Surabh S.; +7 more

X-ray absorption spectroscopy of lanmodulin-derived peptides bound to rare earth elements

Journal Article · Mon Sep 22 00:00:00 UTC 2025 · Journal of Synchrotron Radiation · OSTI ID:2997794

Smerigan, Adam; Hoffman, Adam S.; Perez-Aguilar, Jorge; +2 more

Structure of Bordetella pertussis peptidoglycan

Journal Article · Tue Sep 01 04:00:00 UTC 1987 · J. Bacteriol.; (United States) · OSTI ID:6075681

Folkening, W J; Nogami, W; Martin, S A; +1 more

Related Subjects

chemical structure
elements
ions
lanthanides
peptides
proteins

Title: Rare Earth Element-Induced Condensation of the Block V of the Repeats-in-Toxin Domain from CyaA from Bordetella pertussis for Separations

Citation Formats

References (58)

Similar Records

Related Subjects