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

Abstract

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

The role of microaerophilic Fe‐oxidizing micro‐organisms in producing banded iron formations

“…With a few exceptions (e.g., Melton et al, 2012;Laufer et al, 2015), studies typically focus on one type of FeOM or rely on 16S rRNA phylogeny, which may not reveal metabolism. With a few exceptions (e.g., Melton et al, 2012;Laufer et al, 2015), studies typically focus on one type of FeOM or rely on 16S rRNA phylogeny, which may not reveal metabolism.…”

Microaerophilic Fe(II)-Oxidizing Zetaproteobacteria Isolated from Low-Fe Marine Coastal Sediments: Physiology and Composition of Their Twisted Stalks

“…Microaerophilic Fe(II) oxidizers were isolated and cultivated in zero-valent iron (ZVI) plates with artificial seawater (ASW) medium and CO 2 as a carbon source, as described by Laufer et al (25). Briefly, ZVI plates are petri dishes containing ZVI powder and ASW, incubated under microoxic conditions (O 2 ϭ 6 to 10% of atmospheric O 2 ), that are created with gas packs (BD GasPak EZ Campy; Becton, Dickinson and Co., NJ) inside anoxic jars (Merck, Darmstadt, Germany).…”

“…Furthermore, Fe mats formed by microaerophilic Fe(II)-oxidizing bacteria found on continental margin sediments (12) may impact the transition of organic compounds and transition metals from the water column into the sediment. Since Zetaproteobacteria are only present at low numbers (25) in the sediments in Aarhus Bay, the formation of dense mats of twisted stalks seems unlikely, and therefore, an effect of stalks formed by these bacteria on Ni 2ϩ availability is probably restricted to microniches. However, considering the wide distribution of Zetaproteobacteria (17,21,22,25,50), their impact on trace metal availability might be higher in other marine habitats.…”

“…Since Zetaproteobacteria are only present at low numbers (25) in the sediments in Aarhus Bay, the formation of dense mats of twisted stalks seems unlikely, and therefore, an effect of stalks formed by these bacteria on Ni 2ϩ availability is probably restricted to microniches. However, considering the wide distribution of Zetaproteobacteria (17,21,22,25,50), their impact on trace metal availability might be higher in other marine habitats. In ancient ocean environments, Fe(II) was abundant, oxygen was present at microoxic concentrations, and nickel concentrations were much higher (65-67) than in modern marine habitats (ϳ9 nM [68]).…”

“…In a previous study, it was shown that Fe(III)-reducing bacteria are present and coexist with microaerophilic Fe(II) oxidizers within the same layers in sediment from Norsminde Fjord and Kalø Vig (25). As shown by Roden and coworkers (59) using cocultures of a lithoautotrophic microaerophilic Fe(II) oxidizer and an anaerobic dissimilatory Fe(III) reducer, grown in a column system that provided an oxygen gradient, there is the potential for microscale Fe cycling in such stratified systems.…”