Siderite-based anaerobic iron cycle driven by autotrophic thermophilic microbial consortium

Daria G Zavarzina,Michail S Chernov,Angelina V Antonova,Alexander Yu Merkel,Yury A Koksharov,Nataliya I Chistyakova,Anna A Perevalova,Maria A Gracheva,Tatiana V Kochetkova,Elizaveta A Bonch-Osmolovskaya,Sergey N Gavrilov,Andrey Yu Bychkov

doi:10.1038/s41598-020-78605-7

Abstract

Using a sample from a terrestrial hot spring (pH 6.8, 60 °C), we enriched a thermophilic microbial consortium performing anaerobic autotrophic oxidation of hydrothermal siderite (FeCO3), with CO2/bicarbonate as the electron acceptor and the only carbon source, producing green rust and acetate. In order to reproduce Proterozoic environmental conditions during the deposition of banded iron formation (BIF), we incubated the microbial consortium in a bioreactor that contained an unmixed anoxic layer of siderite, perfectly mixed N2/CO2-saturated liquid medium and microoxic (2% O2) headspace. Long-term incubation (56 days) led to the formation of magnetite (Fe3O4) instead of green rust as the main product of Fe(II) oxidation, the precipitation of newly formed metabolically induced siderite in the anoxic zone, and the deposition of hematite (Fe2O3) on bioreactor walls over the oxycline boundary. Acetate was the only metabolic product of CO2/bicarbonate reduction. Thus, we have demonstrated the ability of autotrophic thermophilic microbial consortium to perform a short cycle of iron minerals transformation: siderite–magnetite–siderite, accompanied by magnetite and hematite accumulation. This cycle is believed to have driven the evolution of the early biosphere, leading to primary biomass production and deposition of the main iron mineral association of BIF.

Highlights

Using a sample from a terrestrial hot spring, we enriched a thermophilic microbial consortium performing anaerobic autotrophic oxidation of hydrothermal siderite (FeCO3), with CO2/ bicarbonate as the electron acceptor and the only carbon source, producing green rust and acetate
A stable siderite-oxidising anaerobic thermophilic microbial consortium was obtained by ten-fold dilutions and multiple consequent transfers on bicarbonate medium with hydrothermal siderite as the electron donor and 20% of CO2 in the gas phase as the electron acceptor
Our experiments clearly show the capability of an autotrophic thermophilic microbial consortium to perform anaerobic oxidation of hydrothermal siderite

Summary

Introduction

Using a sample from a terrestrial hot spring (pH 6.8, 60 °C), we enriched a thermophilic microbial consortium performing anaerobic autotrophic oxidation of hydrothermal siderite (FeCO3), with CO2/ bicarbonate as the electron acceptor and the only carbon source, producing green rust and acetate. We have demonstrated the ability of autotrophic thermophilic microbial consortium to perform a short cycle of iron minerals transformation: siderite–magnetite–siderite, accompanied by magnetite and hematite accumulation. This cycle is believed to have driven the evolution of the early biosphere, leading to primary biomass production and deposition of the main iron mineral association of BIF. The additional formation of acetate was observed instead of its expected oxidation, while Mӧssbauer spectral analysis revealed that magnetite was formed due to Fe(II)-oxidation rather than Fe(III)-reduction Based on these observations, we hypothesize that this microorganism would be able to perform carbonate-dependent Fe(II)-oxidation. Carbonate-dependent iron oxidation by thermophilic microorganisms may have play a significant role in the early development of Earth biosphere

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