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
Summary Microaerophilic, phototrophic and nitrate‐reducing Fe(II)‐oxidizers co‐exist in coastal marine and littoral freshwater sediments. However, the in situ abundance, distribution and diversity of metabolically active Fe(II)‐oxidizers remained largely unexplored. Here, we characterized the microbial community composition at the oxic‐anoxic interface of littoral freshwater (Lake Constance, Germany) and coastal marine sediments (Kalø Vig and Norsminde Fjord, Denmark) using DNA‐/RNA‐based next‐generation 16S rRNA (gene) amplicon sequencing. All three physiological groups of neutrophilic Fe(II)‐oxidizing bacteria were found to be active in marine and freshwater sediments, revealing up to 0.2% anoxygenic photoferrotrophs (e.g., Rhodopseudomonas, Rhodobacter, Chlorobium), 0.1% microaerophilic Fe(II)‐oxidizers (e.g., Mariprofundus, Hyphomonas, Gallionella) and 0.3% nitrate‐reducing Fe(II)‐oxidizers (e.g., Thiobacillus, Pseudomonas, Denitromonas, Hoeflea). Active Fe(III)‐reducing bacteria (e.g., Shewanella, Geobacter) were most abundant (up to 2.8%) in marine sediments and co‐occurred with cable bacteria (up to 4.5%). Geochemical profiles of Fe(III), Fe(II), O2, light, nitrate and total organic carbon revealed a redox stratification of the sediments and explained 75%–85% of the vertical distribution of microbial taxa, while active Fe‐cycling bacteria were found to be decoupled from geochemical gradients. We suggest that metabolic flexibility, microniches in the sediments, or interrelationships with cable bacteria might explain the distribution patterns of active Fe‐cycling bacteria.
Glacial retreat is changing biogeochemical cycling in the Arctic, where glacial runoff contributes iron for oceanic shelf primary production. We hypothesize that in Svalbard fjords, microbes catalyze intense iron and sulfur cycling in loworganic-matter sediments. This is because low organic matter limits sulfide generation, allowing iron mobility to the water column instead of precipitation as iron monosulfides. In this study, we tested this with high-depth-resolution 16S rRNA gene libraries in the upper 20 cm at two sites in Van Keulenfjorden, Svalbard. At the site closer to the glaciers, iron-reducing Desulfuromonadales, iron-oxidizing Gallionella and Mariprofundus, and sulfur-oxidizing Thiotrichales and Epsilonproteobacteria were abundant above a 12-cm depth. Below this depth, the relative abundances of sequences for sulfate-reducing Desulfobacteraceae and Desulfobulbaceae increased. At the outer station, the switch from iron-cycling clades to sulfate reducers occurred at shallower depths (ϳ5 cm), corresponding to higher sulfate reduction rates. Relatively labile organic matter (shown by ␦ 13 C and C/N ratios) was more abundant at this outer site, and ordination analysis suggested that this affected microbial community structure in surface sediments. Network analysis revealed more correlations between predicted iron-and sulfur-cycling taxa and with uncultured clades proximal to the glacier. Together, these results suggest that complex microbial communities catalyze redox cycling of iron and sulfur, especially closer to the glacier, where sulfate reduction is limited due to low availability of organic matter. Diminished sulfate reduction in upper sediments enables iron to flux into the overlying water, where it may be transported to the shelf. IMPORTANCE Glacial runoff is a key source of iron for primary production in the Arctic. In the fjords of the Svalbard archipelago, glacial retreat is predicted to stimulate phytoplankton blooms that were previously restricted to outer margins. Decreased sediment delivery and enhanced primary production have been hypothesized to alter sediment biogeochemistry, wherein any free reduced iron that could potentially be delivered to the shelf will instead become buried with sulfide generated through microbial sulfate reduction. We support this hypothesis with sequencing data that showed increases in the relative abundance of sulfate reducing taxa and sulfate reduction rates with increasing distance from the glaciers in Van Keulenfjorden, Svalbard. Community structure was driven by organic geochemistry, suggesting that enhanced input of organic material will stimulate sulfate reduction in interior fjord sediments as glaciers continue to recede.
