LCZO -- Soil Microbes, Soil Biogeochemistry -- Iron redox, Soil Microbiome -- Bisley -- (2012-2017)

Background

Many 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).

Methods

We 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.

Results

Slow 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.

Conclusions

This 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.

背景
众多环境中存在氧化还原过渡区，其中短暂的氧合事件能够调节厌氧反应，进而影响全球范围内铁（Fe）和碳（C）的循环。在以缺氧为主的土壤中，这种生物地球化学循环依赖于铁矿物的组成以及可能受到周期性分子氧（O2）脉冲影响的混合Fe(III)-还原微生物群体的活性。

方法
我们反复将来自卢基洛关键带观测站的缺氧（4% H2:96% N2）土壤悬浮液暴露于1.05 × 10^2、1.05 × 10^3和1.05 × 10^4 mmol O2 kg−1土壤 h−1的氧气脉冲中。通过元转录组分析和57Fe Mössbauer光谱学，我们分别研究了Fe(III)-还原基因表达和Fe(III)结晶度的变化。

结果
缓慢的氧合导致土壤中Fe-(氧水)氧化物的结晶度（占总Fe的38.1 ± 1.1%）高于快速氧合（30.6 ± 1.5%，P < 0.001）。将转录本分箱到Fe(III)-还原微生物Anaeromyxobacter、Geobacter和Pelosinus的基因组中，表明在微生物Fe(III)还原过程中，缓慢和快速氧合处理之间存在显著的差异，例如细胞外电子传递（例如，多铁卟啉细胞色素c、多铜氧化酶和IV型菌毛基因的表达）、粘附/接触（例如，S层、粘附素和鞭毛蛋白基因的表达）以及选择性微生物竞争（例如，细菌素基因的表达）。这些数据还表明，包括细胞色素依赖性细胞外电子传递在内的多种Fe(III)-还原功能与III型纤连蛋白结构域相关。此外，元转录组数据还显示，在重复快速氧合后，甲烷杆菌在将CO2还原为CH4以及在表达III类信号肽/IV型菌毛基因方面的活性显著高于缓慢氧合。

结论
本研究证明，混合Fe(III)-还原微生物群体中的特定Fe(III)-还原机制对O2流入速率特别敏感，这可能是通过土壤Fe(III)-(氧水)氧化物结晶度的变化介导的。总体而言，我们提供了证据，表明短暂的氧合事件在指导土壤微生物群落中的厌氧途径中发挥着重要作用，这预计将改变氧化还原动态环境中的铁和碳循环。