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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 (Kalo 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), O-2, 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.

Iron is the most abundant redox-active metal in the Earth's crust. The one electron transfer between the two most common redox states, Fe(II) and Fe(III), plays a role in a huge range of environmental processes from mineral formation and dissolution to contaminant remediation and global biogeochemical cycling. It has been appreciated for more than a century that microorganisms can harness the energy of this Fe redox transformation for their metabolic benefit. However, this is most widely understood for anaerobic Fe(III)-reducing or aerobic and microaerophilic Fe(II)-oxidizing bacteria. Only in the past few decades have we come to appreciate that bacteria also play a role in the anaerobic oxidation of ferrous iron, Fe(II), and thus can act to form Fe(III) minerals in anoxic settings. Since this discovery, our understanding of the ecology of these organisms, their mechanisms of Fe(II) oxidation and their role in environmental processes has been increasing rapidly. In this article, we bring these new discoveries together to review the current knowledge on these environmentally important bacteria, and reveal knowledge gaps for future research.

The iron (Fe) isotopic composition of Precambrian iron formations (IFs), besides providing geological context through its mineralogical properties, was suggested to function as a biosignature that can be used to infer a potential microbial role in the formation of the deposited Fe minerals. Anoxygenic phototrophic Fe(II)-oxidizing bacteria (photoferrotrophs), capable of oxidizing Fe(II) anoxically using light energy, were potentially involved in Fe(II) oxidation in anoxic or suboxic Precambrian oceans. The effect of Si on Fe isotopic fractionation between aqueous Fe(II) and Fe-Si-co-precipitates has been investigated before. However, it is currently unknown how stable Fe isotopes are fractionated during enzymatic Fe(II) oxidation under marine hydrogeochemical conditions, and particularly how the presence of Si affects the Fe isotope composition and the isotopic exchange among different Fe phases. We therefore studied Fe isotope fractionation during Fe(II) oxidation by the marine photo-ferrotroph Rhodovulum iodosum in simulated Precambrian seawater amended with 1 mMdissolved Si. Our results show that the change in the Fe isotope compositions over time for both the initial aqueous Fe(II) (Fe-aq) and the Fe(III) precipitates (Fe-ppt) follow a Rayleigh distillation model. Moreover, the fractionation (delta(56) Feppt-aq) determined independently from either d56 Feaq or delta(56) Fe-ppt data resulted in a value of 2.3 perpendicular to 0.3 (2SD, N = 6). This value differs from the fractionation factor determined previously for Fe(II) oxidation by R. iodosum in the absence of Si, where the fractionation calculated from delta(56) Fe-aq (i.e. 0.96-1.18) was different from that calculated from delta(56) Fe-ppt (1.96-1.98). This difference was attributed to isotopic exchange processes with soluble and sorbed Fe species. The present study suggests that Si present in Precambrian oceans retards Fe isotopic exchange, likely through combined effects of complexation of dissolved Fe species by Si and sorption of Si to Fe(III) minerals, thus lowering sorption of Fe(II) to the Fe(III) minerals, which is necessary for isotopic exchange. In summary our data suggests that Si in ancient oceans played a key role for the Fe isotope composition of Fe(III) minerals that were deposited by photoferrotrophic iron oxidation in Precambrian oceans by minimizing subsequent isotope exchange and recrystallization processes with aqueous Fe(II). (C) 2017 Elsevier Ltd. All rights reserved.

Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic and depend on organic cosubstrates for growth. Encrustation of cells in Fe(III) minerals has been observed for mixotrophic NRFeOB but not for autotrophic phototrophic and microaerophilic Fe(II) oxidizers. So far, little is known about cell-mineral associations in the few existing autotrophic NRFeOB. Here, we investigate whether the designated autotrophic Fe(II)-oxidizing strain (closely related to Gallionella and Sideroxydans ) or the heterotrophic nitrate reducers that are present in the autotrophic nitrate-reducing Fe(II)-oxidizing enrichment culture KS form mineral crusts during Fe(II) oxidation under autotrophic and mixotrophic conditions. In the mixed culture, we found no significant encrustation of any of the cells both during autotrophic oxidation of 8 to 10 mM Fe(II) coupled to nitrate reduction and during cultivation under mixotrophic conditions with 8 to 10 mM Fe(II), 5 mM acetate, and 4 mM nitrate, where higher numbers of heterotrophic nitrate reducers were present. Two pure cultures of heterotrophic nitrate reducers ( Nocardioides and Rhodanobacter ) isolated from culture KS were analyzed under mixotrophic growth conditions. We found green rust formation, no cell encrustation, and only a few mineral particles on some cell surfaces with 5 mM Fe(II) and some encrustation with 10 mM Fe(II). Our findings suggest that enzymatic, autotrophic Fe(II) oxidation coupled to nitrate reduction forms poorly crystalline Fe(III) oxyhydroxides and proceeds without cellular encrustation while indirect Fe(II) oxidation via heterotrophic nitrate-reduction-derived nitrite can lead to green rust as an intermediate mineral and significant cell encrustation. The extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible under environmental conditions in most habitats. IMPORTANCE Most described nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOB) are mixotrophic (their growth depends on organic cosubstrates) and can become encrusted in Fe(III) minerals. Encrustation is expected to be harmful and poses a threat to cells if it also occurs under environmentally relevant conditions. Nitrite produced during heterotrophic denitrification reacts with Fe(II) abiotically and is probably the reason for encrustation in mixotrophic NRFeOB. Little is known about cell-mineral associations in autotrophic NRFeOB such as the enrichment culture KS. Here, we show that no encrustation occurs in culture KS under autotrophic and mixotrophic conditions while heterotrophic nitrate-reducing isolates from culture KS become encrusted. These findings support the hypothesis that encrustation in mixotrophic cultures is caused by the abiotic reaction of Fe(II) with nitrite and provide evidence that Fe(II) oxidation in culture KS is enzymatic. Furthermore, we show that the extent of encrustation caused by indirect Fe(II) oxidation by reactive nitrogen species depends on Fe(II) concentrations and is probably negligible in most environmental habitats.

Anoxygenic photoautotrophic bacteria which use light energy and electrons from Fe(II) for growth, so-called photoferrotrophs, are suggested to have been amongst the first phototrophic microorganisms on Earth and to have contributed to the deposition of sedimentary iron mineral deposits, i.e. banded iron formations. To date only two isolates of marine photoferrotrophic bacteria exist, both of which are closely related purple non-sulfur bacteria. Here we present a novel green-sulfur photoautotrophic Fe(II) oxidizer isolated from a marine coastal sediment, Chlorobium sp. strain N1, which is closely related to the freshwater green-sulfur bacterium Chlorobium luteolum DSM273 that is incapable of Fe(II) oxidation. Besides Fe(II), our isolated strain grew phototrophically with other inorganic and organic substrates such as sulfide, hydrogen, lactate or yeast extract. Highest Fe(II) oxidation rates were measured at pH 7.0-7.3, the temperature optimum was 25 degrees C. Mossbauer spectroscopy identified ferrihydrite as the main Fe(III) mineral and fluorescence and helium-ion microscopy revealed cell-mineral aggregates without obvious cell encrustation. In summary, our study showed that the new isolate is physiologically adapted to the conditions of its natural habitat but also to conditions as proposed for early Earth and is thus a suitable model organism for further studies addressing phototrophic Fe(II) oxidation on early Earth.