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First evidence for the presence of iron oxidizing zetaproteobacteria at the Levantine continental margins.

ABSTRACT: During the 2010-2011 E/V Nautilus exploration of the Levantine basin's sediments at the depth of 300-1300 m, densely patched orange-yellow flocculent mats were observed at various locations along the continental margin of Israel. Cores from the mat and the control locations were collected by remotely operated vehicle system (ROV) operated by the E/V Nautilus team. Microscopic observation and phylogenetic analysis of microbial 16S and 23S rRNA gene sequences indicated the presence of zetaproteobacterial stalk forming Mariprofundus spp.-like prokaryotes in the mats. Bacterial tag-encoded FLX amplicon pyrosequencing determined that zetaproteobacterial populations were a dominant fraction of microbial community in the biofilm. We show for the first time that zetaproteobacterial may thrive at the continental margins, regardless of crustal iron supply, indicating significant fluxes of ferrous iron to the sediment-water interface. In light of this discovery, we discuss the potential bioavailability of sediment-water interface iron for organisms in the overlying water column.

SUBMITTER: Rubin-Blum M

PROVIDER: S-EPMC3948872 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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First evidence for the presence of iron oxidizing zetaproteobacteria at the Levantine continental margins.

Rubin-Blum Maxim M Antler Gilad G Tsadok Rami R Shemesh Eli E Austin James A JA Coleman Dwight F DF Goodman-Tchernov Beverly N BN Ben-Avraham Zvi Z Tchernov Dan D

PloS one 20140310 3

During the 2010-2011 E/V Nautilus exploration of the Levantine basin's sediments at the depth of 300-1300 m, densely patched orange-yellow flocculent mats were observed at various locations along the continental margin of Israel. Cores from the mat and the control locations were collected by remotely operated vehicle system (ROV) operated by the E/V Nautilus team. Microscopic observation and phylogenetic analysis of microbial 16S and 23S rRNA gene sequences indicated the presence of zetaproteoba ...[more]

PMID: 24614177

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Project description:Chemolithoautotrophic iron-oxidizing bacteria play an essential role in the global iron cycle. Thus far, the majority of marine iron-oxidizing bacteria have been identified as Zetaproteobacteria, a novel class within the phylum Proteobacteria. Marine iron-oxidizing microbial communities have been found associated with volcanically active seamounts, crustal spreading centers, and coastal waters. However, little is known about the presence and diversity of iron-oxidizing communities at hydrothermal systems along the slow crustal spreading center of the Mid-Atlantic Ridge. From October to November 2012, samples were collected from rust-colored mats at three well-known hydrothermal vent systems on the Mid-Atlantic Ridge (Rainbow, Trans-Atlantic Geotraverse, and Snake Pit) using the ROV Jason II. The goal of these efforts was to determine if iron-oxidizing Zetaproteobacteria were present at sites proximal to black smoker vent fields. Small, diffuse flow venting areas with high iron(II) concentrations and rust-colored microbial mats were observed at all three sites proximal to black smoker chimneys. A novel, syringe-based precision sampler was used to collect discrete microbial iron mat samples at the three sites. The presence of Zetaproteobacteria was confirmed using a combination of 16S rRNA pyrosequencing and single-cell sorting, while light micros-copy revealed a variety of iron-oxyhydroxide structures, indicating that active iron-oxidizing communities exist along the Mid-Atlantic Ridge. Sequencing analysis suggests that these iron mats contain cosmopolitan representatives of Zetaproteobacteria, but also exhibit diversity that may be uncommon at other iron-rich marine sites studied to date. A meta-analysis of publically available data encompassing a variety of aquatic habitats indicates that Zetaproteobacteria are rare if an iron source is not readily available. This work adds to the growing understanding of Zetaproteobacteria ecology and suggests that this organism is likely locally restricted to iron-rich marine environments but may exhibit wide-scale geographic distribution, further underscoring the importance of Zetaproteobacteria in global iron cycling.

Project description:Chemolithotrophic iron-oxidizing bacteria (FeOB) could theoretically inhabit any environment where Fe(II) and O2 (or nitrate) coexist. Until recently, marine Fe-oxidizing Zetaproteobacteria had primarily been observed in benthic and subsurface settings, but not redox-stratified water columns. This may be due to the challenges that a pelagic lifestyle would pose for Zetaproteobacteria, given low Fe(II) concentrations in modern marine waters and the possibility that Fe oxyhydroxide biominerals could cause cells to sink. However, we recently cultivated Zetaproteobacteria from the Chesapeake Bay oxic-anoxic transition zone, suggesting that they can survive and contribute to biogeochemical cycling in a stratified estuary. Here we describe the isolation, characterization, and genomes of two new species, Mariprofundus aestuarium CP-5 and Mariprofundus ferrinatatus CP-8, which are the first Zetaproteobacteria isolates from a pelagic environment. We looked for adaptations enabling strains CP-5 and CP-8 to overcome the challenges of living in a low Fe redoxcline with frequent O2 fluctuations due to tidal mixing. We found that the CP strains produce distinctive dreadlock-like Fe oxyhydroxide structures that are easily shed, which would help cells maintain suspension in the water column. These oxides are by-products of Fe(II) oxidation, likely catalyzed by the putative Fe(II) oxidase encoded by the cyc2 gene, present in both CP-5 and CP-8 genomes; the consistent presence of cyc2 in all microaerophilic FeOB and other FeOB genomes supports its putative role in Fe(II) oxidation. The CP strains also have two gene clusters associated with biofilm formation (Wsp system and the Widespread Colonization Island) that are absent or rare in other Zetaproteobacteria. We propose that biofilm formation enables the CP strains to attach to FeS particles and form flocs, an advantageous strategy for scavenging Fe(II) and developing low [O2] microenvironments within more oxygenated waters. However, the CP strains appear to be adapted to somewhat higher concentrations of O2, as indicated by the presence of genes encoding aa3-type cytochrome c oxidases, but not the cbb3-type found in all other Zetaproteobacteria isolate genomes. Overall, our results reveal adaptations for life in a physically dynamic, low Fe(II) water column, suggesting that niche-specific strategies can enable Zetaproteobacteria to live in any environment with Fe(II).

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Dataset Information

First evidence for the presence of iron oxidizing zetaproteobacteria at the Levantine continental margins.

Publications

First evidence for the presence of iron oxidizing zetaproteobacteria at the Levantine continental margins.

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