HOW CYANOBACTERIA BORE

Some cyanobacteria can bore into carbonates, and are global players in the erosive reworking of limestones, coral reefs and carbonate sands. In spite of their importance, the mechanism of excavation remains unknown. In fact, it represents a geochemical paradox, in that autotrophic metabolism should promote precipitation instead. We have previously advanced mechanistic models to overcome this paradox based on either temporal or spatial separation of photosynthesis and boring, or on the active removal of Ca²⁺ by the cells. Until now, experimental approaches were hampered by the lack of cyanobacteria that could bore in the laboratory. We report here on investigations using a novel isolate (BC00) that can.

Microenvironments around BC008 filaments actively boring on calcite chips were monitored quantitatively for Ca²⁺ using in vivo fluorophore-enabled confocal fluorescence microscopy. The temporal dynamics of a variety of inhibitors were tracked using this system. PCR-based methods were used to detect and track the differential expression of genes putatively involved in boring. We could reject all mechanistic hypotheses but that based on Ca²⁺ transport. Ca-bearing carbonates, or those containing its biochemical analog Sr, were bored; not those with Mg, Mg/Ca, Mn, Fe, K, or Na as metal. Imaging of Ca²⁺ in and around the boreholes of actively boring BC008 demonstrated an active uptake Ca²⁺ at the apical end cell (severe undersaturation) and extrusion at the opposite end of the filaments (supersaturation). This out-of-equilibrium state could be relaxed by i) ceasing illumination, ii) adding inhibitors of ATP generation, and iii) adding specific inhibitors of P-type calcium ATPases. P-type ATPase genes could be detected in BC008’s genome, and showed up-regulation in the presence of solid calcite.

Cyanobacteria thus bore by actively taking up Ca²⁺ from the leading end of a filament at the cost of energy, locally lowering extracellular Ca²⁺ levels to the point that mineral equilibrium is displaced towards dissolution there. Ca²⁺ is then subject to trans-cellular transport along the filament and extruded at the lagging end to the outside aqueous medium. Proton antiport likely maintains charge and neutralizes alkalization by excess carbonate ions. Ensuing free CO₂ is likely fixed into biomass through photosynthesis.