Direct Use of Mineral Carbonate for Autotrophy Among Euendolithic Cyanobacteria

Abstract:

Cyanobacteria are oxygenic photoautotrophs, and arguably the most important primary producers on the planet, fixing carbon from dissolved inorganic carbon (DIC) in the aquatic environment, and directly from atmospheric CO₂ in terrestrial systems. Euendolithic cyanobacteria occupy a very specific niche, inside rocks, which can potentially preclude them from easily accessing those carbon pools, and yet, natural euendolithic communities can support food webs in habitats where they are prominent, such as in marine carbonate platforms and desert carbonate outcrops. In a recently proposed model describing the mechanism of cyanobacterial carbonate boring, we postulated that as the organism dissolves the mineral, liberated CO₃^2- anions will be quickly converted to HCO₃^- and assimilated directly, making the cyanobacterium independent of external DIC pools for autotrophy. We used natural abundance and tracer stable carbon (¹³C) isotope analyses accompanied by nanoSIMS imaging in model laboratory systems of cultivated cyanobacteria and in natural mixed communities of marine euendoliths to study the ultimate source of carbon in their biomass. Our results clearly demonstrate that endolithic biomass of these cyanobacteria is significantly derived from mineral carbonate, as opposed to free-living or epilithic biomass, where the source is mixed or coming from the dissolved pool, this holds for model cultures as well as natural communities. In fact, we can increase the lifestyle preference of cultures for endolithic growth versus planktonic or benthic growth, by simply imposing an external DIC limitation in the presence of a carbonate substrate. Our results predict that benthic communities (extant or fossil) that rely heavily on primary production by euendolithic primary producers may show ¹³C signatures that mimic those of the surrounding carbonate substrate rather than from those of the local seawater.