1. Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria
- Author
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Béatrice Alonso, Magali Floriani, Camille Garau, Elodie Duprat, Christopher T. Lefèvre, Vincent Busigny, Sufal Swaraj, Caroline L. Monteil, Margot Coutaud, Eric Viollier, Didier Jézéquel, Martin Sachse, Romain Bolzoni, Nicolas Menguy, Karim Benzerara, Emmanuel Michot-Achdjian, Nicolas Ginet, Cécile C. Bidaud, François Guyot, François P. Mathon, Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB) (BIAM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Institut de minéralogie, de physique des matériaux et de cosmochimie (IMPMC), Muséum national d'Histoire naturelle (MNHN)-Institut de recherche pour le développement [IRD] : UR206-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Institut de Physique du Globe de Paris (IPG Paris), Laboratoire de chimie bactérienne (LCB), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut de Radioprotection et de Sûreté Nucléaire (IRSN), Synchrotron SOLEIL (SSOLEIL), Centre National de la Recherche Scientifique (CNRS), Plateforme BioImagerie Ultrastructurale – Ultrastructural BioImaging Platform (UTechS UBI), Institut Pasteur [Paris] (IP), Institut Universitaire de France (IUF), Ministère de l'Education nationale, de l’Enseignement supérieur et de la Recherche (M.E.N.E.S.R.), This work was supported by the CNRS: 'Programme national Ecosphère Continentale et Côtière (EC2CO)' (BACCARAT2 – N°13068) and the French National Research Agency (SIGMAG: ANR-18-CE31-0003 and PHOSTORE: ANR-19-CE01-0005-02). CCB was supported by the Frontières de l’Innovation en Recherche et Éducation (FIRE) Ph.D. programme from the Centre de Recherches Interdisciplinaires (CRI). Support for the confocal microscope was provided by the Région Provence Alpes Côte d’Azur, Conseil Général des Bouches du Rhône, French Ministry of Research, CNRS and Commissariat à l’Energie Atomique et aux Energies Alternatives., ANR-18-CE31-0003,SIGMAG,SIGNATURE DES MAGNETITES PRODUITES PAR LES BACTERIES MAGNETOTACTIQUES : PERSPECTIVES CHIMIQUES ET ISOTOPIQUES(2018), ANR-19-CE01-0005,PHOSTORE,Piégeage du phosphore : contribution des bactéries magnétotactiques dans les zones de transition oxique-anoxique(2019), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut de Physique du Globe de Paris, and Institut Pasteur [Paris]
- Subjects
Biomineralization ,[SDV]Life Sciences [q-bio] ,Magnetosome ,Carbonates ,Biology ,Microbiology ,Article ,03 medical and health sciences ,chemistry.chemical_compound ,In Situ Hybridization, Fluorescence ,Ecology, Evolution, Behavior and Systematics ,Alphaproteobacteria ,030304 developmental biology ,0303 health sciences ,030306 microbiology ,biology.organism_classification ,Ferrosoferric Oxide ,Calcium carbonate ,[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology ,chemistry ,Ultrastructure ,Biophysics ,Carbonate ,Magnetosomes ,Intracellular ,Bacteria - Abstract
International audience; Bacteria synthesize a wide range of intracellular submicrometer-sized inorganic precipitates of diverse chemical compositions and structures, called biominerals. Their occurrences, functions and ultrastructures are not yet fully described despite great advances in our knowledge of microbial diversity. Here, we report bacteria inhabiting the sediments and water column of the permanently stratified ferruginous Lake Pavin, that have the peculiarity to biomineralize both intracellular magnetic particles and calcium carbonate granules. Based on an ultrastructural characterization using transmission electron microscopy (TEM) and synchrotron-based scanning transmission X-ray microscopy (STXM), we showed that the calcium carbonate granules are amorphous and contained within membrane-delimited vesicles. Single-cell sorting, correlative fluorescent in situ hybridization (FISH), scanning electron microscopy (SEM) and molecular typing of populations inhabiting sediments affiliated these bacteria to a new genus of the Alphaproteobacteria. The partially assembled genome sequence of a representative isolate revealed an atypical structure of the magnetosome gene cluster while geochemical analyses indicate that calcium carbonate production is an active process that costs energy to the cell to maintain an environment suitable for their formation. This discovery further expands the diversity of organisms capable of intracellular Ca-carbonate biomineralization. If the role of such biomineralization is still unclear, cell behaviour suggests that it may participate to cell motility in aquatic habitats as magnetite biomineralization does.
- Published
- 2020