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Diurnal Fe(II)/Fe(III) cycling and enhanced O₂ production in a simulated Archean marine oxygen oasis.

ABSTRACT: The oxygenation of early Earth's atmosphere during the Great Oxidation Event, is generally accepted to have been caused by oceanic Cyanobacterial oxygenic photosynthesis. Recent studies suggest that Fe(II) toxicity delayed the Cyanobacterial expansion necessary for the GOE. This study investigates the effects of Fe(II) on two Cyanobacteria, Pseudanabaena sp. PCC7367 and Synechococcus sp. PCC7336, in a simulated shallow-water marine Archean environment. A similar Fe(II) toxicity response was observed as reported for closed batch cultures. This toxicity was not observed in cultures provided with continuous gaseous exchange that showed significantly shorter doubling times than the closed-culture system, even with repeated nocturnal addition of Fe(II) for 12 days. The green rust (GR) formed under high Fe(II) conditions, was not found to be directly toxic to Pseudanabaena sp. PCC7367. In summary, we present evidence of diurnal Fe cycling in a simulated shallow-water marine environment for two ancestral strains of Cyanobacteria, with increased O₂ production under anoxic conditions.

SUBMITTER: Herrmann AJ

PROVIDER: S-EPMC8024245 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fe-organic matter (Fe-OM) complexes are abundant in the environment and, due to their mobility, reactivity, and bioavailability, play a significant role in the biogeochemical Fe cycle. In photic zones of aquatic environments, Fe-OM complexes can potentially be reduced and oxidized, and thus cycled, by light-dependent processes, including abiotic photoreduction of Fe(III)-OM complexes and microbial oxidation of Fe(II)-OM complexes, by anoxygenic phototrophic bacteria. This could lead to a cryptic iron cycle in which continuous oxidation and rereduction of Fe could result in a low and steady-state Fe(II) concentration despite rapid Fe turnover. However, the coupling of these processes has never been demonstrated experimentally. In this study, we grew a model anoxygenic phototrophic Fe(II) oxidizer, Rhodobacter ferrooxidans SW2, with either citrate, Fe(II)-citrate, or Fe(III)-citrate. We found that strain SW2 was capable of reoxidizing Fe(II)-citrate produced by photochemical reduction of Fe(III)-citrate, which kept the dissolved Fe(II)-citrate concentration at low (<10 μM) and stable concentrations, with a concomitant increase in cell numbers. Cell suspension incubations with strain SW2 showed that it can also oxidize Fe(II)-EDTA, Fe(II)-humic acid, and Fe(II)-fulvic acid complexes. This work demonstrates the potential for active cryptic Fe cycling in the photic zone of anoxic aquatic environments, despite low measurable Fe(II) concentrations which are controlled by the rate of microbial Fe(II) oxidation and the identity of the Fe-OM complexes.IMPORTANCE Iron cycling, including reduction of Fe(III) and oxidation of Fe(II), involves the formation, transformation, and dissolution of minerals and dissolved iron-organic matter compounds. It has been shown previously that Fe can be cycled so rapidly that no measurable changes in Fe(II) and Fe(III) concentrations occur, leading to a so-called cryptic cycle. Cryptic Fe cycles have been shown to be driven either abiotically by a combination of photochemical reduction of Fe(III)-OM complexes and reoxidation of Fe(II) by O2, or microbially by a combination of Fe(III)-reducing and Fe(II)-oxidizing bacteria. Our study demonstrates a new type of light-driven cryptic Fe cycle that is relevant for the photic zone of aquatic habitats involving abiotic photochemical reduction of Fe(III)-OM complexes and microbial phototrophic Fe(II) oxidation. This new type of cryptic Fe cycle has important implications for biogeochemical cycling of iron, carbon, nutrients, and heavy metals and can also influence the composition and activity of microbial communities.

Project description:BackgroundMany environments contain redox transition zones, where transient oxygenation events can modulate anaerobic reactions that influence the cycling of iron (Fe) and carbon (C) on a global scale. In predominantly anoxic soils, this biogeochemical cycling depends on Fe mineral composition and the activity of mixed Fe(III)-reducer populations that may be altered by periodic pulses of molecular oxygen (O2).MethodsWe repeatedly exposed anoxic (4% H2:96% N2) suspensions of soil from the Luquillo Critical Zone Observatory to 1.05 × 102, 1.05 × 103, and 1.05 × 104 mmol O2 kg-1 soil h-1 during pulsed oxygenation treatments. Metatranscriptomic analysis and 57Fe Mössbauer spectroscopy were used to investigate changes in Fe(III)-reducer gene expression and Fe(III) crystallinity, respectively.ResultsSlow oxygenation resulted in soil Fe-(oxyhydr)oxides of higher crystallinity (38.1 ± 1.1% of total Fe) compared to fast oxygenation (30.6 ± 1.5%, P < 0.001). Transcripts binning to the genomes of Fe(III)-reducers Anaeromyxobacter, Geobacter, and Pelosinus indicated significant differences in extracellular electron transport (e.g., multiheme cytochrome c, multicopper oxidase, and type-IV pilin gene expression), adhesion/contact (e.g., S-layer, adhesin, and flagellin gene expression), and selective microbial competition (e.g., bacteriocin gene expression) between the slow and fast oxygenation treatments during microbial Fe(III) reduction. These data also suggest that diverse Fe(III)-reducer functions, including cytochrome-dependent extracellular electron transport, are associated with type-III fibronectin domains. Additionally, the metatranscriptomic data indicate that Methanobacterium was significantly more active in the reduction of CO2 to CH4 and in the expression of class(III) signal peptide/type-IV pilin genes following repeated fast oxygenation compared to slow oxygenation.ConclusionsThis study demonstrates that specific Fe(III)-reduction mechanisms in mixed Fe(III)-reducer populations are uniquely sensitive to the rate of O2 influx, likely mediated by shifts in soil Fe(III)-(oxyhydr)oxide crystallinity. Overall, we provide evidence that transient oxygenation events play an important role in directing anaerobic pathways within soil microbiomes, which is expected to alter Fe and C cycling in redox-dynamic environments.

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Diurnal Fe(II)/Fe(III) cycling and enhanced O₂ production in a simulated Archean marine oxygen oasis.

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Diurnal Fe(II)/Fe(III) cycling and enhanced O2 production in a simulated Archean marine oxygen oasis.

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OmicsDI is part of the ELIXIR infrastructure

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Diurnal Fe(II)/Fe(III) cycling and enhanced O₂ production in a simulated Archean marine oxygen oasis.