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

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          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.

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          Most cited references18

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          The atomic structure of protein-protein recognition sites.

          The non-covalent assembly of proteins that fold separately is central to many biological processes, and differs from the permanent macromolecular assembly of protein subunits in oligomeric proteins. We performed an analysis of the atomic structure of the recognition sites seen in 75 protein-protein complexes of known three-dimensional structure: 24 protease-inhibitor, 19 antibody-antigen and 32 other complexes, including nine enzyme-inhibitor and 11 that are involved in signal transduction.The size of the recognition site is related to the conformational changes that occur upon association. Of the 75 complexes, 52 have "standard-size" interfaces in which the total area buried by the components in the recognition site is 1600 (+/-400) A2. In these complexes, association involves only small changes of conformation. Twenty complexes have "large" interfaces burying 2000 to 4660 A2, and large conformational changes are seen to occur in those cases where we can compare the structure of complexed and free components. The average interface has approximately the same non-polar character as the protein surface as a whole, and carries somewhat fewer charged groups. However, some interfaces are significantly more polar and others more non-polar than the average. Of the atoms that lose accessibility upon association, half make contacts across the interface and one-third become fully inaccessible to the solvent. In the latter case, the Voronoi volume was calculated and compared with that of atoms buried inside proteins. The ratio of the two volumes was 1.01 (+/-0.03) in all but 11 complexes, which shows that atoms buried at protein-protein interfaces are close-packed like the protein interior. This conclusion could be extended to the majority of interface atoms by including solvent positions determined in high-resolution X-ray structures in the calculation of Voronoi volumes. Thus, water molecules contribute to the close-packing of atoms that insure complementarity between the two protein surfaces, as well as providing polar interactions between the two proteins. Copyright 1999 Academic Press.
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            Magnetotactic bacteria.

            Bacteria with motility directed by the local geomagnetic field have been observed in marine sediments. These magnetotactic microorganisms possess flagella and contain novel structured particles, rich in iron, within intracytoplasmic membrane vesicles. Conceivably these particles impart to cells a magnetic moment. This could explain the observed migration of these organisms in fields as weak as 0.5 gauss.
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              Ecology, diversity, and evolution of magnetotactic bacteria.

              Magnetotactic bacteria (MTB) are widespread, motile, diverse prokaryotes that biomineralize a unique organelle called the magnetosome. Magnetosomes consist of a nano-sized crystal of a magnetic iron mineral that is enveloped by a lipid bilayer membrane. In cells of almost all MTB, magnetosomes are organized as a well-ordered chain. The magnetosome chain causes the cell to behave like a motile, miniature compass needle where the cell aligns and swims parallel to magnetic field lines. MTB are found in almost all types of aquatic environments, where they can account for an important part of the bacterial biomass. The genes responsible for magnetosome biomineralization are organized as clusters in the genomes of MTB, in some as a magnetosome genomic island. The functions of a number of magnetosome genes and their associated proteins in magnetosome synthesis and construction of the magnetosome chain have now been elucidated. The origin of magnetotaxis appears to be monophyletic; that is, it developed in a common ancestor to all MTB, although horizontal gene transfer of magnetosome genes also appears to play a role in their distribution. The purpose of this review, based on recent progress in this field, is focused on the diversity and the ecology of the MTB and also the evolution and transfer of the molecular determinants involved in magnetosome formation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                26 June 2015
                2015
                : 10
                : 6
                : e0130394
                Affiliations
                [1 ]Department of Life Sciences and The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer Sheva, Israel
                [2 ]CEA/CNRS/Aix-Marseille Université, UMR 7265 Biologie Végétale et Microbiologie Environnementales, Laboratoire de Bioénergétique Cellulaire, Saint Paul les Durance, France
                Louisiana State University and A & M College, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NZ SC RZ. Performed the experiments: NZ SC CTL DB ZS GD. Analyzed the data: NZ SC CTL RZ. Contributed reagents/materials/analysis tools: CTL PA. Wrote the paper: NZ SC CTL RZ.

                Article
                PONE-D-15-09111
                10.1371/journal.pone.0130394
                4482739
                26114501
                33767cbe-1af4-4329-b61e-0d8d45cde293
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 2 March 2015
                : 20 May 2015
                Page count
                Figures: 6, Tables: 1, Pages: 17
                Funding
                This research was made possible through grants from the Israeli Ministry of Science, Technology and Space and EMBO, the European Molecular Biology Organisation.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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