The Role of Cell Compartmentalization and Cell Differentiation in Cyanobacterial Excavation of Miineral Carbonates

Abstract:

The bioerosion of coastal limestones and biogenic carbonates by boring filamentous or pseudo-filamentous cyanobacteria is not only a geomicrobial phenomenon of global proportions, but also plays an important role in the demise of coral reefs, and affects significantly human enterprises like bivalve fisheries. In spite of its importance, the mechanism by which cyanobacteria excavate carbonates constitutes an apparent paradox, in that their metabolism will tend to precipitate carbonates, not dissolved them. We have previously advanced, and obtained evidence for, a mechanism of excavation that relies on the uptake of Ca²⁺ by cells at the boring front, its trans-cellular transport along the filaments, and its eventual active excretion at the solid/liquid interface. It was postulated that the mechanism involved the strategically organized deployment of Ca²⁺ transport enzymes like P-type Ca²⁺ ATPases and Ca²⁺ channels. Here we present evidence that confirms this basic mechanism, but also reveals that it is based on an unexpected level of cellular complexity. The model organism Mastigocoleus testarum BC008, transports Ca²⁺ from the mineral to the external medium using a repetitive, polar arrangement of Ca²⁺ ATPases, localized preferentially on one cellular pole, in a ring conformation on the cell membrane adjacent to the trans-cellular septum, pumping Ca²⁺ locally towards the periplasmic space, from which it passively enters the next cell. This strain also develops specialized groups of cells, which we named calcicytes, often but not exclusively located at the ends of filaments, that accumulate large concentrations of Ca²⁺, some 40-fold higher than typical in microbes, and seem to act as sinks or capacitors in the trans-cellular Ca²⁺ transport. Calcicytes are also characterized by a lack of photosynthetic pigments, and a very high intracellular pH. These cellular adaptations can also be found in evolutionary distant euendoliths such as the pseudofilamentous Hyella sp.