Coastal marine sediments contain varying concentrations of iron, oxygen, nitrate and organic carbon. It is unknown how organic carbon content influences the activity of nitrate-reducing and phototrophic Fe(II)-oxidizers and microbial Fe-redox cycling in such sediments. Therefore, microcosms were prepared with two coastal marine sediments (Kalø Vig and Norsminde Fjord at Aarhus Bay, Denmark) varying in TOC from 0.4 to 3.0 wt%. The microcosms were incubated under light/dark conditions with/without addition of nitrate and/or Fe(II). Although most probable number (MPN) counts of phototrophic Fe(II)-oxidizers were five times lower in the low-TOC sediment, phototrophic Fe(II) oxidation rates were higher compared with the high-TOC sediment. Fe(III)-amended microcosms showed that this lower net Fe(II) oxidation in the high-TOC sediment is caused by concurrent bacterial Fe(III) reduction. In contrast, MPN counts of nitrate-reducing Fe(II)-oxidizers and net rates of nitrate-reducing Fe(II) oxidation were comparable in low- and high-TOC sediments. However, the ratio of nitratereduced :iron(II)oxidized was higher in the high-TOC sediment, suggesting that a part of the nitrate was reduced by mixotrophic nitrate-reducing Fe(II)-oxidizers and chemoorganoheterotrophic nitrate-reducers. Our results demonstrate that dynamic microbial Fe cycling occurs in these sediments and that the extent of Fe cycling is dependent on organic carbon content.
Nitrate-reducing Fe(II)-oxidizing microorganisms were described for the first time ca. 20 years ago. Most pure cultures of nitrate-reducing Fe(II) oxidizers can oxidize Fe(II) only under mixotrophic conditions, i.e., when an organic cosubstrate is provided. A small number of nitrate-reducing Fe(II)-oxidizing cultures have been proposed to grow autotrophically, but unambiguous evidence for autotrophy has not always been provided. Thus, it is still unclear whether or to what extent Fe(II) oxidation coupled to nitrate reduction is an enzymatically catalyzed and energy-yielding autotrophic process or whether Fe(II) is abiotically oxidized by nitrite from heterotrophic nitrate reduction. The aim of the present study was to find evidence for the existence of autotrophic nitrate-reducing Fe(II) oxidizers in coastal marine sediments. Microcosm incubations showed that with increasing incubation times, the stoichiometric ratio of reduced nitrate/oxidized Fe(II) [NO3−reduced/Fe(II)oxidized] decreased, indicating a decreasing contribution of heterotrophic denitrification and/or an increasing contribution of autotrophic nitrate-reducing Fe(II) oxidation over time. After incubations of sediment slurries for >10 weeks, nitrate-reducing activity ceased, although nitrate was still present. This suggests that heterotrophic nitrate reduction had ceased due to the depletion of readily available organic carbon. However, after the addition of Fe(II) to these batch incubation mixtures, the nitrate-reducing activity resumed, and Fe(II) was oxidized, indicating the activity of autotrophic nitrate-reducing Fe(II) oxidizers. The concurrent reduction of 14C-labeled bicarbonate concentrations unambiguously proved that autotrophic C fixation occurred during Fe(II) oxidation and nitrate reduction. Our results clearly demonstrated that autotrophic nitrate-reducing Fe(II)-oxidizing bacteria were present in the investigated coastal marine sediments. IMPORTANCE Twenty years after the discovery of nitrate-reducing Fe(II) oxidizers, it is still controversially discussed whether autotrophic nitrate-reducing Fe(II)-oxidizing microorganisms exist and to what extent Fe(II) oxidation in this reduction/oxidation process is enzymatically catalyzed or which role abiotic side reactions of Fe(II) with reactive N species play. Most pure cultures of nitrate-reducing Fe(II) oxidizers are mixotrophic; i.e., they need an organic cosubstrate to maintain their activity over several cultural transfers. For the few existing autotrophic isolates and enrichment cultures, either the mechanism of nitrate-reducing Fe(II) oxidation is not known or evidence for their autotrophic lifestyle is controversial. In the present study, we provide evidence for the existence of autotrophic nitrate-reducing Fe(II) oxidizers in coastal marine sediments. The evidence is based on stoichiometries of nitrate reduction and Fe(II) oxidation determined in microcosm incubations and the incorporation of carbon from CO2 under conditions that favor the activity of nitrate-reducing Fe(II) o...
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