ABSTRACT

With a proof-of-concept award, this project will examine the diversity of microorganisms that breathe iron in place of oxygen. Since oxygen was absent on early Earth and iron-breathing bacteria are found near the root of the tree of life, they are likely to represent one of the first life forms that evolved on our planet. In the modern world, iron-breathing bacteria are important to many environmental and energy-generating processes, including release of iron nutrients to organisms residing in ocean and lake waters, degradation of hazardous pollutants in drinking water supplies, and electricity generation by bacteria. The biodiversity of iron-breathing bacteria in the environment, however, is poorly understood. Work by researchers at Georgia Tech will greatly expand our knowledge of these bacteria, and will test a novel hypothesis about how they breath iron. Since the iron rust particles are located outside the cell, generating energy by breathing iron rust particles requires novel strategies that this project will unravel. The hypothesis is that bacteria breathe iron rust particles and generate energy by producing sulfur molecules that are transferred outside the cell to interact with the external iron rust particles. Interaction between the sulfur compounds and the iron rust particles outside the cell results in energy production inside the cell. Experiments will involve examining the biodiversity of iron breathing bacteria in the salt marsh sediments of Skidaway Island (GA), which represents a coastal marine ecosystem replete with sulfur and iron. The research will also include training opportunities for women students from underrepresented groups in science at Alverno College in Milwaukee, WI.

The proposed research will integrate state-of-the-art taxonomic (phylogenetic), genetic (metagenomic, metatranscriptomic), and functional (electrochemical, geochemical) approaches to determine the biodiversity of a previously overlooked microbial community linking the biogeochemical cycles of iron (Fe) and sulfur (S) in anaerobic marine and freshwater sediments. Initial geochemical and genetic findings indicate that bacterially-produced organic S (thiol) compounds can function as electron shuttles to deliver electrons to extracellular Fe(III) oxides, but the environmental significance of this activity is unproven. Since thiols are potent chemical reductants of Fe(III) oxides, yet are not detected in significant concentrations in sedimentary environments, these findings suggest that a cryptic organic S cycle fuels widespread microbial Fe(III) reduction activity in both freshwater and marine sediments. Field collections will be conducted at the salt marsh sediments of Skidaway Island (GA), which represents a coastal marine ecosystem replete with organic S and Fe. The overall experimental approach is divided into three main components: 1) identification of sediment layers displaying overlapping zones of Fe and organic S redox signals; 2) correlation of changes in gene expression profiles and the metabolic activity of organic S-driven Fe(III)-reducing bacteria and in perturbed sediment incubations; and 3) taxonomic (phylogenetic) and genetic (metagenomic, metatranscriptomic) analyses to determine the microbial community composition and functional gene expression patterns of pure (or highly enriched) cultures of organic S-driven Fe(III)-reducing bacteria. The project has the potential to transform a broad range of scientific disciplines by establishing a new link between organic S chemistry and microbial Fe metabolism through exploration of novel bacterial diversity. Microbial Fe(III) reduction is central to a wide variety of global processes, including the biogeochemical cycling of Fe (via reductive mobilization of insoluble Fe(III) oxides) and carbon (via anaerobic oxidation of organic matter). A large fraction of the flux of organic carbon remineralization in redox-stratified soils, peats, and freshwater and marine sediments has been attributed to microbial Fe(III) reduction, while microbially-catalyzed reductive dissolution of insoluble Fe(III) oxides may act a source of dissolved Fe to drive primary productivity in marine environments. A novel connection between the biogeochemical cycles of Fe, S, and C (potentially in a single bacterial cell) will revolutionize the current dogma concerning pathways for microbial Fe(III) reduction in the environment and will provide a new model for interpreting the global biogeochemical importance of microbial Fe(III) reduction. Microbial Fe(III) reduction is also central to a wide variety of other significant environmental and energy related processes, including reductive precipitation of toxic metals and radionuclides and generation of electricity in microbial fuel cells. If successful, this research will refine carbon cycling models (in which Fe(III) reduction is traditionally assumed to be a direct enzymatic process) and identify new diverse microorganisms for use in alternate strategies for remediation of radionuclide-contaminated aquifers and increasing power output in microbial fuel cells. Fe(III)-reducing microorganisms are also deeply rooted and scattered throughout the domains Bacteria and Archaea, an indication that microbial Fe(III) reduction may represent an ancient metabolic process. The phylogenetic link between microbial sulfur metabolism and Fe(III) reduction may therefore also have a significant impact on interpreting the evolutionary history and biodiversity of microbial respiratory systems. The research will broaden participation in science via educational opportunities for undergraduate students who are members of underrepresented groups in science.

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