Magnetotactic bacteria affiliated with diverse <i>Pseudomonadota</i> families biomineralize intracellular Ca-carbonate
Intracellular calcium carbonate formation has long been associated with a single genus of giant Gammaproteobacteria, Achromatium. However, this biomineralization has recently received increasing attention after being observed in photosynthetic Cyanobacteriota and in two families of magnetotactic bacteria affiliated with the Alphaproteobacteria. In the latter group, bacteria form not only intracellular amorphous calcium carbonates into large inclusions that are refringent under the light microscope, but also intracellular ferrimagnetic crystals into organelles called magnetosomes. Here new observations suggest that magnetotactic bacteria previously identified in the sediments and water column of Lake Pavin (France) were only a small fraction of the diversity of bacteria producing intracellular amorphous calcium carbonates. To explore this diversity further, we conducted a comprehensive investigation of magnetotactic populations with refractive granules using a combination of environmental microbiology, genomic and mineralogy approaches on cells sorted by micromanipulation. Several species belonging to divergent genera of two Pseudomonadota classes were identified and characterized. Scanning transmission electron microscopy coupled with energy-dispersive X-ray spectrometry support that all these species indeed form intracellular amorphous calcium carbonates. Cryo soft X-ray tomography experiments conducted on ice-vitrified cells, enabled 3D investigation of inclusions volume, which was found to occupy 44-68% of the cell volume. Metabolic network modeling highlighted different metabolic abilities of Alpha- and Gammaproteobacteria, including methylotrophy and CO2 fixation via the reverse Krebs cycle or the Calvin-Benson-Bassham cycle. Overall, this study strengthens a convergent evolution scenario for intracellular carbonatogenesis in Bacteria, and further supports that it is promoted by the fixation of CO2 in anoxic environments.
Authors
- Nicolas Menguy (ORCID: https://orcid.org/0000-0003-4613-2490)
- Caroline Monteil (ORCID: https://orcid.org/0000-0002-2834-6834)
- Stéphanie Fouteau (ORCID: https://orcid.org/0000-0003-4720-4951)
- Camille Mangin
- Béatrice Alonso
- Daniel M. Chevrier (ORCID: https://orcid.org/0000-0002-0914-6714)
- Marine Bergot
- Karim Benzerara (ORCID: https://orcid.org/0000-0002-0553-0137)
- Christopher T. Lefèvre (ORCID: https://orcid.org/0000-0002-1692-0245)
- Corinne Cruaud (ORCID: https://orcid.org/0000-0002-4752-7278)
- Romain Bolzoni (ORCID: https://orcid.org/0000-0002-5741-3856)
- Cynthia Travert (ORCID: https://orcid.org/0009-0001-5108-6911)
- David Vallenet (ORCID: https://orcid.org/0000-0001-6648-0332)
- Éric Viollier (ORCID: https://orcid.org/0000-0002-8863-4563)
- Vincent Busigny (ORCID: https://orcid.org/0000-0001-7556-0772)
- Raphaël Méheust (ORCID: https://orcid.org/0000-0002-4847-426X)
- Neha Mehta (ORCID: https://orcid.org/0000-0002-7312-6398)
- Élodie Duprat (ORCID: https://orcid.org/0000-0003-4150-6967)
- Didier Jézéquel (ORCID: https://orcid.org/0000-0002-1983-9899)
- Arnaud Duverger (ORCID: https://orcid.org/0000-0001-5347-1701)
- Christian Godon
- Elsa Turrini
Institutions
- Centre National de la Recherche Scientifique (FR)
- Institut de physique du globe de Paris (FR)
- Université de Versailles Saint-Quentin-en-Yvelines (FR)
- Université Paris Cité (FR)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- Université Paris-Saclay (FR)
- Sorbonne Université (FR)
- Laboratoire de Minéralogie & Cosmochimie du Muséum (FR)
- Génomique Métabolique du Genoscope (FR)
- CEA Cadarache (FR)
- Genoscope (FR)
- Muséum national d'Histoire naturelle (FR)
- Laboratoire des Sciences du Climat et de l'Environnement (FR)
- CEA Paris-Saclay (FR)
- Institut de minéralogie, de physique des matériaux et de cosmochimie (FR)
- Institut de Biosciences et Biotechnologies (FR)
- Université Savoie Mont Blanc (FR)
Publication Details
- Journal
- The ISME Journal
- Published
- 2025-01-01
- DOI
- https://doi.org/10.1093/ismejo/wrae260
- Citations
- 13
- Primary Topic
- Geomagnetism and Paleomagnetism Studies
- Type
- article
- Field-Weighted Citation Impact
- 10.48
Funders
- Aix-Marseille Université
- European Commission
- Agence Nationale de la Recherche
- Institut de Radioprotection et de SÛreté Nucléaire
- Centre National de la Recherche Scientifique
- Institut National de la Recherche Agronomique