Widespread formation of intracellular calcium carbonates by the bloom‐forming cyanobacterium Microcystis

Abstract

The formation of intracellular amorphous calcium carbonates (iACC) has been recently observed in a few cultured strains of Microcystis, a potentially toxic bloom‐forming cyanobacterium found worldwide in freshwater ecosystems. If iACC‐forming Microcystis are abundant within blooms, they may represent a significant amount of particulate Ca. Here, we investigate the significance of iACC biomineralization by Microcystis. First, the presence of iACC‐forming Microcystis cells has been detected in several eutrophic lakes, indicating that this phenomenon occurs under environmental conditions. Second, some genotypic (presence/absence of ccyA, a marker gene of iACC biomineralization) and phenotypic (presence/absence of iACC) diversity have been detected within a collection of strains isolated from one single lake. This illustrates that this trait is frequent but also variable within Microcystis even at a single locality. Finally, one‐third of publicly available genomes of Microcystis were shown to contain the ccyA gene, revealing a wide geographic and phylogenetic distribution within the genus. Overall, the present work shows that the formation of iACC by Microcystis is common under environmental conditions. While its biological function remains undetermined, this process should be further considered regarding the biology of Microcystis and implications on the Ca geochemical cycle in freshwater environments.

Calcium speciation and coordination environment in intracellular amorphous calcium carbonate (ACC) formed by cyanobacteria

“…Furthermore, X-ray diffraction patterns of all ACC (+) strains showed the absence of calcite and any other crystalline carbonates, consistently with previous studies documenting the amorphous nature of the intracellular carbonates by TEM and FTIR [e.g. 15,39,48,50] (Figure S3).…”

“…The cell suspensions of all strains were harvested by centrifugation, rinsed, and dried at 40 o C for 48 hours. The presence/absence of ACC in these strains was assessed in a previous study by FTIR spectroscopy and electron microscopy [15,48] . Furthermore, X-ray diffraction patterns of all ACC (+) strains showed the absence of calcite and any other crystalline carbonates, consistently with previous studies documenting the amorphous nature of the intracellular carbonates by TEM and FTIR [e.g.…”

Searching for microbial contribution to micritization of shallow marine sediments

“…Bacteria can also actively control the biomineralization process, as evidenced in the case of the Gammaproteobacteria genus Achromatium (e.g., Achromatium oxaliferum ; Babenzien, 1991), capable of producing intracellular calcium carbonate precipitates (Gray, 2006; Gray & Head, 2014). Such a trait is also shared by an increasing diversity of cyanobacterial species (Benzerara et al, 2014; Couradeau et al, 2012; Gaëtan et al, 2023) as well as non‐phototrophic bacteria (Monteil et al, 2021). While the fate of these precipitates is not clear after cell death, their potential role in micrite formation within sediments should be considered in the future.…”

Calcium isotope fractionation by intracellular amorphous calcium carbonate (ACC) forming cyanobacteria

“…The formation of intracellular ACC by cyanobacteria also holds biogeochemical implications. Among ACC‐forming cyanobacteria, some can bloom and locally reach relatively high cell density, suggesting that they may produce significant amounts of ACC in these environments and perturb C and Ca cycles, although this remains to be demonstrated (Gaëtan et al., 2022). Moreover, the ACC inclusions formed by some cyanobacteria strains sequester high concentrations of alkaline earth elements such as Ba, Sr, and the radioactive 90 Sr and 226 Ra isotopes, which holds two implications: (1) these cyanobacteria may be overlooked actors in the biogeochemical cycles of these trace elements (Blondeau et al., 2018; Cam et al., 2016); (2) they may offer some potential for remediating pollution of these radioactive isotopes (Mehta et al., 2019; Mehta, Bougoure, et al., 2022).…”