Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

Klueglein, Nicole; Zeitvogel, Fabian; Stierhof, York‐Dieter; Floetenmeyer, Matthias; Konhauser, Kurt O.; Kappler, Andreas; Obst, Martin

doi:10.1128/aem.03277-13

Cited by 182 publications

(250 citation statements)

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“…Interestingly, Fe(II) oxidation seems to be a universal ability of all NO 3 Ϫ -reducing bacteria when an organic substrate is provided (28). A unique feature of this group of Fe(II) oxidizers is that the cells become encrusted with Fe(III) minerals during Fe(II) oxidation (27), a process that is potentially harmful to the cells (29). A few strains have been proposed to be able to live autotrophically with only NO 3 Ϫ and Fe(II) (4,(30)(31)(32)(33)(34)(35), although unambiguous evidence for this is missing.…”

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confidence: 99%

“…For these mixotrophic strains, it is not yet known whether Fe(II) oxidation is just a chemical side reaction with nitrite, which is produced during heterotrophic denitrification (26,27), or if it is an enzymatic reaction from which the bacteria can gain energy. Interestingly, Fe(II) oxidation seems to be a universal ability of all NO 3 Ϫ -reducing bacteria when an organic substrate is provided (28).…”

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confidence: 99%

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Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

Laufer

Nordhoff

Røy

et al. 2016

Appl Environ Microbiol

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Iron is abundant in sediments, where it can be biogeochemically cycled between its divalent and trivalent redox states. The neutrophilic microbiological Fe cycle involves Fe(III)-reducing and three different physiological groups of Fe(II)-oxidizing microorganisms, i.e., microaerophilic, anoxygenic phototrophic, and nitrate-reducing Fe(II) oxidizers. However, it is unknown whether all three groups coexist in one habitat and how they are spatially distributed in relation to gradients of O 2 , light, nitrate, and Fe(II). We examined two coastal marine sediments in Aarhus Bay, Denmark, by cultivation and most probable number ( Fe(III)-reducing microorganisms were discovered in the late 1980s (6). Many of the better-known Fe(III)-reducing bacteria of the genera Shewanella, Geobacter, and Geothrix are found mainly in freshwater and more rarely in marine sediments (7,8). Still, Fe(III) reduction can account for a large fraction of organic-matter mineralization in coastal marine sediments (up to 50%) (9).Fe(II)-oxidizing bacteria were first described in 1836 by Ehrenberg (10) as so-called "iron bacteria." It took more than a century before the first microbes belonging to this group could be grown in the laboratory (11) and even longer until it was demonstrated that they grow autotrophically by oxidizing Fe(II) with O 2 (12). These bacteria face the problem that, at neutral pH, the abiotic reaction of oxygen and Fe(II) is fast. Therefore, bacterial Fe(II) oxidation with O 2 at neutral pH is limited to micro-oxic ([O 2 ] Ͻ 50 M) conditions, where microbial iron oxidation can compete favorably with the [O 2 ]-limited abiotic reaction (13,14). Favorable conditions for the growth of microaerophilic Fe(II) oxidizers are found in opposing gradients of Fe(II) and O 2 , e.g., in the oxicanoxic transition zone in sediments or groundwater seeps (15). Today, there are at least four known groups of exclusively microaerophilic Fe(II) oxidizers, i.e., Gallionella (11, 12), Sideroxydans (3), Leptothrix (16,17), and Mariprofundus (18). Furthermore, certain bacteria belonging to the genera Marinobacter and Hyphomonas are also described as growing under micro-oxic conditions by Fe(II) oxidation (19,20).The photoferrotrophs (5) are not only of interest for modern habitats, but may also be responsible for the formation of banded iron formations (BIFs) in the Precambrian (21,22). Until now, only a few pure cultures have been known, and there is no known monophylogenetic group that specializes solely in anoxygenic phototrophic Fe(II) oxidation. Known strains are metabolically flexible and belong to various physiological groups of anoxygenic phototrophs, i.e., the purple sulfur, purple nonsulfur, and green anoxygenic phototrophic bacteria (5,(23)(24)(25).For the nitrate-reducing Fe(II) oxidizers, most known strains cannot be maintained in culture over several transfers with nitrate

