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MamA as a Model Protein for Structure-Based Insight into the Evolutionary Origins of Magnetotactic Bacteria.

Zeytuni N, Cronin S, Lefèvre CT, Arnoux P, Baran D, Shtein Z, Davidov G, Zarivach R - PLoS ONE (2015)

Bottom Line: As such, this allows us to perform structural- and phylogenetic-based analyses using a variety of previously determined MamA from a diverse range of MTB species across various phylogenetic groups.We found that MamA has remained remarkably constant throughout evolution with minimal change between different taxa despite sequence variations.These findings, coupled with the generation of phylogenetic trees using both amino acid sequences and 16S rRNA, indicate that magnetotaxis likely did not spread via horizontal gene transfer and instead has a significantly earlier, primordial origin.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer Sheva, Israel.

ABSTRACT
MamA is a highly conserved protein found in magnetotactic bacteria (MTB), a diverse group of prokaryotes capable of navigating according to magnetic fields - an ability known as magnetotaxis. Questions surround the acquisition of this magnetic navigation ability; namely, whether it arose through horizontal or vertical gene transfer. Though its exact function is unknown, MamA surrounds the magnetosome, the magnetic organelle embedding a biomineralised nanoparticle and responsible for magnetotaxis. Several structures for MamA from a variety of species have been determined and show a high degree of structural similarity. By determining the structure of MamA from Desulfovibrio magneticus RS-1 using X-ray crystallography, we have opened up the structure-sequence landscape. As such, this allows us to perform structural- and phylogenetic-based analyses using a variety of previously determined MamA from a diverse range of MTB species across various phylogenetic groups. We found that MamA has remained remarkably constant throughout evolution with minimal change between different taxa despite sequence variations. These findings, coupled with the generation of phylogenetic trees using both amino acid sequences and 16S rRNA, indicate that magnetotaxis likely did not spread via horizontal gene transfer and instead has a significantly earlier, primordial origin.

No MeSH data available.


ArsTM crystal packing, asymmetric unit composition and overall structure.(A) ArsTM crystal packing and asymmetric unit composition. The molecules are shown in three rotation-related views. (B) Overlay of all six ArsTM monomers reveals the high degree of structural similarity. The representative ArsTM monomer contains five sequential TPR motifs. The molecule is shown in two views, related by a 90° rotation. (C) An overlay of representative monomers from ArsTM (green), MamAΔ41Mbav (PDB ID: 3VTX, orange) and Magnetospirillum species MamAΔ41AMB-1 (PDB ID: 3AS5 chain A and B in light pink and brown, respectively) related by a 180° rotation. A high structural similarity of MamAΔ41 between the species can be observed, apart from the helical conformation of the identical His-tag linker sequence remaining after thrombin proteolysis (H11: ELALVPR) seen in the 3AS5 chain B and 3VTX. In addition, a light flexibility is observed at the NTD of the monomers. All images were produced by PyMOL.
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pone.0130394.g004: ArsTM crystal packing, asymmetric unit composition and overall structure.(A) ArsTM crystal packing and asymmetric unit composition. The molecules are shown in three rotation-related views. (B) Overlay of all six ArsTM monomers reveals the high degree of structural similarity. The representative ArsTM monomer contains five sequential TPR motifs. The molecule is shown in two views, related by a 90° rotation. (C) An overlay of representative monomers from ArsTM (green), MamAΔ41Mbav (PDB ID: 3VTX, orange) and Magnetospirillum species MamAΔ41AMB-1 (PDB ID: 3AS5 chain A and B in light pink and brown, respectively) related by a 180° rotation. A high structural similarity of MamAΔ41 between the species can be observed, apart from the helical conformation of the identical His-tag linker sequence remaining after thrombin proteolysis (H11: ELALVPR) seen in the 3AS5 chain B and 3VTX. In addition, a light flexibility is observed at the NTD of the monomers. All images were produced by PyMOL.

Mentions: ArsTM monomers assemble to form a trimeric ring, each enclosing a ~15 Å diameter inner void (Fig 3A); the crystal asymmetric unit includes six ArsTM monomers arranged as two trimeric rings (Fig 4A). The employed forces that allow the stabilisation of each trimeric ring include salt bridges as well as hydrophobic interactions between the N-terminal of a single monomer and the C-terminal of a nearby monomer in a continuous manner, resulting in a ring with surface properties akin to a Möbius strip. These ring-stabilising salt bridges include a double salt bridge between Glu61 and Tyr65 from a single monomer to Gln183 from the nearby monomer, as well as a single salt bridge between Arg56 from a single monomer to Glu209 from the nearby monomer. The network of hydrophobic interactions includes Lys42, Leu45, Tyr46, Ile49, Arg52, Ser53, Arg64 and Glu68 from the N-terminal of a single monomer to Phe187, Val190, Ala198, Ala199, Phe202, Val205 and Met206 to the C-terminal of the nearby monomer (Fig 3B). As such, ArsTM presents a distinctly atypical binding surface since, as mentioned, the protein-protein interactions involving MamA typically bind via the concave or convex surfaces. Overall, the trimeric ring contains three of these identical, N-to-C-terminal interaction surfaces. Unexpectedly, but not altogether unsurprisingly, the triple mutated residues (E140A, K141A and E143A), along the ‘backbone’ of the monomers, were found to be at the centre of a crystal contact (S3 Fig). The tight packing of ArsTM within the crystal could not occur with the original residues, which contained long and charged side chains and hence, could not be crystallised. This interaction surface includes two symmetric backbone polar contacts between two monomers (Phe111 to Ala140), where each monomer originates from a different ring. In addition, the interaction surface is stabilised through double hydrophobic interactions between Pro142 to His 110 (S3 Fig).


