Magnetotactic Bacteria Affiliated with Diverse Pseudomonadota Families Biomineralize Intracellular Ca-carbonate

Overview

Journal ISME J

Publisher Oxford University Press

Date 2025 Jan 8

PMID 39776138

Authors

Camille C Mangin

Karim Benzerara

Marine Bergot

Nicolas Menguy

Beatrice Alonso

Stephanie Fouteau

Raphael Meheust

Daniel M Chevrier

Daniel Chevrier

Christian Godon

Elsa Turrini

Neha Mehta

Arnaud Duverger

Cynthia Travert

Vincent Busigny

Elodie Duprat

Romain Bolzoni

Corinne Cruaud

Eric Viollier

Didier Jezequel

David Vallenet

Christopher T Lefevre

Caroline L Monteil

Affiliations

Soon will be listed here.

Abstract

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.

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