Elsevier

Applied Geochemistry

Volume 31, April 2013, Pages 216-227
Applied Geochemistry

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

https://doi.org/10.1016/j.apgeochem.2013.01.007Get rights and content

Abstract

Chemical weathering of Mg, Ca-silicates and alumino-silicates contributes significantly to the drawdown of atmospheric CO2 over long time scales. The present work focuses on how this mode of weathering may change in the presence of free-living bacteria in oligotrophic waters, which compose most of the surface freshwaters of the Earth. Forsterite (Fo90) was reacted for 1 week with a stable Escherichia coli population in water maintained at 37 °C and neutral pH in a batch reactor. Control samples with suspensions of pure olivine powders and E. coli cells in pure water were also used for reference. Olivine controls reproduce the Mg, Si and Fe release in solutions predicted from rates published in the literature with pH shifts of less than 0.5 unit. After 1 week, under abiotic conditions, weathered surfaces are enriched in Fe and Fe3+ relative to the initial composition of the mineral. Bacterial controls (without minerals) show decreasing Eh with increasing cell concentrations (−50 mV with 7 × 107 cells/mL and −160 mV with 8 × 108 cells/mL). Magnesium concentrations in bacterial control solutions are in the μg/L range and can be accounted for by the release of Mg from dead cells. More than 80% of the cells were still alive after 1 week. The solutions obtained in the experiments in which olivine reacts in the presence of cells show Mg and Si concentrations a few tens of percent lower than in the mineral control samples, with a prominent depletion of Fe(III) content of the mineral surfaces. Magnesium mass balance discounts both significant bacterial uptake and inhibition of the Mg dissolution rates as a consequence of changing pH and Eh. Coating by bacterial cell layers is also negligible. E. coli reduces the chemical weathering of olivine. This study infers that the presence of free-living Proteobacteria, a prevalent group of subsurface bacteria, should decrease the amount of riverine Mg released by chemical weathering of mafic rocks.

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:CO2+H2A(electron source)CH2O+2Ait 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.

References (100)

  • R.W. Luce et al.

    Dissolution kinetics of magnesium silicates

    Geochim. Cosmochim. Acta

    (1972)
  • J.E. Lusk et al.

    Magnesium and the growth of Escherichia coli

    J. Biol. Chem.

    (1968)
  • W.G. Miller et al.

    An improved GFP cloning cassette designed for prokaryotic transcriptional fusions

    Genes

    (1997)
  • P.M. Morris et al.

    Phthalic acid complexation and the dissolution of forsteritic glass studies via in situ FTIR and X-ray scattering

    Geochim. Cosmochim. Acta

    (2008)
  • A. Navarre-Sitchler et al.

    Basalt weathering across scales

    Earth Planet. Sci. Lett.

    (2007)
  • H.C. Neu et al.

    The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts

    J. Biol. Chem.

    (1965)
  • W. Norde et al.

    Protein adsorption and bacterial adhesion to solid surfaces: a colloid chemical approach

    Colloids Surf.

    (1989)
  • A.A. Olsen et al.

    Oxalate-promoted forsterite dissolution at low pH

    Geochim. Cosmochim. Acta

    (2008)
  • F.W. Outten et al.

    The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli

    J. Biol. Chem.

    (2001)
  • P.A.E. Pogge von Strandmann et al.

    The influence of weathering processes on riverine magnesium isotopes in a basaltic terrain

    Earth Planet. Sci. Lett.

    (2008)
  • O.S. Pokrovsky et al.

    Kinetics and mechanism of forsterite dissolution at 25 °C and pH from 1 to 12

    Geochim. Cosmochim. Acta

    (2000)
  • J.J. Rosso et al.

    A high resolution study of forsterite dissolution rates

    Geochim. Cosmochim. Acta

    (2000)
  • C.M. Santelli et al.

    The effect of Fe-oxidizing bacteria on Fe-silicate mineral dissolution

    Chem. Geol.

    (2001)
  • J. Schott et al.

