MECHANISMS FOR BIOEROSION IN EUENDOLITHIC CYANOBACTERIA: MINERALS, ENZYMES AND BUGS

Some cyanobacteria, referred to as boring or euendolithic, are capable of excavating tunnels into calcareous substrates, both mineral and biogenic. The erosive activity of these cyanobacteria results in the destruction of coastal limestones and dead corals, the reworking of carbonate sands, and the cementation of microbialites. They thus link the biological and mineral parts of the global carbon cycle directly. They are also relevant for marine aquaculture as pests of mollusk populations. In spite of their importance, the mechanism by which these cyanobacteria bore have remained obscure until recently. To approach this paradox experimentally we have developed an empirical model based on a newly isolated euendolith (Mastigocoleus testarum BC008). Using this model, mechanistic hypotheses suggesting the aid of accompanying heterotrophic bacteria, or the spatial/temporal separation of photosynthesis and boring could be readily rejected. BC008 bores on pure calcite and other calcium and strontium carbonates in the laboratory under controlled conditions, but not on other calcium minerals or on non-calcium carbonates. This diversity of substrates implies that the mechanism might be calcium dependent. Real-time Ca²⁺ mapping by laser scanning confocal microscopy of boring BC008 cells and genetic analyses of boring cells, showed that the process of uptake of Ca²⁺ from the boring front, trans-cellular mobilization, and extrusion at the distal end of the filaments is involved in bioerosive activity, and that P-type Ca²⁺ ATPase transporters and calcium channel proteins are involved. This demonstrates that BC008 bores by promoting calcite dissolution locally at the boring front through Ca²⁺ uptake, an unprecedented capacity among living organisms. Parallel studies using mixed microbial assemblages of euendoliths in Nature, boring into Caribbean, Mediterranean, South and North Pacific marine carbonates, demonstrate that the mechanism operating in BC008 is widespread, but perhaps not universal.