Nitrate-Dependent Iron Oxidation: A Potential Mars Metabolism

This work considers the hypothetical viability of microbial nitrate-dependent Fe2+ oxidation (NDFO) for supporting simple life in the context of the early Mars environment. This draws on knowledge built up over several decades of remote and in situ observation, as well as recent discoveries that have shaped current understanding of early Mars. Our current understanding is that certain early martian environments fulfill several of the key requirements for microbes with NDFO metabolism. First, abundant Fe2+ has been identified on Mars and provides evidence of an accessible electron donor; evidence of anoxia suggests that abiotic Fe2+ oxidation by molecular oxygen would not have interfered and competed with microbial iron metabolism in these environments. Second, nitrate, which can be used by some iron oxidizing microorganisms as an electron acceptor, has also been confirmed in modern aeolian and ancient sediment deposits on Mars. In addition to redox substrates, reservoirs of both organic and inorganic carbon are available for biosynthesis, and geochemical evidence suggests that lacustrine systems during the hydrologically active Noachian period (4.1–3.7 Ga) match the circumneutral pH requirements of nitrate-dependent iron-oxidizing microorganisms. As well as potentially acting as a primary producer in early martian lakes and fluvial systems, the light-independent nature of NDFO suggests that such microbes could have persisted in sub-surface aquifers long after the desiccation of the surface, provided that adequate carbon and nitrates sources were prevalent. Traces of NDFO microorganisms may be preserved in the rock record by biomineralization and cellular encrustation in zones of high Fe2+ concentrations. These processes could produce morphological biosignatures, preserve distinctive Fe-isotope variation patterns, and enhance preservation of biological organic compounds. Such biosignatures could be detectable by future missions to Mars with appropriate instrumentation

Phosphorus–iron interaction in sediments : can an electrode minimize phosphorus release from sediments?

All restoration strategies to mitigate eutrophication depend on the success of phosphorus (P) removal from the water body. Therefore, the inputs from the watershed and from the enriched sediments, that were the sink of most P that has been discharged in the water body, should be controlled. In sediments, iron (hydr)oxides minerals are potent repositories of P and the release of P into the water column may occur upon dissolution of the iron (hydr)oxides mediated by iron reducing bacteria. Several species of these bacteria are also known as electroactive microorganisms and have been recently identified in lake sediments. This capacity of bacteria to transfer electrons to electrodes, producing electricity from the oxidation of organic matter, might play a role on P release in sediments. In the present work it is discussed the relationship between phosphorus and iron cycling as well as the application of an electrode to work as external electron acceptor in sediments, in order to prevent metal bound P dissolution under anoxic conditions.The authors are grateful to two anonymous reviewers of a previous version of the manuscript for the constructive comments and suggestions. The authors also acknowledge the Grant SFRH/BPD/80528/2011 from the Foundation for Science and Technology, Portugal, awarded to Gilberto Martins

Photoferrotrophy: Remains of an ancient photosynthesis in modern environments

© 2017 Camacho, Walter, Picazo and Zopfi. Photoferrotrophy, the process by which inorganic carbon is fixed into organic matter using light as an energy source and reduced iron [Fe(II)] as an electron donor, has been proposed as one of the oldest photoautotrophic metabolisms on Earth. Under the iron-rich (ferruginous) but sulfide poor conditions dominating the Archean ocean, this type of metabolism could have accounted for most of the primary production in the photic zone. Here we review the current knowledge of biogeochemical, microbial and phylogenetic aspects of photoferrotrophy, and evaluate the ecological significance of this process in ancient and modern environments. From the ferruginous conditions that prevailed during most of the Archean, the ancient ocean evolved toward euxinic (anoxic and sulfide rich) conditions and, finally, much after the advent of oxygenic photosynthesis, to a predominantly oxic environment. Under these new conditions photoferrotrophs lost importance as primary producers, and now photoferrotrophy remains as a vestige of a formerly relevant photosynthetic process. Apart from the geological record and other biogeochemical markers, modern environments resembling the redox conditions of these ancient oceans can offer insights into the past significance of photoferrotrophy and help to explain how this metabolism operated as an important source of organic carbon for the early biosphere. Iron-rich meromictic (permanently stratified) lakes can be considered as modern analogs of the ancient Archean ocean, as they present anoxic ferruginous water columns where light can still be available at the chemocline, thus offering suitable niches for photoferrotrophs. A few bacterial strains of purple bacteria as well as of green sulfur bacteria have been shown to possess photoferrotrophic capacities, and hence, could thrive in these modern Archean ocean analogs. Studies addressing the occurrence and the biogeochemical significance of photoferrotrophy in ferruginous environments have been conducted so far in lakes Matano, Pavin, La Cruz, and the Kabuno Bay of Lake Kivu. To date, only in the latter two lakes a biogeochemical role of photoferrotrophs has been confirmed. In this review we critically summarize the current knowledge on iron-driven photosynthesis, as a remains of ancient Earth biogeochemistry

