Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction

Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction
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DOI:
10.1073/pnas.1203885109
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发表时间:
2012-07-31
影响因子:
11.1
通讯作者:
Webb, Samuel M.
Webb, Samuel M.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Hansel, Colleen M.;Zeiner, Carolyn A.;Webb, Samuel M.

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锰(Mn)氧化物是环境中最具反应性的矿物质之一,它们控制着碳,营养素和许多金属的生物利用度。尽管微生物将Mn(II)氧化成Mn(III/IV)氧化物的能力分散在细菌和真菌的生命领域中,但Mn(II)氧化的机制和生理基础仍然是一个谜。在这里,我们使用的化合物特定的化学分析,显微光谱学和电子显微镜的组合,以显示一个共同的子囊菌丝状真菌,刺状斯氏藻,氧化锰(II)锰氧化物,通过在细胞分化过程中产生细胞外超氧化物。活性锰氧化物相水钠锰矿和活性氧物种超氧化物和过氧化氢共定位在无性生殖结构的基础上。在超氧化物清除剂(例如,Cu)和NADPH氧化酶的抑制剂(例如,二亚苯基氯化碘鎓),负责真菌中超氧化物产生和细胞分化的酶。考虑到最近通过一种常见的海洋细菌(Rosebrum sp.)的基于NADH氧化酶的超氧化物产生对Mn(II)氧化的鉴定,这些结果在负责Mn(II)氧化的机制中引入了一些原核生物和真核生物之间令人惊讶的同源性,其中氧化似乎是细胞外超氧化物产生的副反应。考虑到超氧化物作为氧化还原反应物的多功能性和真菌产生超氧化物的广泛能力,这种微生物胞外超氧化物产生可能在金属的循环和生物利用度中发挥核心作用(例如,汞,铁,锰)和碳的自然系统。
Manganese (Mn) oxides are among the most reactive minerals within the environment, where they control the bioavailability of carbon, nutrients, and numerous metals. Although the ability of microorganisms to oxidize Mn(II) to Mn(III/IV) oxides is scattered throughout the bacterial and fungal domains of life, the mechanism and physiological basis for Mn(II) oxidation remains an enigma. Here, we use a combination of compound-specific chemical assays, microspectroscopy, and electron microscopy to show that a common Ascomycete filamentous fungus, Stilbella aciculosa, oxidizes Mn(II) to Mn oxides by producing extracellular superoxide during cell differentiation. The reactive Mn oxide phase birnessite and the reactive oxygen species superoxide and hydrogen peroxide are colocalized at the base of asexual reproductive structures. Mn oxide formation is not observed in the presence of superoxide scavengers (e.g., Cu) and inhibitors of NADPH oxidases (e.g., diphenylene iodonium chloride), enzymes responsible for superoxide production and cell differentiation in fungi. Considering the recent identification of Mn(II) oxidation by NADH oxidase-based superoxide production by a common marine bacterium (Roseobacter sp.), these results introduce a surprising homology between some prokaryotic and eukaryotic organisms in the mechanisms responsible for Mn(II) oxidation, where oxidation appears to be a side reaction of extracellular superoxide production. Given the versatility of superoxide as a redox reactant and the widespread ability of fungi to produce superoxide, this microbial extracellular superoxide production may play a central role in the cycling and bioavailability of metals (e.g., Hg, Fe, Mn) and carbon in natural systems.