It has been shown that reactive soil minerals, specifically iron(III) (oxyhydr)oxides, can trap organic carbon in soils overlying intact permafrost, and may limit carbon mobilization and degradation as it is observed in other environments. However, the use of iron(III)-bearing minerals as terminal electron acceptors in permafrost environments, and thus their stability and capacity to prevent carbon mobilization during permafrost thaw, is poorly understood. We have followed the dynamic interactions between iron and carbon using a space-for-time approach across a thaw gradient in Abisko (Sweden), where wetlands are expanding rapidly due to permafrost thaw. We show through bulk (selective extractions, EXAFS) and nanoscale analysis (correlative SEM and nanoSIMS) that organic carbon is bound to reactive Fe primarily in the transition between organic and mineral horizons in palsa underlain by intact permafrost (41.8 ± 10.8 mg carbon per g soil, 9.9 to 14.8% of total soil organic carbon). During permafrost thaw, water-logging and O2 limitation lead to reducing conditions and an increase in abundance of Fe(III)-reducing bacteria which favor mineral dissolution and drive mobilization of both iron and carbon along the thaw gradient. By providing a terminal electron acceptor, this rusty carbon sink is effectively destroyed along the thaw gradient and cannot prevent carbon release with thaw.

Anoxygenic photoautotrophic bacteria which use light energy and electrons from Fe(II) for growth, so-called photoferrotrophs, are suggested to have been amongst the first phototrophic microorganisms on Earth and to have contributed to the deposition of sedimentary iron mineral deposits, i.e. banded iron formations. To date only two isolates of marine photoferrotrophic bacteria exist, both of which are closely related purple non-sulfur bacteria. Here we present a novel green-sulfur photoautotrophic Fe(II) oxidizer isolated from a marine coastal sediment, Chlorobium sp. strain N1, which is closely related to the freshwater green-sulfur bacterium Chlorobium luteolum DSM273 that is incapable of Fe(II) oxidation. Besides Fe(II), our isolated strain grew phototrophically with other inorganic and organic substrates such as sulfide, hydrogen, lactate or yeast extract. Highest Fe(II) oxidation rates were measured at pH 7.0-7.3, the temperature optimum was 25°C. Mössbauer spectroscopy identified ferrihydrite as the main Fe(III) mineral and fluorescence and helium-ion microscopy revealed cell-mineral aggregates without obvious cell encrustation. In summary, our study showed that the new isolate is physiologically adapted to the conditions of its natural habitat but also to conditions as proposed for early Earth and is thus a suitable model organism for further studies addressing phototrophic Fe(II) oxidation on early Earth.

It has been shown that reactive soil minerals, specifically iron(III) (oxyhydr)oxides, can trap organic carbon in soils overlying intact permafrost, and may limit carbon mobilization and degradation as it is observed in other environments. However, the use of iron(III)-bearing minerals as terminal electron acceptors in permafrost environments and thus their stability and capacity to prevent carbon mobilization during permafrost thaw is poorly understood. We have followed the dynamic interactions between iron and carbon, using a “space for time” approach, across a thaw gradient in Abisko (Sweden), where wetlands are expanding rapidly due to permafrost thaw. We show through bulk (selective extractions, EXAFS) and nanoscale analysis (correlative SEM and nanoSIMS) that organic carbon is bound to reactive Fe primarily in the transition between organic and mineral horizons in palsa underlain by intact permafrost. During thaw, water-logging and O2 limitation lead to reducing conditions and an increase in abundance of Fe(III)-reducing bacteria which favor mineral dissolution and drive mobilization of both iron and carbon along the thaw gradient. By providing a terminal electron acceptor, the “rusty carbon sink” is effectively destroyed along the thaw gradient and cannot prevent carbon release with thaw.

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Anthropogenic activities are modifying the oceanic environment rapidly and are causing ocean warming and deoxygenation, affecting biodiversity, productivity, and biogeochemical cycling. In coastal sediments, anaerobic organic matter degradation essentially fuels the production of hydrogen sulfide and methane. The release of these compounds from sediments is detrimental for the (local) environment and entails socio-economic consequences. Therefore, it is vital to understand which microbes catalyze the re-oxidation of these compounds under environmental dynamics, thereby mitigating their release to the water column. Here we use the seasonally dynamic Boknis Eck study site (SW Baltic Sea), where bottom waters annually fall hypoxic or anoxic after the summer months, to extrapolate how the microbial community and its activity reflects rising temperatures and deoxygenation. During October 2018, hallmarked by warmer bottom water and following a hypoxic event, modeled sulfide and methane production and consumption rates are higher than in March at lower temperatures and under fully oxic bottom water conditions. The microbial populations catalyzing sulfide and methane metabolisms are found in shallower sediment zones in October 2018 than in March 2019. DNA-and RNA profiling of sediments indicate a shift from primarily organotrophic to (autotrophic) sulfide oxidizing Bacteria, respectively. Previous studies using data collected over decades demonstrate rising temperatures, decreasing eutrophication, lower primary production and thus less fresh organic matter transported to the Boknis Eck sediments. Elevated temperatures are known to stimulate methanogenesis, anaerobic oxidation of methane, sulfate reduction and essentially microbial sulfide consumption, likely explaining the shift to a phylogenetically more diverse sulfide oxidizing community based on RNA.

Anoxygenic phototrophic Fe(II)-oxidizers (photoferrotrophs) are thought to have thrived in Earth’s ancient ferruginous oceans and played a primary role in the precipitation of Archean and Paleoproterozoic (3.8-1.85 Ga) banded iron formations (BIF). The end of BIF deposition by photoferrotrophs has often been interpreted as being the result a deepening of water column oxygenation below the photic zone concomitant with the proliferation of cyanobacteria. We suggest here that a potentially overlooked aspect influencing BIF precipitation by photoferrotrophs is competition with another anaerobic Fe(II)-oxidizing metabolism. It is speculated that microorganisms capable of coupling Fe(II) oxidation to the reduction of nitrate were also present early in Earth history when BIF were being deposited, but the extent to which they could compete with photoferrotrophs when favourable geochemical conditions overlapped is unknown. Utilizing microbial incubations and numerical modelling, we show that nitrate-reducing Fe(II)-oxidizers metabolically outcompete photoferrotrophs for dissolved Fe(II). Moreover, the nitrate-reducing Fe(II)-oxidizers inhibit photoferrotrophy via the production of toxic nitric oxide (NO). Four different photoferrotrophs, representing both green sulfur and purple non-sulfur bacteria, are susceptible to this toxic effect despite having genomic capabilities for NO detoxification. Indeed, despite NO detoxification mechanisms being ubiquitous in some groups of phototrophs at the genomic level (e.g. Chlorobi and Cyanobacteria) it is likely they would still be influenced by NO stress. We suggest that the production of NO during nitrate-reducing Fe(II) oxidation in ferruginous environments represents an as yet unreported control on the activity of photoferrotrophs in the ancient oceans and thus the mechanisms driving precipitation of BIF.

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