An experimental model approach of biologically-assisted silicate dissolution with olivine and Escherichia coli – Impact on chemical weathering of mafic rocks and atmospheric CO2 drawdown
Highlights
► The mass balance of magnesium has been established. ► The presence of bacteria inhibits Mg release during weathering of olivine. ► The free-living Proteobacteria should decrease the amount of riverine Mg. ► Proteobacteria could play an inhibitor role in the drawdown of atmospheric CO2.
Introduction
The impact of microbial–mineralogical feedback mechanisms on the long-term response of the Earth system is unclear. Global-scale models verify that chemical weathering of Mg and Ca-bearing silicates and alumino-silicates present in the continent directly impact climate. Their weathering products releasing alkalinity into the ocean, which in turn is primarily removed from seawater by precipitation of marine carbonates (Garrels and MacKenzie, 1971, Broecker and Peng, 1982) leading to draw down of CO2. The rates of chemical weathering of Ca-silicates, Mg-silicates, and Ca–Mg-silicates determine the rate of supply of Ca and Mg to oceans and thus affect the magnitude of this critical feedback mechanism. If microorganisms significantly affect mineral dissolution rates (e.g. Kalinowski et al., 2000a, Kalinowski et al., 2000b, Liermann et al., 2000, Santelli et al., 2001), then the evolution of the biosphere (dominated by microorganisms for the majority of time), atmosphere, hydrosphere, and lithosphere must have been closely coupled (Banfield et al., 1999). It is, for example, widely accepted that early in Earth’s history (between 1 and 3 Ga, Kasting, 1992, Kasting, 1993, Kasting et al., 1992), the atmosphere was dominated by CO2 and that O2 concentrations only increased with the evolution of efficient oxygenic photosynthetic microbial populations. Indeed, from the following equation:it can be shown that one C atom (from one molecule of atmospheric CO2) becomes a C in organic matter (CH2O) and, during sedimentation processes, this C in organic matter could become hydrocarbon implying that one C atom from one molecule of CO2 is utilized in hydrocarbon production. With photosynthesis (CO2 + H2O → CH2O + O2), for each C atom stored in sediments, one molecule of O2 is liberated to the atmosphere.
Moreover, early inorganic rock weathering resulted in the accumulation of Ca and Mg in ocean waters, leading to precipitation of Ca-, Mg-carbonates and draw down of CO2. At present, silicate weathering is known to account for a global CO2 drawdown rate of ≈108 tons/a (Gaillardet et al., 1999, Hilley and Porder, 2008). Basalts are responsible for one third of this consumption, even though they represent less than 5% of the continental area covered by silicates (Dessert et al., 2003, Navarre-Sitchler and Brantley, 2007). Chemical release of Mg and Ca into rivers is dominated by carbonate dissolution (Meybeck, 1987, Stallard and Edmond, 1983, Louvat et al., 2008) but dissolution of mafic silicates by runoff and subsurface waters still represents a major sink for CO2 (Regnier et al., 2005). Currently, quantitative impact of microbes on this draw down is not predictable. Chemical weathering results from intricate relationships between biological and geochemical processes in soils, sediments and aquifers. Biomass modifies the chemistry of soil solutions (Lucas, 2001) and affects the composition of river waters (Benedetti et al., 2003, Pogge von Strandmann et al., 2008). Vegetal cover and associated mycorrhiza affect the pH and organic ligand abundances in soil solutions and consequently change the dissolution rates of silicates (White and Brantley, 1995). Biomass fluctuations modify the storage and release into soil solutions of Mg and Ca, which are major elements in cells. Bacteria and solutions are washed out from soils during floods and over the rainy season causing microbial concentration (Palijan and Fuks, 2006) peaks in rivers.
The elemental composition of bacteria has not been determined extensively (Jones et al., 1979). Although increasing interest has developed in the role of mineral elements in the physiology of microbial cells (e.g. Epstein and Schultz, 1965) and their transformations in nature (e.g., Jernelov and Martin, 1975), data on the bioaccumulation of mineral cations by bacteria have remained sparse (e.g. Bowen, 1966). Washing procedures have been variable, if performed at all. The conditions of growth such as pH, elemental composition of the medium, growth rate, and the source of the electron donor in photosynthetic organisms influence the elemental composition of bacteria. Magnesium is the most abundant divalent cation in living cells and mediates in numerous cellular activities. The uptake of this ion in most prokaryotes is through the action of the CorA family, which is also one of the most studied families of divalent cation transporters (Guskov et al., 2012). Jasper and Silver (1977) reported that total cellular Mg was generally in the range of 360–840 mg/L (wet cells).
