Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

The ISME Journal volume 15, pages1–18(2021)Cite this article

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Abstract

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.

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Fig. 1: Observation of the refractive magnetotactic bacterium from Lake Pavin.
Fig. 2: Microscopy images of magnetotactic bacteria with electron-dense inclusions isolated from Lake Pavin sediment samples.
Fig. 3: Chemical identification of the mineral phase in the magnetosomes and the large inclusions of bacteria isolated from sediment samples.
Fig. 4: Evidence of strontium and barium in the calcium-rich inclusions.
Fig. 5: STXM analyses measured at the C K-edge on intracellular inclusions of magnetotactic bacteria isolated from Lake Pavin.
Fig. 6: Phylogenetic and magnetosome gene cluster (MGC) analyses of ACC-producing MTB isolated from sediment samples of Lake Pavin.
Fig. 7: Fluorescence in situ hybridization (FISH) of magnetically concentrated MTB from the sediments of Lake Pavin.

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Acknowledgements

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. We acknowledge the Institut de Radioprotection et de Sûreté Nucléaire (IRSN) at CEA Cadarache for the access of the transmission electron microscope Tecnai G2 BioTWIN. We are grateful to the INRA MIGALE bioinformatics platform (http://migale.jouy.inra.fr) for providing computational resources. We thank Stefan Stanescu and Rachid Belkhou for user support on the HERMES STXM beamline at Synchrotron SOLEIL, Fériel Skouri-Panet and Cynthia Travert for user support on the IMPMC Biology facility, Jean-Michel Guigner for user support on the IMPMC TEM facility and Imène Esteve, Béatrice Doisneau and Stéphanie Delbrel for user support on the IMPMC SEM facility. We are grateful to the genomic platform at the Institut de Microbiologie de la Méditerranée (IMM) and to Yann Denis for helpful advices. We thank Alexis Canette from the Service de Microscopie Electronique at the IBPS for his help in CEMOVIS sample preparation. We thank Maria Pilar Asta and Alejandro Fernandez-Martinez from ISTerre, University Grenoble Alpes, for providing a reference ACC sample.

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Author notes

  1. These authors contributed equally: Caroline L. Monteil, Karim Benzerara, Nicolas Menguy

Affiliations

  1. Aix-Marseille University, CNRS, CEA, UMR7265 Institute of Biosciences and Biotechnologies of Aix-Marseille (BIAM), CEA Cadarache, F-13108, Saint-Paul-lez-Durance, France

    Caroline L. Monteil, Cécile C. Bidaud, Emmanuel Michot-Achdjian, Romain Bolzoni, François P. Mathon, Béatrice Alonso, Camille Garau & Christopher T. Lefevre

  2. Sorbonne Université, Muséum National d’Histoire Naturelle, UMR CNRS 7590, IRD. Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie (IMPMC), 4 Place Jussieu, 75005, Paris, France

    Caroline L. Monteil, Karim Benzerara, Nicolas Menguy, Cécile C. Bidaud, Romain Bolzoni, Margot Coutaud, Elodie Duprat & François Guyot

  3. Université de Paris, Institut de Physique du Globe de Paris, CNRS, F-75005, Paris, France

    François P. Mathon, Didier Jézéquel, Eric Viollier & Vincent Busigny

  4. Laboratoire de Chimie Bactérienne, UMR 7283 CNRS, Aix-Marseille Université, Institut de Microbiologie de la Méditerranée, 13402, Marseille, France

    Nicolas Ginet

  5. Institut de Radioprotection et de Sûreté Nucléaire (IRSN), PRP-ENV/SERIS/LECO, Cadarache, Saint-Paul-lez-Durance, 13115, France

    Magali Floriani

  6. Synchrotron SOLEIL, L’Orme des Merisiers, Saint-Aubin-BP 48, 91192, Gif-sur-YVETTE cedex, France

    Sufal Swaraj

  7. Ultrastructural Bioimaging unit, Institut Pasteur, 24-28 rue du Docteur-Roux, 75015, Paris, France

    Martin Sachse

  8. Institut Universitaire de France, 75005, Paris, France

    Vincent Busigny & François Guyot

Authors
  1. Caroline L. Monteil
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  2. Karim Benzerara
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  3. Nicolas Menguy
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  4. Cécile C. Bidaud
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  5. Emmanuel Michot-Achdjian
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  6. Romain Bolzoni
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  7. François P. Mathon
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  8. Margot Coutaud
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  9. Béatrice Alonso
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  10. Camille Garau
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  11. Didier Jézéquel
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  12. Eric Viollier
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  13. Nicolas Ginet
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  14. Magali Floriani
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  15. Sufal Swaraj
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  16. Martin Sachse
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  17. Vincent Busigny
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  18. Elodie Duprat
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  19. François Guyot
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  20. Christopher T. Lefevre
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Corresponding author

Correspondence to Christopher T. Lefevre.

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Monteil, C.L., Benzerara, K., Menguy, N. et al. Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria. ISME J 15, 1–18 (2021). https://doi.org/10.1038/s41396-020-00747-3

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