Results of magnetic analysis

Microorganisms are a primary control on the redox-induced cycling of iron in the environment. Despite the ability of bacteria to grow using both Fe(II) and Fe(III) bound in solid-phase iron minerals, it is currently unknown if changing environmental conditions enable the sharing of electrons in mixed-valent iron oxides between bacteria with different metabolisms. We show through magnetic and spectroscopic measurements that the phototrophic Fe(II)-oxidizing bacterium Rhodopseudomonas palustris TIE-1 oxidizes magnetite (Fe3O4) nanoparticles using light energy. This process is reversible in co-cultures by the anaerobic Fe(III)-reducing bacterium Geobacter sulfurreducens. These results demonstrate that Fe ions bound in the highly crystalline mineral magnetite are bioavailable as electron sinks and electron sources under varying environmental conditions, effectively rendering a naturally occurring battery

Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria

Building a biogeochemical battery Iron acts as both a source and sink of electrons for microorganisms in the environment. Some anaerobic bacteria use oxidized Fe(III) as an electron acceptor, whereas phototrophic bacteria can use reduced Fe(II) as an electron donor. Byrne et al. show that the iron-bearing mineral magnetite, which contains both Fe(II) and Fe(III), can serve as both an electron acceptor and donor. Cocultures of iron-reducing and iron-oxidizing bacteria exposed to simulated day/night cycles or changes in organic matter altered the ratio of Fe(II) to Fe(III) in magnetite particles. Science , this issue p. 1473 </jats:p

Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

Microorganisms have been observed to oxidize Fe(II) at neutral pH under anoxic and microoxic conditions. While most of the mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria become encrusted with Fe(III)-rich minerals, photoautotrophic and microaerophilic Fe(II) oxidizers avoid cell encrustation. The Fe(II) oxidation mechanisms and the reasons for encrustation remain largely unresolved. Here we used cultivation-based methods and electron microscopy to compare two previously described nitrate-reducing Fe(II) oxidizers ( Acidovorax sp. strain BoFeN1 and Pseudogulbenkiania sp. strain 2002) and two heterotrophic nitrate reducers (Paracoccus denitrificans ATCC 19367 and P. denitrificans Pd 1222). All four strains oxidized ∼8 mM Fe(II) within 5 days in the presence of 5 mM acetate and accumulated nitrite (maximum concentrations of 0.8 to 1.0 mM) in the culture media. Iron(III) minerals, mainly goethite, formed and precipitated extracellularly in close proximity to the cell surface. Interestingly, mineral formation was also observed within the periplasm and cytoplasm; intracellular mineralization is expected to be physiologically disadvantageous, yet acetate consumption continued to be observed even at an advanced stage of Fe(II) oxidation. Extracellular polymeric substances (EPS) were detected by lectin staining with fluorescence microscopy, particularly in the presence of Fe(II), suggesting that EPS production is a response to Fe(II) toxicity or a strategy to decrease encrustation. Based on the data presented here, we propose a nitrite-driven, indirect mechanism of cell encrustation whereby nitrite forms during heterotrophic denitrification and abiotically oxidizes Fe(II). This work adds to the known assemblage of Fe(II)-oxidizing bacteria in nature and complicates our ability to delineate microbial Fe(II) oxidation in ancient microbes preserved as fossils in the geological record