Structural Basis for Rare Earth Element Recognition by Methylobacterium extorquens Lanmodulin

Erik C. Cook, Emily R. Featherston, Scott A. Showalter, Joseph Alfred Cotruvo, Jr.

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Lanmodulin (LanM) is a high-affinity lanthanide (Ln)-binding protein recently identified in Methylobacterium extorquens, a bacterium that requires Lns for the function of at least two enzymes. LanM possesses four EF-hands, metal coordination motifs generally associated with Ca II binding, but it undergoes a metal-dependent conformational change with a 100 million-fold selectivity for Ln III s and Y III over Ca II . Here we present the nuclear magnetic resonance solution structure of LanM complexed with Y III . This structure reveals that LanM features an unusual fusion of adjacent EF-hands, resulting in a compact fold to the best of our knowledge unique among EF-hand-containing proteins. It also supports the importance of an additional carboxylate ligand in contributing to the protein's picomolar affinity for Ln III s, and it suggests a role of unusual N i+1 -H···N i hydrogen bonds, in which LanM's unique EF-hand proline residues are engaged, in selective Ln III recognition. This work sets the stage for a detailed mechanistic understanding of LanM's Ln selectivity, which may inspire new strategies for binding, detecting, and sequestering these technologically important metals.

Original languageEnglish (US)
Pages (from-to)120-125
Number of pages6
JournalBiochemistry
Volume58
Issue number2
DOIs
StatePublished - Jan 15 2019

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Methylobacterium extorquens
Lanthanoid Series Elements
EF Hand Motifs
Rare earth elements
Metals
Proline
Hydrogen
Bacteria
Carrier Proteins
Hydrogen bonds
Proteins
Magnetic Resonance Spectroscopy
Fusion reactions
Nuclear magnetic resonance
Ligands
Enzymes

All Science Journal Classification (ASJC) codes

  • Biochemistry

Cite this

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abstract = "Lanmodulin (LanM) is a high-affinity lanthanide (Ln)-binding protein recently identified in Methylobacterium extorquens, a bacterium that requires Lns for the function of at least two enzymes. LanM possesses four EF-hands, metal coordination motifs generally associated with Ca II binding, but it undergoes a metal-dependent conformational change with a 100 million-fold selectivity for Ln III s and Y III over Ca II . Here we present the nuclear magnetic resonance solution structure of LanM complexed with Y III . This structure reveals that LanM features an unusual fusion of adjacent EF-hands, resulting in a compact fold to the best of our knowledge unique among EF-hand-containing proteins. It also supports the importance of an additional carboxylate ligand in contributing to the protein's picomolar affinity for Ln III s, and it suggests a role of unusual N i+1 -H···N i hydrogen bonds, in which LanM's unique EF-hand proline residues are engaged, in selective Ln III recognition. This work sets the stage for a detailed mechanistic understanding of LanM's Ln selectivity, which may inspire new strategies for binding, detecting, and sequestering these technologically important metals.",
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Structural Basis for Rare Earth Element Recognition by Methylobacterium extorquens Lanmodulin. / Cook, Erik C.; Featherston, Emily R.; Showalter, Scott A.; Cotruvo, Jr., Joseph Alfred.

In: Biochemistry, Vol. 58, No. 2, 15.01.2019, p. 120-125.

Research output: Contribution to journalArticle

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N2 - Lanmodulin (LanM) is a high-affinity lanthanide (Ln)-binding protein recently identified in Methylobacterium extorquens, a bacterium that requires Lns for the function of at least two enzymes. LanM possesses four EF-hands, metal coordination motifs generally associated with Ca II binding, but it undergoes a metal-dependent conformational change with a 100 million-fold selectivity for Ln III s and Y III over Ca II . Here we present the nuclear magnetic resonance solution structure of LanM complexed with Y III . This structure reveals that LanM features an unusual fusion of adjacent EF-hands, resulting in a compact fold to the best of our knowledge unique among EF-hand-containing proteins. It also supports the importance of an additional carboxylate ligand in contributing to the protein's picomolar affinity for Ln III s, and it suggests a role of unusual N i+1 -H···N i hydrogen bonds, in which LanM's unique EF-hand proline residues are engaged, in selective Ln III recognition. This work sets the stage for a detailed mechanistic understanding of LanM's Ln selectivity, which may inspire new strategies for binding, detecting, and sequestering these technologically important metals.

AB - Lanmodulin (LanM) is a high-affinity lanthanide (Ln)-binding protein recently identified in Methylobacterium extorquens, a bacterium that requires Lns for the function of at least two enzymes. LanM possesses four EF-hands, metal coordination motifs generally associated with Ca II binding, but it undergoes a metal-dependent conformational change with a 100 million-fold selectivity for Ln III s and Y III over Ca II . Here we present the nuclear magnetic resonance solution structure of LanM complexed with Y III . This structure reveals that LanM features an unusual fusion of adjacent EF-hands, resulting in a compact fold to the best of our knowledge unique among EF-hand-containing proteins. It also supports the importance of an additional carboxylate ligand in contributing to the protein's picomolar affinity for Ln III s, and it suggests a role of unusual N i+1 -H···N i hydrogen bonds, in which LanM's unique EF-hand proline residues are engaged, in selective Ln III recognition. This work sets the stage for a detailed mechanistic understanding of LanM's Ln selectivity, which may inspire new strategies for binding, detecting, and sequestering these technologically important metals.

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