Cryptic Cycling of Complexes Containing Fe(III) and Organic Matter by Phototrophic Fe(II)-Oxidizing Bacteria

Cryptic Cycling of Complexes Containing Fe(III) and Organic Matter by Phototrophic Fe(II)-Oxidizing Bacteria
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光养型 Fe(II) 氧化细菌对含 Fe(III) 和有机物的复合物进行隐性循环

DOI:
10.1128/aem.02826-18
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发表时间:
2019
影响因子:
4.4
通讯作者:
Kappler
Kappler
中科院分区:
生物学2区
文献类型:
--
作者:
Sundman;Kappler

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Fe-有机物(Fe- om)配合物在环境中丰富,由于其迁移性、反应性和生物利用度,在生物地球化学铁循环中起着重要作用。在水生环境的光区,Fe-OM配合物可以通过依赖光的过程被潜在地还原和氧化,从而循环,包括Fe(III)-OM配合物的非生物光还原和Fe(II)-OM配合物的微生物氧化,由无氧光养细菌进行。这可能导致一个隐铁循环,其中铁的持续氧化和还原可能导致低且稳定的铁(II)浓度,尽管铁的快速周转。然而,这些过程的耦合从未在实验中得到证实。在这项研究中,我们培养了一个无氧光养铁(II)氧化剂模型,氧化亚铁红杆菌SW2,其中有柠檬酸盐、铁(II)-柠檬酸盐或铁(III)-柠檬酸盐。结果表明,菌株SW2能够对Fe(III)-柠檬酸盐光化学还原产生的Fe(II)-柠檬酸盐进行再氧化,使溶解的Fe(II)-柠檬酸盐浓度保持在较低(<10 μM)且稳定的浓度,同时细胞数量增加。菌株SW2的细胞悬浮培养表明,它还能氧化Fe(II)-EDTA、Fe(II)-腐殖酸和Fe(II)-黄腐酸配合物。这项工作表明,尽管微生物铁(II)氧化速率和铁- om络合物的特性控制了可测量的低铁(II)浓度,但在缺氧水生环境的光区,潜在的活跃的隐铁循环是可能的。铁循环,包括铁(III)的还原和铁(II)的氧化,涉及矿物和溶解的铁-有机物化合物的形成、转化和溶解。以前的研究表明,铁的循环速度非常快,以至于铁(II)和铁(III)的浓度不会发生可测量的变化,从而导致所谓的隐循环。已经证明,隐铁循环要么是由Fe(III)-OM络合物的光化学还原和Fe(II)被O2再氧化的非生物组合驱动的,要么是由Fe(III)还原和Fe(II)氧化细菌的微生物组合驱动的。我们的研究证明了一种新型的光驱动隐铁循环,它与水生栖息地的光区有关,涉及铁(III)-OM复合物的非生物光化学还原和微生物光养铁(II)氧化。这种新型的隐铁循环对铁、碳、营养物质和重金属的生物地球化学循环具有重要意义,也可以影响微生物群落的组成和活性。
Fe-organic matter (Fe-OM) complexes are abundant in the environment and, due to their mobility, reactivity, and bioavailability, play a significant role in the biogeochemical Fe cycle. In photic zones of aquatic environments, Fe-OM complexes can potentially be reduced and oxidized, and thus cycled, by light-dependent processes, including abiotic photoreduction of Fe(III)-OM complexes and microbial oxidation of Fe(II)-OM complexes, by anoxygenic phototrophic bacteria. This could lead to a cryptic iron cycle in which continuous oxidation and rereduction of Fe could result in a low and steady-state Fe(II) concentration despite rapid Fe turnover. However, the coupling of these processes has never been demonstrated experimentally. In this study, we grew a model anoxygenic phototrophic Fe(II) oxidizer, Rhodobacter ferrooxidans SW2, with either citrate, Fe(II)-citrate, or Fe(III)-citrate. We found that strain SW2 was capable of reoxidizing Fe(II)-citrate produced by photochemical reduction of Fe(III)-citrate, which kept the dissolved Fe(II)-citrate concentration at low (<10 μM) and stable concentrations, with a concomitant increase in cell numbers. Cell suspension incubations with strain SW2 showed that it can also oxidize Fe(II)-EDTA, Fe(II)-humic acid, and Fe(II)-fulvic acid complexes. This work demonstrates the potential for active cryptic Fe cycling in the photic zone of anoxic aquatic environments, despite low measurable Fe(II) concentrations which are controlled by the rate of microbial Fe(II) oxidation and the identity of the Fe-OM complexes.IMPORTANCEIron cycling, including reduction of Fe(III) and oxidation of Fe(II), involves the formation, transformation, and dissolution of minerals and dissolved iron-organic matter compounds. It has been shown previously that Fe can be cycled so rapidly that no measurable changes in Fe(II) and Fe(III) concentrations occur, leading to a so-called cryptic cycle. Cryptic Fe cycles have been shown to be driven either abiotically by a combination of photochemical reduction of Fe(III)-OM complexes and reoxidation of Fe(II) by O2, or microbially by a combination of Fe(III)-reducing and Fe(II)-oxidizing bacteria. Our study demonstrates a new type of light-driven cryptic Fe cycle that is relevant for the photic zone of aquatic habitats involving abiotic photochemical reduction of Fe(III)-OM complexes and microbial phototrophic Fe(II) oxidation. This new type of cryptic Fe cycle has important implications for biogeochemical cycling of iron, carbon, nutrients, and heavy metals and can also influence the composition and activity of microbial communities.
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