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confidence: 99%

mentioning

confidence: 99%

Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

Laufer

Nordhoff

Røy

et al. 2016

Appl Environ Microbiol

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“…Under these conditions, we found that completely consuming cells always consume all of the nitrogen oxides more rapidly than co-cultures of nitrite cross-feeding cells, regardless of the magnitude of nitrite inhibition (i.e., t stat,CF /t stat,CC is always greater than 1 and increases monotonically as nitrite inhibition increases; Figure 6, solid line). However, if mass transfer of nitrite between the periplasm and the culture medium is slower than the maximum reaction rate of the nitrate and nitrite reductases, which is supported by experimental evidence (Klueglein et al, 2014), then the concentrations of nitrite within the periplasm of the nitrite-consuming cells are necessarily less than in the culture medium (i.e., nitrite is consumed faster than it enters the cell). This reduces nitrite inhibition of nitrite-consuming cells and consequently accelerates nitrite consumption, thus reducing nitrite accumulation.…”

Section: Alternative Explanations For the Accumulation Of Nitritementioning

confidence: 96%

“…Second, we can manipulate the growth-inhibiting effects of the cross-fed metabolic intermediatenitrite-and measure the consequences on substrate consumption. Nitrite accumulates within the periplasm during denitrification (Lalucat et al, 2006;Klueglein et al, 2014) and can inhibit growth by at least two different pH-dependent mechanisms, both of which act indirectly. First, as the pH decreases, nitrite increasingly protonates to nitrous acid (HNO 2 ) and uncouples proton translocation (Sijbesma et al, 1996;Zhou et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates

2016

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Different microbial cell types typically specialize at performing different metabolic processes. A canonical example is substrate cross-feeding, where one cell type consumes a primary substrate into an intermediate and another cell type consumes the intermediate. While substrate cross-feeding is widely observed, its consequences on ecosystem processes is often unclear. How does substrate cross-feeding affect the rate or extent of substrate consumption? We hypothesized that substrate cross-feeding eliminates competition between different enzymes and reduces the accumulation of growth-inhibiting intermediates, thus accelerating substrate consumption. We tested this hypothesis using isogenic mutants of the bacterium Pseudomonas stutzeri that either completely consume nitrate to dinitrogen gas or cross-feed the intermediate nitrite. We demonstrate that nitrite crossfeeding eliminates inter-enzyme competition and, in turn, reduces nitrite accumulation. We further demonstrate that nitrite cross-feeding accelerates substrate consumption, but only when nitrite has growth-inhibiting effects. Knowledge about inter-enzyme competition and the inhibitory effects of intermediates could therefore be important for deciding how to best segregate different metabolic processes into different microbial cell types to optimize a desired biotransformation.

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“…Nitrite, if accumulated, can rapidly react abiotically with dissolved Fe(II) (53), forming precipitates at the cell surface and leading to periplasmic and eventually cytoplasmic mineralization (54). Therefore, rapid biological reduction of nitrite may be important for achieving robust NDFO.…”

Section: G a Ll Io N E Ll A C E A E C O M A M O N A D A C E A E R H Imentioning

confidence: 99%

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Tominski

Kappler

et al. 2016

Appl Environ Microbiol

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f Nitrate-dependent ferrous iron [Fe(II)] oxidation (NDFO) is a well-recognized chemolithotrophic pathway in anoxic sediments. The neutrophilic chemolithoautotrophic enrichment culture KS originally obtained from a freshwater sediment (K. L. Straub, M. Benz, B. Schink, and F. Widdel, Appl Environ Microbiol 62:1458 -1460, 1996) has been used as a model system to study NDFO. However, the primary Fe(II) oxidizer in this culture has not been isolated, despite extensive efforts to do so. Here, we present a metagenomic analysis of this enrichment culture in order to gain insight into electron transfer pathways and the roles of different bacteria in the culture. We obtained a near-complete genome of the primary Fe(II) oxidizer, a species in the family Gallionellaceae, and draft genomes from its flanking community members. A search of the putative extracellular electron transfer pathways in these genomes led to the identification of a homolog of the MtoAB complex [a porin-multiheme cytochrome c system identified in neutrophilic microaerobic Fe(II)-oxidizing Sideroxydans lithotrophicus ES-1] in a Gallionellaceae sp., and findings of other putative genes involving cytochrome c and multicopper oxidases, such as Cyc2 and OmpB. Genome-enabled metabolic reconstruction revealed that this Gallionellaceae sp. lacks nitric oxide and nitrous oxide reductase genes and may partner with flanking populations capable of complete denitrification to avoid toxic metabolite accumulation, which may explain its resistance to growth in pure culture. This and other revealed interspecies interactions and metabolic interdependencies in nitrogen and carbon metabolisms may allow these organisms to cooperate effectively to achieve robust chemolithoautotrophic NDFO. Overall, the results significantly expand our knowledge of NDFO and suggest a range of genetic targets for further exploration.

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Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

Cited by 182 publications

References 79 publications

Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

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