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.

Several species of cyanobacteria biomineralizing intracellular amorphous calcium carbonates (ACC) were recently discovered. However, the mechanisms involved in this biomineralization process and the determinants discriminating species forming intracellular ACC from those not forming intracellular ACC remain unknown. Recently, it was hypothesized that the intensity of Ca uptake (i.e., how much Ca was scavenged from the extracellular solution) might be a major parameter controlling the capability of a cyanobacterium to form intracellular ACC. Here, we tested this hypothesis by systematically measuring the Ca uptake by a set of 52 cyanobacterial strains cultured in the same growth medium. The results evidenced a dichotomy among cyanobacteria regarding Ca sequestration capabilities, with all strains forming intracellular ACC incorporating significantly more calcium than strains not forming ACC. Moreover, Ca provided at a concentration of 50 μM in BG‐11 was shown to be limiting for the growth of some of the strains forming intracellular ACC, suggesting an overlooked quantitative role of Ca for these strains. All cyanobacteria forming intracellular ACC contained at least one gene coding for a mechanosensitive channel, which might be involved in Ca influx, as well as at least one gene coding for a Ca2+/H+ exchanger and membrane proteins of the UPF0016 family, which might be involved in active Ca transport either from the cytosol to the extracellular solution or the cytosol toward an intracellular compartment. Overall, massive Ca sequestration may have an indirect role by allowing the formation of intracellular ACC. The latter may be beneficial to the growth of the cells as a storage of inorganic C and/or a buffer of intracellular pH. Moreover, high Ca scavenging by cyanobacteria biomineralizing intracellular ACC, a trait shared with endolithic cyanobacteria, suggests that these cyanobacteria should be considered as potentially significant geochemical reservoirs of Ca.

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The response in metal concentrations and isotopic composition to variations in photosynthetic activity of aquatic micro-organisms is crucially important for understanding the environmental controls on metal fluxes and isotope excursions. Here we studied the impacts of two successive diel cycles on physicochemical parameters, Cu and Zn concentrations, and isotopic composition in solution in the presence of mature phototrophic biofilm in a rotating annular bioreactor. The diel cycles induced fluctuations in temperature, pH, and dissolved oxygen concentration following the variation in the photosynthesis activity of the biofilm. Diel variations in metal concentrations were primarily related to the pH variation, with an increase in metal concentration in solution related to a pH decrease. For both metals, δ( 66 Zn) and δ( 65 Cu) in solution exhibited complex but reproducible diel cycles. Diel variations in photosynthetic activity led to alternatively positive and negative isotope fractionation, producing the sorption of light Zn (Δ( 66 Zn sorbed-solution ) = −0.1 ± 0.06‰) and heavy Cu isotopes (Δ( 65 Cu sorbed-solution ) = +0.17 ± 0.06‰) during the day at high pH and the excretion of lighter Zn isotopes (−0.4‰ < Δ( 66 Zn excreted-biofilm ) < +0.14‰) and heavy Cu isotopes (Δ( 65 Cu excreted-biofilm ) = +0.7 ± 0.3‰) during the night at lower pH. We interpreted Zn and Cu diel cycles as a combination of a desorption of exopolymeric substance−metal complexes and a small active efflux during the night with adsorption and incorporation via an active uptake during the day. The hysteresis of metal concentration in solution over the diel cycle suggested the more important role of uptake compared to desorption and efflux from the biofilm. The phototrophic biofilm presents a non-negligible highly labile metal pool with important potential for contrasting isotopic fractionation at the diel scale.