    X-ray photoelectron studies of the mechanism of iron silicate dissolution during weathering

    Geochim. Cosmochim. Acta

    (1983)
  • J.H. Scofield

    Hartree–Slater subshell photoionization cross-sections at 1254 and 1487 eV

    J. Electron Spectrosc. Rel. Phen.

    (1976)
  • H. Seyama et al.

    Surface characterization of acid-leached olivines by X-ray photoelectron spectroscopy

    Chem. Geol.

    (1996)
  • L.S. Shirokova et al.

    Effect of the heterotrophic bacterium Pseudomonas reactans on olivine dissolution kinetics and implications for CO2 storage in basalts

    Geochim. Cosmochim. Acta

    (2012)
  • S. Silver et al.

    Magnesium transport in Escherichia coli. Interference by manganese with magnesium metabolism

    J. Biol. Chem.

    (1971)
  • S. Silver et al.

    Reversible alterations in membrane permeability of Escherichia coli induced by a steroidal diamine, irehdiamine A

    Biochem. Biophys. Res. Commun.

    (1968)
  • J.D. Stopar et al.

    Kinetic model of olivine dissolution and extent of aqueous alteration on Mars

    Geochim. Cosmochim. Acta

    (2006)
  • I.H. Thorseth et al.

    Textural and chemical effects of bacterial-activity on basaltic glass – an experimental approach

    Chem. Geol.

    (1995)
  • W.J. Ullman et al.

    Laboratory evidence for microbially mediated silicate mineral dissolution in nature

    Chem. Geol.

    (1996)
  • J. Van Herk et al.

    Neutralization of industrial waste acids with olivine – the dissolution of forsteritic olivine at 40–70 °C

    Chem. Geol.

    (1989)
  • S.A. Welch et al.

    Modification of olivine surface morphology and reactivity during natural and experimental chemical weathering

    Geochim. Cosmochim. Acta

    (2002)
  • S.A. Welch et al.

    The effect of microbial glucose metabolism on bytownite feldspar dissolution rates between 5° and 35 °C

    Geochim. Cosmochim. Acta

    (1999)
  • A.F. White et al.

    The effect of time on the weathering of silicate minerals: why do weathering rates differ in the laboratory and field?

    Chem. Geol.

    (2003)
  • R.A. Wogelius et al.

    Olivine dissolution at 25 °C: Effects of pH, CO2, and organic acids

    Geochim. Cosmochim. Acta

    (1991)
  • R.A. Wogelius et al.

    Olivine dissolution kinetics at near-surface conditions

    Chem. Geol.

    (1992)
  • L. Wu et al.

    Characterization of elemental release during microbe-basalt interactions at T = 28 °C

    Geochim. Cosmochim. Acta

    (2007)
  • N.A. Amro et al.

    High resolution atomic force microscopy studies of the Escherichia coli outer membrane: structural basis for permeability

    Langmuir

    (2000)
  • Banfield, J.F., Hamers, R.J., 1997. Processes at minerals and surfaces with relevance to microorganisms and prebiotic...
  • J.F. Banfield et al.

    Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere

    Proc. Natl. Acad. Sci.

    (1999)
  • Barker, W.W., Welch, S.A., Banfield, J.F., 1997. Biogeochemical weathering of silicate minerals. In: Banfield, J.F.,...
  • B.K. Basu et al.

    Factors related to heterotrophic bacterial and flagellate abundance in temperate rivers

    Aquat. Microb. Ecol.

    (1997)
  • J. Berthelin

    Microbial weathering processes in natural environments

  • T.J. Beveridge

    Structures of gram-negative cell walls and their derived membrane vesicles

    J. Bacteriol.

    (1999)
  • T.J. Beveridge et al.

    Binding of metals to cell envelopes of Escherichia coli – K12

    Appl. Environ. Microbiol.

    (1981)
  • T.L. Boone et al.

    Morphological and cultural comparison of microorganisms in surface soil and subsurface sediment at a pristine study site in Oklahoma

    Microb. Ecol.

    (1988)
  • H.J.M. Bowen

    Trace Elements in Biochemistry

    (1966)
  • G. Bratbak et al.

    Bacterial dry matter content and biomass estimation

    Appl. Environ. Microbiol.

    (1984)
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