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Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures.

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.

SUBMITTER: Aromokeye DA

PROVIDER: S-EPMC8115662 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Anaerobic biodegradation of aromatic compounds under sulfate-reducing conditions is important to marine sediments. Sulfate respiration by a single bacterial strain and syntrophic metabolism by a syntrophic bacterial consortium are primary strategies for sulfate-dependent biodegradation of aromatic compounds. The objective of this study was to investigate the potential of conductive iron oxides to facilitate the degradation of aromatic compounds under sulfate-reducing conditions in marine sediments, using benzoate as a model aromatic compound. Here, in anaerobic incubations of sediments from the Pearl River Estuary, the addition of hematite or magnetite (20 mM as Fe atom) enhanced the rates of sulfate-dependent benzoate degradation by 81.8 and 91.5%, respectively, compared with control incubations without iron oxides. Further experiments demonstrated that the rate of sulfate-dependent benzoate degradation accelerated with increased magnetite concentration (5, 10, and 20 mM). The detection of acetate as an intermediate product implied syntrophic benzoate degradation pathway, which was also supported by the abundance of putative acetate- or/and H2-utilizing sulfate reducers from microbial community analysis. Microbial reduction of iron oxides under sulfate-reducing conditions only accounted for 2-11% of electrons produced by benzoate oxidation, thus the stimulatory effect of conductive iron oxides on sulfate-dependent benzoate degradation was not mainly due to an increased pool of terminal electron acceptors. The enhanced rates of syntrophic benzoate degradation by the presence of conductive iron oxides probably resulted from the establishment of a direct interspecies electron transfer (DIET) between syntrophic partners. In the presence of magnetite, Bacteroidetes and Desulfobulbaceae with potential function of extracellular electron transfer might be involved in syntrophic benzoate degradation. Results from this study will contribute to the development of new strategies for in situ bioremediation of anaerobic sediments contaminated with aromatic compounds, and provide a new perspective for the natural attenuation of aromatic compounds in iron-rich marine sediments.

Project description:Syntrophic consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) consume large amounts of methane and serve as the foundational microorganisms in marine methane seeps. Despite their importance in the carbon cycle, research on the physiology of ANME-SRB consortia has been hampered by the slow growth and complex physicochemical environment the consortia inhabit. Here, we report successful sediment-free enrichment of ANME-SRB consortia from deep-sea methane seep sediments in the Santa Monica Basin, California. Anoxic Percoll density gradients and size-selective filtration were used to separate ANME-SRB consortia from sediment particles and single cells to accelerate the cultivation process. Over a 3-year period, a subset of the sediment-associated ANME and SRB lineages, predominantly comprised of ANME-2a/2b ("Candidatus Methanocomedenaceae") and their syntrophic bacterial partners, SEEP-SRB1/2, adapted and grew under defined laboratory conditions. Metagenome-assembled genomes from several enrichments revealed that ANME-2a, SEEP-SRB1, and Methanococcoides in different enrichments from the same inoculum represented distinct species, whereas other coenriched microorganisms were closely related at the species level. This suggests that ANME, SRB, and Methanococcoides are more genetically diverse than other members in methane seeps. Flow cytometry sorting and sequencing of cell aggregates revealed that Methanococcoides, Anaerolineales, and SEEP-SRB1 were overrepresented in multiple ANME-2a cell aggregates relative to the bulk metagenomes, suggesting they were physically associated and possibly interacting. Overall, this study represents a successful case of selective cultivation of anaerobic slow-growing microorganisms from sediments based on their physical characteristics, introducing new opportunities for detailed genomic, physiological, biochemical, and ecological analyses. IMPORTANCE Biological anaerobic oxidation of methane (AOM) coupled with sulfate reduction represents a large methane sink in global ocean sediments. Methane consumption is carried out by syntrophic archaeal-bacterial consortia and fuels a unique ecosystem, yet the interactions in these slow-growing syntrophic consortia and with other associated community members remain poorly understood. The significance of this study is the establishment of sediment-free enrichment cultures of anaerobic methanotrophic archaea and sulfate-reducing bacteria performing AOM with sulfate using selective cultivation approaches based on size, density, and metabolism. By reconstructing microbial genomes and analyzing community composition of the enrichment cultures and cell aggregates, we shed light on the diversity of microorganisms physically associated with AOM consortia beyond the core syntrophic partners. These enrichment cultures offer simplified model systems to extend our understanding of the diversity of microbial interactions within marine methane seeps.

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Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures.

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