Abstract
Elevated dissolved iron concentrations in the methanic zone are typical geochemical signatures of rapidly accumulating marine sediments. These sediments are often characterized by co-burial of iron oxides with recalcitrant aromatic organic matter of terrigenous origin. Thus far, iron oxides are predicted to either impede organic matter degradation, aiding its preservation, or identified to enhance organic carbon oxidation via direct electron transfer. Here, we investigated the effect of various iron oxide phases with differing crystallinity (magnetite, hematite, and lepidocrocite) during microbial degradation of the aromatic model compound benzoate in methanic sediments. In slurry incubations with magnetite or hematite, concurrent iron reduction, and methanogenesis were stimulated during accelerated benzoate degradation with methanogenesis as the dominant electron sink. In contrast, with lepidocrocite, benzoate degradation, and methanogenesis were inhibited. These observations were reproducible in sediment-free enrichments, even after five successive transfers. Genes involved in the complete degradation of benzoate were identified in multiple metagenome assembled genomes. Four previously unknown benzoate degraders of the genera Thermincola (Peptococcaceae, Firmicutes), Dethiobacter (Syntrophomonadaceae, Firmicutes), Deltaproteobacteria bacteria SG8_13 (Desulfosarcinaceae, Deltaproteobacteria), and Melioribacter (Melioribacteraceae, Chlorobi) were identified from the marine sediment-derived enrichments. Scanning electron microscopy (SEM) and catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) images showed the ability of microorganisms to colonize and concurrently reduce magnetite likely stimulated by the observed methanogenic benzoate degradation. These findings explain the possible contribution of organoclastic reduction of iron oxides to the elevated dissolved Fe2+ pool typically observed in methanic zones of rapidly accumulating coastal and continental margin sediments.
Highlights
Microbial degradation of organic matter controls the carbon flux and biogeochemical cycling of elements in marine environments [1, 2]
By stimulating microbial communities involved in concurrent benzoate degradation, iron reduction and methanogenesis, the findings demonstrate how crystalline iron oxides enhance the ability of microorganisms to efficiently degrade recalcitrant organic matter in methanic marine sediments
The results presented show sediment-free microbial communities involved in benzoate degradation with methanogenesis as primary electron sink
Summary
Microbial degradation of organic matter controls the carbon flux and biogeochemical cycling of elements in marine environments [1, 2]. Crystalline iron oxide phases accelerate organic carbon degradation to methane as primary electron sink (i.e., methanogenic degradation) in rice field soils, lake, and marine sediments by serving as conduits for direct electron transfer [24–27] Given these previous findings, a hitherto unexplored strategy for microbes to efficiently degrade recalcitrant organic matter may rely on crystalline iron oxides acting concurrently as electron acceptors while serving as conduits. We hypothesize that during the degradation of recalcitrant organic matter of terrestrial origin, crystalline portions of co-buried iron oxides act as conduits, facilitating efficient methanogenic organic matter degradation The feasibility of this concurrent dual role of crystalline iron oxides has not yet been demonstrated in marine sediments and is the focus of this study. Our results show (1) how the presence of crystalline iron oxides stimulates methanogenic benzoate degradation, (2) the possible dynamics of microbe-crystalline mineral interaction during recalcitrant organic matter degradation, and (3) novel benzoate degrading communities enriched from marine sediments
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