Limits...
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.


NTD stabilisation of MamAΔ41 from different species.(A) Detailed representation of the interactions stabilising the ArsTM NTD. The ArsTM NTD is stabilised by a diverse network of hydrophobic interactions. (B) Detailed representation of the interactions stabilising the MamAΔ41Mbav NTD. The MamAΔ41Mbav NTD is stabilised by a diverse network of hydrogen bonds and a single non-conserved salt bridge. (C) Detailed representation of the interactions stabilising the MamAΔ41AMB-1 NTD. The MamAΔ41AMB-1 NTD is stabilised through numerous hydrophobic interactions, a few hydrogen bonds and a single conserved salt bridge. Both NTD domains are shown in two views, related by a 90° rotation.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4482739&req=5

pone.0130394.g005: NTD stabilisation of MamAΔ41 from different species.(A) Detailed representation of the interactions stabilising the ArsTM NTD. The ArsTM NTD is stabilised by a diverse network of hydrophobic interactions. (B) Detailed representation of the interactions stabilising the MamAΔ41Mbav NTD. The MamAΔ41Mbav NTD is stabilised by a diverse network of hydrogen bonds and a single non-conserved salt bridge. (C) Detailed representation of the interactions stabilising the MamAΔ41AMB-1 NTD. The MamAΔ41AMB-1 NTD is stabilised through numerous hydrophobic interactions, a few hydrogen bonds and a single conserved salt bridge. Both NTD domains are shown in two views, related by a 90° rotation.

Mentions: MamA proteins from different species display a high degree of sequence and structural similarity (S2 Fig) [11,19]. Most of the fully conserved residues are related to the TPR motif consensus sequence apart from Asp159. Previous work on Magnetospirillum species revealed that mutating Asp159 had no effect on the overall structure of MamAΔ41, MamA complex formation or the in vivo sub-cellular localisation to the magnetosome chain [19]. Nevertheless, it is possible that Asp159 mediates other cellular protein-protein interactions with MamA. In addition to Asp159, two other MamA residues, Arg50 and Asp79, were considered to be highly conserved in all available species prior to the release of Mbav and BW-1 (a magnetotactic Deltaproteobacteria) sequences. The determined structures of MamA from Magnetospirillum species revealed that Arg50 and Asp79 form a salt bridge that stabilises the NTD by connecting the TPR1 and TPR2 motifs. Whilst these salt bridge-forming residues are conserved in ArsTM (Arg47 and Asp76), the salt bridge itself is not since the distance between these two residues is too great (Fig 5A). Furthermore, due to steric interference by the large Trp69, clearly shown in the structure, we could find no rotameric combinations for Arg47 and Asp76 capable of forming the salt bridge around Trp69. Trp69 occupies a large volume and is part of an extensive hydrophobic surface that stabilises the NTD packing. We presume that, due to the large volume of the Trp69 side chain, motifs TPR1 and TPR2 cannot be packed as tightly as their homologous motifs from Magnetospirillum species and MamAΔ41Mbav (Fig 5B & 5C).


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)

NTD stabilisation of MamAΔ41 from different species.(A) Detailed representation of the interactions stabilising the ArsTM NTD. The ArsTM NTD is stabilised by a diverse network of hydrophobic interactions. (B) Detailed representation of the interactions stabilising the MamAΔ41Mbav NTD. The MamAΔ41Mbav NTD is stabilised by a diverse network of hydrogen bonds and a single non-conserved salt bridge. (C) Detailed representation of the interactions stabilising the MamAΔ41AMB-1 NTD. The MamAΔ41AMB-1 NTD is stabilised through numerous hydrophobic interactions, a few hydrogen bonds and a single conserved salt bridge. Both NTD domains are shown in two views, related by a 90° rotation.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0130394.g005: NTD stabilisation of MamAΔ41 from different species.(A) Detailed representation of the interactions stabilising the ArsTM NTD. The ArsTM NTD is stabilised by a diverse network of hydrophobic interactions. (B) Detailed representation of the interactions stabilising the MamAΔ41Mbav NTD. The MamAΔ41Mbav NTD is stabilised by a diverse network of hydrogen bonds and a single non-conserved salt bridge. (C) Detailed representation of the interactions stabilising the MamAΔ41AMB-1 NTD. The MamAΔ41AMB-1 NTD is stabilised through numerous hydrophobic interactions, a few hydrogen bonds and a single conserved salt bridge. Both NTD domains are shown in two views, related by a 90° rotation.
Mentions: MamA proteins from different species display a high degree of sequence and structural similarity (S2 Fig) [11,19]. Most of the fully conserved residues are related to the TPR motif consensus sequence apart from Asp159. Previous work on Magnetospirillum species revealed that mutating Asp159 had no effect on the overall structure of MamAΔ41, MamA complex formation or the in vivo sub-cellular localisation to the magnetosome chain [19]. Nevertheless, it is possible that Asp159 mediates other cellular protein-protein interactions with MamA. In addition to Asp159, two other MamA residues, Arg50 and Asp79, were considered to be highly conserved in all available species prior to the release of Mbav and BW-1 (a magnetotactic Deltaproteobacteria) sequences. The determined structures of MamA from Magnetospirillum species revealed that Arg50 and Asp79 form a salt bridge that stabilises the NTD by connecting the TPR1 and TPR2 motifs. Whilst these salt bridge-forming residues are conserved in ArsTM (Arg47 and Asp76), the salt bridge itself is not since the distance between these two residues is too great (Fig 5A). Furthermore, due to steric interference by the large Trp69, clearly shown in the structure, we could find no rotameric combinations for Arg47 and Asp76 capable of forming the salt bridge around Trp69. Trp69 occupies a large volume and is part of an extensive hydrophobic surface that stabilises the NTD packing. We presume that, due to the large volume of the Trp69 side chain, motifs TPR1 and TPR2 cannot be packed as tightly as their homologous motifs from Magnetospirillum species and MamAΔ41Mbav (Fig 5B & 5C).

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.