Biomineralization Patterns of Intracellular Carbonatogenesis in Cyanobacteria: Molecular Hypotheses

Abstract

Abstract:The recent discovery of intracellular carbonatogenesis in several cyanobacteria species has challenged the traditional view that this process was extracellular and not controlled. However, a detailed analysis of the size distribution, chemical composition and 3-D-arrangement of carbonates in these cyanobacteria is lacking. Here, we characterized these features in Candidatus Gloeomargarita lithophora C7 and Candidatus Synechococcus calcipolaris G9 by conventional transmission electron microscopy, tomography, ultramicrotomy, and scanning transmission X-ray microscopy (STXM). Both Ca. G. lithophora C7 and Ca. S. calcipolaris G9 formed numerous polyphosphate granules adjacent or engulfing Ca-carbonate inclusions when grown in phosphate-rich solutions. Ca-carbonates were scattered within Ca. G. lithophora C7 cells under these conditions, but sometimes arranged in one or several chains. In contrast, Ca-carbonates formed at cell septa in Ca. S. calcipolaris G9 and were segregated equally between daughter cells after cell division, arranging as distorted disks at cell poles. The size distribution of carbonates evolved from a positively to a negatively skewed distribution as particles grew. Conventional ultramicrotomy did not preserve Ca-carbonates explaining partly why intracellular calcification has been overlooked in the past. All these new observations allow discussing with unprecedented insight some nucleation and growth processes occurring in intracellularly calcifying cyanobacteria with a particular emphasis on the possible involvement of intracellular compartments and cytoskeleton.

Intracellular amorphous carbonates uncover a new biomineralization process in eukaryotes

“…S4). A very similar feature has been described in cyanobacteria featuring ACC inclusions (Li et al., ).…”

“…Finally, intracellular formation of ACC requires supersaturation with Ca carbonates in the cytoplasm. Although the present state of our research does not allow to judge, this can be either the result of concentration inside intracellular vesicles or due to high viscosity of the cytoplasm creating local chemical heterogeneities (Li et al., ).…”

“…Some electron‐transparent features, attributed to starch grains, could perhaps represent the location of dissolved micropearls. Interestingly, a recent study showed that conventional preparation by ultramicrotomy fails in preserving intracellular carbonate inclusions in cyanobacteria (Li et al., ).…”

“…Moreover, the comparison between two cyanobacteria strains producing intracellular ACC inclusions ( Candidatus Gloeomargarita lithophora C7 and Candidatus Synechococcus calcipolaris G9), both cultivated in two different media, showed that the chemical compositions of the carbonate inclusions varied mostly with the nature of the cyanobacterial strain, independently of the medium in which they were grown (Li et al., ). As previously stated, our results similarly indicate that the chemical composition of the micropearls seems characteristic of the eukaryote organism which produces them.…”

Beachrock formation via microbial dissolution and re-precipitation of carbonate minerals

“…While the molecular structure and chemical reactivity of EPS produced by a biofilm can vary, depending on the environment in which the biofilm is growing, the ability of EPS to bind metal ions is universal (Rietveld, 1969;De Philippis and Vincenzini, 1998;Gutierrez et al, 2012;Li et al, 2016). In beachrock, locally high concentrations of cations released into solution via microbial boring would typically be washed away from the system with the onset of the next high tide.…”