The present work focuses on the influence of free-living heterotrophic, Proteobacteria, that are often predominant in rivers, on the dissolved Mg load into runoff during chemical weathering of a common and fairly soluble mafic mineral, olivine under oligotrophic conditions. Experiments on silicate dissolution performed in the presence of microbial cells in low-nutrient culture media suggest a limited geochemical impact of free-living bacteria on chemical weathering of mafic rocks in subsurface oligotrophic waters. Oligotrophic refers to bodies of water with very low nutrient levels, nutrients being here considered as any chemical substance providing energy or supporting metabolism that must be extracted from the environment by the organism to live. Under oligotrophic conditions, basaltic glass has been suggested to remain unaltered in the presence of bacteria isolated from marine basalts (Einen et al., 2006), whereas dissolution was enhanced in media amended with glucose (Thorseth et al., 1995). Similarly, under oligotrophic conditions, no apparent effect was observed of a population presence of a model soil strain belonging to Proteobacteria (Welch and Ullman, 1999) on Ca-rich feldspar dissolution rate was reported and glucose addition increased the dissolution rate due to metabolic processes. Such observations illustrate a limitation of the general inference that the presence of microorganisms enhances the rate of silicate weathering (White and Brantley, 2003). This is widely interpreted as a result of bacterial populations decreasing the pH and increasing the concentrations of organic ligands (Barker et al., 1997, Banfield et al., 1999, Liermann et al., 2000, Wu et al., 2007) when they are grown in nutrient-rich media. Experiments in the presence of Proteobacteria treated with azide, a metabolic inhibitor, show that the dissolution rate of fayalite is indistinguishable from that measured under abiotic acidic (pH < 4) conditions (Santelli et al., 2001). Extrapolating the lack of impact of a stable population of bacteria on the weathering of fayalite to the nearly neutral pH of natural subsurface waters needs some re-evaluation. Both the physics and chemistry of the cell wall (Norde and Lyklema, 1989) and the dissolution kinetics (Wogelius and Walther, 1991) are indeed strongly pH dependent.
The present study sets out to investigate the influence of a stable free-living bacteria population of Escherichia coli, a well-understood strain of Proteobacteria, on the fraction of dissolved Mg originating from chemical weathering of olivine, an ubiquitous and fairly soluble mineral of mafic rocks, in near-neutral and oligotrophic waters. Mass-balance of Mg will be presented both for olivine/E. coli suspensions and for abiotic and bacterial reference samples.
Section snippets
Methodology
The present study aims to investigate the influence of a fixed sized-population of bacteria (E. coli) on the amount of Mg released by chemical weathering of olivine powder in pure water. In order to facilitate the assessment of elemental mass balance, the runs were conducted in open air and in batch reactors. Olivine is an important Mg-silicate as it is a major mineral of various mafic rocks (Delvigne et al., 1979, Smith et al., 1987, Banfield and Hamers, 1997, Welch and Banfield, 2002, Fisk et
Mg, Si and Fe concentrations of the solutions
The Mg, Si and Fe concentrations of the different solutions are reported in Table 1. The Mg concentrations in the mg/L range in the stirred solutions are similar to those reported by Wogelius and Walther (1991) for batch experiments at pH = 6, in reactors of similar volume and specific surface of the powder. Once corrected for temperature differences, the initial dissolution rates are consistent with these literature values (Fig. 1). After 48 h, the Mg and Si release rates are constant (Fig. 2).
Mass balance in abiotic control solutions
The purpose of this section is to assess the distribution of Mg, Si and Fe between coexisting solution, olivine and other potential solid phases. The first parameter to evaluate is the proportion of olivine dissolved in the different experiments. Loss of Mg and Si does not affect the average grain size of the powders, but markedly alters and dismantles the surface layers. The Mg and Si contents of the stirred solutions correspond to less than 1019 (a = 0.09 ± 0.01 m2/g) and 1020 (a = 1.46 ± 0.04 m2/g)
Conclusions
Assessing the mass balance of Mg in experimental open-air suspensions of olivine powders with a stable population of E. coli in water at neutral pH demonstrates that the presence of bacteria inhibits Mg release during weathering of olivine. Although Mg and oligotroph data in watersheds with abundant mafic and ultramafic bedrocks are critically missing, this study suggests that free-living Proteobacteria, a prevalent group of subsurface bacteria, should decrease the amount of riverine Mg
Acknowledgements
B.G. is grateful to C. Douchet for precious technical assistance, to E. Albalat for the analyses of the E. coli Mg content, and to Ph. Telouk for ICP-AES and ICP-MS instrumental assistance. LL gratefully acknowledges Dr. Fabien Mongelard, for his constructive comments. He helped to significantly improve the presentation of this work. This work was supported by the CNRS, CNES and an ANR Jeune Chercheur Fellowship.
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