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      Microbial chemolithotrophy mediates oxidative weathering of granitic bedrock

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          Abstract

          The flux of solutes from the chemical weathering of the continental crust supplies a steady supply of essential nutrients necessary for the maintenance of Earth’s biosphere. Promotion of weathering by microorganisms is a well-documented phenomenon and is most often attributed to heterotrophic microbial metabolism for the purposes of nutrient acquisition. Here, we demonstrate the role of chemolithotrophic ferrous iron [Fe(II)]-oxidizing bacteria in biogeochemical weathering of subsurface Fe(II)-silicate minerals at the Luquillo Critical Zone Observatory in Puerto Rico. Under chemolithotrophic growth conditions, mineral-derived Fe(II) in the Rio Blanco Quartz Diorite served as the primary energy source for microbial growth. An enrichment in homologs to gene clusters involved in extracellular electron transfer was associated with dramatically accelerated rates of mineral oxidation and adenosine triphosphate generation relative to sterile diorite suspensions. Transmission electron microscopy and energy-dispersive spectroscopy revealed the accumulation of nanoparticulate Fe–oxyhydroxides on mineral surfaces only under biotic conditions. Microbially oxidized quartz diorite showed greater susceptibility to proton-promoted dissolution, which has important implications for weathering reactions in situ. Collectively, our results suggest that chemolithotrophic Fe(II)-oxidizing bacteria are likely contributors in the transformation of rock to regolith.

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          Most cited references58

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          Ferrozine---a new spectrophotometric reagent for iron

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            Siderophores: structure and function of microbial iron transport compounds.

            Siderophores are common products of aerobic and facultative anaerobic bacteria and of fungi. Elucidation of the molecular genetics of siderophore synthesis, and the regulation of this process by iron, has been facilitated by the fact that E. coli uses its own siderophores as well as those derived from other species, including fungi. Overproduction of the siderophore and its transport system at low iron is in this species well established to be the result of negative transcriptional repression, but the detailed mechanism may be positive in other organisms. Siderophores are transported across the double membrane envelope of E. coli via a gating mechanism linking the inner and outer membranes.
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              Mineral weathering by bacteria: ecology, actors and mechanisms.

              Soil microbes play an essential role in the environment by contributing to the release of key nutrients from primary minerals that are required not only for their own nutrition but also for that of plants. Although the role of fungi in mineral weathering is beginning to be elucidated, the relative impact of bacteria in this process and the molecular mechanisms involved remain poorly understood. Here, we discuss the ecological relevance of bacterial weathering, mainly in the soil and especially in acidic forest ecosystems, which strongly depend on mineral weathering for their sustainability. We also present highlights from recent studies showing molecular mechanisms and genetic determinants involved in the dissolution of complex minerals under aerobic conditions. Finally, we consider the potential applications of genomic resources to the study of bacterial weathering.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                December 26 2019
                December 26 2019
                December 26 2019
                December 16 2019
                : 116
                : 52
                : 26394-26401
                Article
                10.1073/pnas.1909970117
                6936594
                31843926
                fcfb8c31-0bb9-40f4-b99a-103f5a3f3d78
                © 2019

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