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Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures
The ISME Journal ( IF 11.0 ) Pub Date : 2020-11-05 , DOI: 10.1038/s41396-020-00824-7
David A Aromokeye 1, 2 , Oluwatobi E Oni 1 , Jan Tebben 3 , Xiuran Yin 1, 2 , Tim Richter-Heitmann 1 , Jenny Wendt 2, 4 , Rolf Nimzyk 1 , Sten Littmann 5 , Daniela Tienken 5 , Ajinkya C Kulkarni 1 , Susann Henkel 2, 3 , Kai-Uwe Hinrichs 2, 4 , Marcus Elvert 2, 4 , Tilmann Harder 1, 3 , Sabine Kasten 2, 3, 4 , Michael W Friedrich 1, 2
Affiliation  

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.



中文翻译:

结晶氧化铁刺激海洋沉积物衍生的富集培养物中产甲烷苯甲酸盐的降解

甲烷化带中溶解铁浓度升高是快速积累海洋沉积物的典型地球化学特征。这些沉积物的特征通常是氧化铁与陆源顽固芳香族有机物共埋。到目前为止,预计氧化铁会阻止有机物降解,帮助其保存,或被确定为通过直接电子转移增强有机碳氧化。在这里,我们研究了甲烷沉积物中芳香模型化合物苯甲酸盐在微生物降解过程中具有不同结晶度的各种氧化铁相(磁铁矿、赤铁矿和纤铁矿)的影响。在与磁铁矿或赤铁矿的泥浆孵育中,同时进行铁还原,和甲烷生成在加速苯甲酸盐降解过程中受到刺激,甲烷生成是主要的电子汇。相反,纤铁矿可抑制苯甲酸盐降解和产甲烷作用。即使在连续五次转移之后,这些观察结果在无沉积物富集中也是可重复的。在多个宏基因组组装的基因组中鉴定出参与苯甲酸盐完全降解的基因。该属的四种以前未知的苯甲酸盐降解剂Thermincola (Peptococcaceae, Firmicutes) 、Dethiobacter (Syntrophomonadaceae, Firmicutes)、Deltaproteobacteria 细菌 SG8_13 (Desulfosarcinaceae, Deltaproteobacteria) 和Melioribacter (Melioribacteraceae, Chlorobi) 从海洋沉积物衍生的富集物中鉴定出来。扫描电子显微镜 (SEM) 和催化报告基因沉积荧光原位杂交 (CARD-FISH) 图像显示微生物定殖并同时减少磁铁矿的能力,这可能是由观察到的产甲烷苯甲酸盐降解所刺激的。这些发现解释了氧化铁的有机碎屑还原对升高的溶解 Fe 2+的可能贡献通常在快速积累的沿海和大陆边缘沉积物的甲烷化带中观察到的池。

更新日期:2020-11-06
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