Inside the alkalinity engine: the role of electron donors in the organomineralization potential of sulfate‐reducing bacteria

Abstract

Mineral precipitation in microbial mats may have been the key to their preservation as fossil stromatolites, potentially documenting evidence of the earliest life on Earth. Two factors that contribute to carbonate mineral precipitation are the saturation index (SI) and the presence of nucleation sites. Both of these can be influenced by micro-organisms, which can either alter SI through their metabolisms, or produce and consume organic substances such as extracellular polymeric substances (EPS) that can affect nucleation. It is the balance of individual metabolisms within the mat community that determines the pH and the dissolved inorganic carbon concentration, thereby potentially increasing the alkalinity and consequently the SI. Sulfate-reducing bacteria (SRB) are an important component of this 'alkalinity engine.' The activity of SRB often peaks in layers where CaCO(3) precipitates, and mineral precipitation has been demonstrated in SRB cultures; however, the effect of their metabolism on the alkalinity engine and actual contribution to mineral precipitation is the subject of controversy. Here, we show through culture experiments, theoretical calculations, and geochemical modeling studies that the pH, alkalinity, and organomineralization potential will vary depending on the type of electron donor. Specifically, hydrogen and formate can increase the pH, but electron donors like lactate and ethanol, and to a lesser extent glycolate, decrease the pH. The implication of this for the lithification of mats is that the combination of processes supplying electron donors and the utilization of these compounds by SRB may be critical to promoting mineral precipitation.

Effects of Elevated Carbon Dioxide and Salinity on the Microbial Diversity in Lithifying Microbial Mats

“…As outlined above, this pattern can easily be attributed to changes in fermentation patterns yielding different organic substrates (e.g., organic acids) available to the sulfate-reducing population. This change could have a major impact on the CaCO 3 precipitation by the microbial community [61,62]. These results suggest that although the microbial diversity did not profoundly change during the experiment, the metabolic activity of the mat community may have been impacted in response to elevated pCO 2 .…”

“…A variety of different fermentation products have been found in cyanobacteria [63] and a shift in community metabolism, especially in fermentation pathways of the cyanobacteria, could have accounted for the drop in pH followed by an increase observed in the current study. Additionally, a shift of community metabolism to favor H 2 , formate, acetate and glycolate production could result in an increase in diversity and abundance of sulfate-reducing bacteria, accompanied by a slight increase in pH resulting from the metabolism of the anaerobic heterotrophs [62]. An argument based on modeling efforts was made that shifts in fermentation patterns would not affect the lithification potential [64,65] and further investigations are needed.…”

“…The persistence of a carbonate crust under elevated CO 2 conditions and the enrichment of Desulfobacterales under elevated CO 2 may reflect the increased availability of organic carbon under elevated CO 2 for sulfate reduction. Recent studies [61,62] demonstrated that the type of organic carbon metabolized by sulfate-reducing bacteria impacts the pH; modeling and culture experiments revealed that oxidation of some electron donors (i.e., formate, H 2 ) increased the pH, while others (i.e., lactate, ethanol) decreased the pH. A variety of different fermentation products have been found in cyanobacteria [63] and a shift in community metabolism, especially in fermentation pathways of the cyanobacteria, could have accounted for the drop in pH followed by an increase observed in the current study.…”

“…Therefore, an increase in sulfate-reducing bacteria diversity and/or abundance may increase the microbial mat lithification potential. Clearly, microbial mats and microbialites are complex ecosystems in which the entire community determines the CaCO 3 precipitation potential [11,15,16,62].…”

The oyster enigma variations: a hypothesis of microbial calcification

“…Sulfate-reducing bacteria, comprising a diverse assemblage representing many clades and various biochemical pathways, abet dolomitization under anoxic hypersaline conditions (Vasconcelos and McKenzie 1997). Depending on which organic substrate they use, sulfate-reducers may create alkaline conditions (high concentrations of dissolved inorganic carbon) favorable for the precipitation of calcium carbonate (Gallagher et al 2012) in a process analogous to diagenetic sulfate reduction in sediments where organic carbonates are precipitated (Schrag et al 2013;Canfield and Kump 2013). Although Meister (2013) has suggested that the (acidic) hydrogen ions released by sulfate reduction counteract the rise in alkalinity, thus potentially preventing precipitation of carbonate minerals, experiments on and models of microbial mineral formation indicate that sulfate-reducers, perhaps together with bacteria using other biochemical pathways, can precipitate carbonate minerals including calcium carbonate (Visscher et al 2000;Visscher and Stolz 2005;Bergmann et al 2013).…”