MamA as a Model Protein for Structure-Based Insight into the Evolutionary Origins of Magnetotactic Bacteria.

Zeytuni N, Cronin S, Lefèvre CT, Arnoux P, Baran D, Shtein Z, Davidov G, Zarivach R - PLoS ONE (2015)

ArsTM crystal packing, asymmetric unit composition and overall structure.(A) ArsTM crystal packing and asymmetric unit composition. The molecules are shown in three rotation-related views. (B) Overlay of all six ArsTM monomers reveals the high degree of structural similarity. The representative ArsTM monomer contains five sequential TPR motifs. The molecule is shown in two views, related by a 90° rotation. (C) An overlay of representative monomers from ArsTM (green), MamAΔ41Mbav (PDB ID: 3VTX, orange) and Magnetospirillum species MamAΔ41AMB-1 (PDB ID: 3AS5 chain A and B in light pink and brown, respectively) related by a 180° rotation. A high structural similarity of MamAΔ41 between the species can be observed, apart from the helical conformation of the identical His-tag linker sequence remaining after thrombin proteolysis (H11: ELALVPR) seen in the 3AS5 chain B and 3VTX. In addition, a light flexibility is observed at the NTD of the monomers. All images were produced by PyMOL.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482739&req=5

pone.0130394.g004: ArsTM crystal packing, asymmetric unit composition and overall structure.(A) ArsTM crystal packing and asymmetric unit composition. The molecules are shown in three rotation-related views. (B) Overlay of all six ArsTM monomers reveals the high degree of structural similarity. The representative ArsTM monomer contains five sequential TPR motifs. The molecule is shown in two views, related by a 90° rotation. (C) An overlay of representative monomers from ArsTM (green), MamAΔ41Mbav (PDB ID: 3VTX, orange) and Magnetospirillum species MamAΔ41AMB-1 (PDB ID: 3AS5 chain A and B in light pink and brown, respectively) related by a 180° rotation. A high structural similarity of MamAΔ41 between the species can be observed, apart from the helical conformation of the identical His-tag linker sequence remaining after thrombin proteolysis (H11: ELALVPR) seen in the 3AS5 chain B and 3VTX. In addition, a light flexibility is observed at the NTD of the monomers. All images were produced by PyMOL.
Mentions: ArsTM monomers assemble to form a trimeric ring, each enclosing a ~15 Å diameter inner void (Fig 3A); the crystal asymmetric unit includes six ArsTM monomers arranged as two trimeric rings (Fig 4A). The employed forces that allow the stabilisation of each trimeric ring include salt bridges as well as hydrophobic interactions between the N-terminal of a single monomer and the C-terminal of a nearby monomer in a continuous manner, resulting in a ring with surface properties akin to a Möbius strip. These ring-stabilising salt bridges include a double salt bridge between Glu61 and Tyr65 from a single monomer to Gln183 from the nearby monomer, as well as a single salt bridge between Arg56 from a single monomer to Glu209 from the nearby monomer. The network of hydrophobic interactions includes Lys42, Leu45, Tyr46, Ile49, Arg52, Ser53, Arg64 and Glu68 from the N-terminal of a single monomer to Phe187, Val190, Ala198, Ala199, Phe202, Val205 and Met206 to the C-terminal of the nearby monomer (Fig 3B). As such, ArsTM presents a distinctly atypical binding surface since, as mentioned, the protein-protein interactions involving MamA typically bind via the concave or convex surfaces. Overall, the trimeric ring contains three of these identical, N-to-C-terminal interaction surfaces. Unexpectedly, but not altogether unsurprisingly, the triple mutated residues (E140A, K141A and E143A), along the ‘backbone’ of the monomers, were found to be at the centre of a crystal contact (S3 Fig). The tight packing of ArsTM within the crystal could not occur with the original residues, which contained long and charged side chains and hence, could not be crystallised. This interaction surface includes two symmetric backbone polar contacts between two monomers (Phe111 to Ala140), where each monomer originates from a different ring. In addition, the interaction surface is stabilised through double hydrophobic interactions between Pro142 to His 110 (S3 Fig).

Bottom Line: As such, this allows us to perform structural- and phylogenetic-based analyses using a variety of previously determined MamA from a diverse range of MTB species across various phylogenetic groups.We found that MamA has remained remarkably constant throughout evolution with minimal change between different taxa despite sequence variations.These findings, coupled with the generation of phylogenetic trees using both amino acid sequences and 16S rRNA, indicate that magnetotaxis likely did not spread via horizontal gene transfer and instead has a significantly earlier, primordial origin.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences and The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer Sheva, Israel.

ABSTRACT
MamA is a highly conserved protein found in magnetotactic bacteria (MTB), a diverse group of prokaryotes capable of navigating according to magnetic fields - an ability known as magnetotaxis. Questions surround the acquisition of this magnetic navigation ability; namely, whether it arose through horizontal or vertical gene transfer. Though its exact function is unknown, MamA surrounds the magnetosome, the magnetic organelle embedding a biomineralised nanoparticle and responsible for magnetotaxis. Several structures for MamA from a variety of species have been determined and show a high degree of structural similarity. By determining the structure of MamA from Desulfovibrio magneticus RS-1 using X-ray crystallography, we have opened up the structure-sequence landscape. As such, this allows us to perform structural- and phylogenetic-based analyses using a variety of previously determined MamA from a diverse range of MTB species across various phylogenetic groups. We found that MamA has remained remarkably constant throughout evolution with minimal change between different taxa despite sequence variations. These findings, coupled with the generation of phylogenetic trees using both amino acid sequences and 16S rRNA, indicate that magnetotaxis likely did not spread via horizontal gene transfer and instead has a significantly earlier, primordial origin.

No MeSH data available.