Faculty of Biology/Chemistry, University of Bremen, Bremen, Germany.
MARUM-Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.
ISME J. 2021 Apr;15(4):965-980. doi: 10.1038/s41396-020-00824-7. Epub 2020 Nov 5.
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 Fe pool typically observed in methanic zones of rapidly accumulating coastal and continental margin sediments.
甲烷区溶解态铁浓度升高是海洋沉积物快速积累的典型地球化学特征。这些沉积物的特点通常是铁氧化物与源自陆源的难降解芳香族有机物共埋。到目前为止，铁氧化物被预测要么阻碍有机质降解，有助于其保存，要么通过直接电子转移来促进有机碳氧化。在这里，我们研究了不同结晶度的各种氧化铁相（磁铁矿、赤铁矿和纤铁矿）在甲烷沉积物中芳香族模型化合物苯甲酸微生物降解过程中的影响。在含有磁铁矿或赤铁矿的泥浆培养中，在加速苯甲酸降解过程中同时刺激了铁还原和产甲烷作用，而产甲烷作用是主要的电子汇。相比之下，添加纤铁矿则抑制了苯甲酸的降解和产甲烷作用。这些观察结果在无沉积物的富集物中是可重复的，甚至在连续五次传代后也是如此。在多个宏基因组组装基因组中鉴定出了参与苯甲酸完全降解的基因。从海洋沉积物衍生的富集物中鉴定出了四个以前未知的苯甲酸降解菌，属于 Thermincola（Peptococcaceae，Firmicutes）、Dethiobacter（Syntrophomonadaceae，Firmicutes）、Deltaproteobacteria 细菌 SG8_13（Desulfosarcinaceae，Deltaproteobacteria）和 Melioribacter（Melioribacteraceae，Chlorobi）属。扫描电子显微镜（SEM）和催化报告物沉积荧光原位杂交（CARD-FISH）图像显示，微生物能够定植并同时还原磁铁矿，这可能是由于观察到的产甲烷苯甲酸降解所刺激的。这些发现解释了有机络合还原铁氧化物对快速积累的沿海和大陆边缘沉积物甲烷区中通常观察到的溶解态 Fe 库升高的可能贡献。
