Microbial mediation of stromatolite formation in karst-water creeks

Epilithic and endolithic biofilms were found to control the formation of stromatolites in karst-water creeks. We used microsensors to determine the influence of biological processes on chemical conditions within the microenvironment of crystal nucleation sites: the stromatolite surface. Phototrophic members of the biofilms consisted of mainly cyanobacteria and diatoms. Oxygen, pH, calcium, and carbonate concentration microprofiles at the stromatolite surface and boundary layer showed a strong diurnal rhythm of calcium carbonate precipitation. During illumination, photosynthesis caused oxygen production, a marked increase in pH and CO 2{ 3 concentrations, and a decrease in Ca 2+ concentration at the stromatolite surface due to calcium carbonate precipitation. The opposite occurred in the dark, indicating decalcification. Calcite was approximately 16 times oversaturated in the bulk water, photosynthesis induced an increase of the supersaturation to .27 at the stromatolite surface under illumination, and respiration induced a decrease of the supersaturation to ,10 in the dark. Photosynthetically stimulated calcium carbonate precipitation was confirmed by radioactive isotope (45Ca2+) uptake studies. Over a 24 h light : dark cycle, biofilms showed net calcification. Biotic activity within the stromatolite has a large effect on conditions at its surface and, therefore, contributes considerably to the stromatolite precipitation process. Calcareous stromatolites are amongst the oldest known biological formations, and they provide insight into early Earth environments and climates. For this reason, it is essential to understand the processes governing their formation and dissolution. Presently forming stromatolites are rare in marine settings, but they are a common and much investigated feature of karst regions (Grüninger 1965; Merz-Preiss and Riding 1999). Such karst-water creek stromatolites have been termed tufa stromatolites, and they are defined as macroscopically laminated benthic microbial deposits produced by precipitation of minerals on organic tissue (Riding 1990). The role of biofilms in the formation of these stromatolites is still under debate. Early studies suggested that precipitation was primarily caused by CO2 assimilation by cyanobacteria, eukaryotic algae, and plants (Pia 1926, 1933; Wallner 1934). Later hydrochemical investigations, however, concluded that precipitation is largely physicochemically driven by rapid CO2 degassing from high-pCO2 groundwater (Usdowski et al. 1979; Herman and Lorah 1987; Merz-Preiss and Riding 1999), with only a minor contribution from photosynthetic CO2 removal. This conclusion was reached when it was observed that calcium and dissolved inorganic carbon (DIC) were lost from water as it moved downstream, but no diurnal pattern was observed in creek-water chemistry. Even in instances where phototrophic communities were observed to affect whole-stream inorganic carbon dynamics (Spiro and Pentecost 1991), the development of tufa travertine deposits was seen as a largely abiotic process. The biofilms in the creeks investigated in the current study were very thin (,100 mm), and indeed whole-stream-water chemistry parameters were hardly affected by biological activity. We tested the hypothesis that in these thin biofilms, strong shifts in local water chemistry are possible due to photosynthetic and respiratory activity, and that these shifts have highly localized effects on the stromatolite surface, where calcium carbonate precipitates. Precipitation of calcite is initiated when calcium carbonate becomes supersaturated and suitable nucleation sites are present. Karst waters have a low Mg2+ : Ca2+ ratio (,2), and, therefore, low-Mg-calcite is usually the main component in their stromatolite formations (Irion and Müller 1968; Arp et al. 2001). Photosynthesis and respiration can have a large effect on carbonate chemistry. Photosynthesis removes CO2 and shifts the carbonate equilibrium toward carbonate, thereby increasing calcite saturation state (V). Respiration increases CO2 and therefore has the opposite effect. Consequently, photosynthesis can lead to calcification, while respiration can lead to calcite dissolution when V decreases to values below one. In other aquatic settings, such as hypersaline lakes (Ludwig et al. 2005) and marine sediments (Werner et al. 2008) microsensor studies have demonstrated the potential for phototrophic communities to remove large amounts of CO2 and enhance calcification. For stromatolite-forming biofilms in freshwater settings, this has not yet been investigated, and the view still prevails 1 Corresponding author ([email protected]; phone: +49 421-2028830; fax: +49 421-2028690). Acknowledgments We thank the microsensor technicians at the Max Planck Institute for Marine Microbiology, Bremen, for assistance with microsensor construction, and Lubos Polerecky for the microprofiling software. We thank Hakhyun Nam (Kwangwoon University, Korea) for supplying the carbonate ionophore. This project is part of the Research Unit ‘‘Geobiology of Organoand Biofilms’’ funded by the German Research Foundation (DFGFOR 571, publication 23). Limnol. Oceanogr., 53(3), 2008, 1159–1168 E 2008, by the American Society of Limnology and Oceanography, Inc.