Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

Abstract

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.

A Genetic Toolbox for the New Model Cyanobacterium Cyanothece PCC 7425: A Case Study for the Photosynthetic Production of Limonene

“…Interestingly, Cyanothece PCC 7425 grew up to increasing cell densities in response to increasing urea quantities, which needed to be supplied not all at once, but as small successive subdoses along cell growth (Supplementary Figure S1). Also interestingly, the maximal growth (biomass production) of Cyanothece PCC 7425 was greatly improved by supplementing the MM with both 9.52 mM NaHCO 3 and 2.92 mM CaCl 2 ( Figure 1A), in agreement with the previous finding that Cyanothece PCC 7425 forms intracellular calcium carbonate granules (De Wever et al, 2019).…”

The diversity of molecular mechanisms of carbonate biomineralization by bacteria

“…However, no molecular actor has been identified yet which might be exclusively shared by all iACC-forming cyanobacteria. Genes coding for Ca 2+ /H + exchangers, and diverse calcium/cation exchangers, all involved in Ca active transport, have been found in all studied genomes of iACC-forming cyanobacteria [160]. Genes coding for a mechanosensitive channel have also been found in all these genomes.…”

“…This active transport may be at least partly at the origin of the energy cost of this biomineralization pathway and explain how cyanobacteria can form ACC in otherwise undersaturated extracellular solutions [165]. Following the same line of a strong connection between ACC biomineralization and a particular Ca homeostasis, De Wever et al [160] showed that iACC-forming cyanobacteria incorporate much more Ca than other cyanobacteria. Moreover, some of the iACC-forming strains require higher Ca concentrations to grow well.…”

“…All the members of the Thermosynechococcus elongatus BP-1 clade, shared the ability to form iACC showing that this biomineralization process is heritable, and might be ancient [43]. Moreover, two types of intracellular distributions of the inclusions were observed among the 16 iACC-forming strains known so far: iACC granules were scattered throughout the cells in 11 cyanobacteria, whereas they were located at cell poles and septa in five other cyanobacteria [14,43,160,162] (Fig. 5).…”

“…There are 21 ± 5 inclusions per cells on average, occupying ~ 6% of the total cell volume and these inclusions measure 270 ± 44 nm in diameter. Fifteen additional cultivable cyanobacterial strains were later found to form intracellular ACC (iACC) [43,160] (see Additional file 2). Some of these strains had been extensively studied before, including by TEM, supporting the idea that they have been overlooked.…”