Metagenomic insights into the dominant Fe(II) oxidizing Zetaproteobacteria from an iron mat at Lo´ihi, Hawai´l.
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ABSTRACT:
SUBMITTER: Singer E
PROVIDER: S-EPMC3603346 | biostudies-literature | 2013
REPOSITORIES: biostudies-literature
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Metagenomic insights into the dominant Fe(II) oxidizing Zetaproteobacteria from an iron mat at Lō´ihi, Hawai´l.
Singer Esther E Heidelberg John F JF Dhillon Ashita A Edwards Katrina J KJ
Frontiers in microbiology 20130319
Zetaproteobacteria are among the most prevalent Fe(II)-oxidizing bacteria (FeOB) at deep-sea hydrothermal vents; however, knowledge about their environmental significance is limited. We provide metagenomic insights into an iron mat at the Lō´ihi Seamount, Hawai´l, revealing novel genomic information of locally dominant Zetaproteobacteria lineages. These lineages were previously estimated to account for ~13% of all local Zetaproteobacteria based on 16S clone library data. Biogeochemically relevan ...[more]
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Project description:The Zetaproteobacteria are a class of bacteria typically associated with marine Fe(II)-oxidizing environments. First discovered in the hydrothermal vents at Loihi Seamount, Hawaii, they have become model organisms for marine microbial Fe(II) oxidation. In addition to deep sea and shallow hydrothermal vents, Zetaproteobacteria are found in coastal sediments, other marine subsurface environments, steel corrosion biofilms and saline terrestrial springs. Isolates from a range of environments all grow by autotrophic Fe(II) oxidation. Their success lies partly in their microaerophily, which enables them to compete with abiotic Fe(II) oxidation at Fe(II)-rich oxic/anoxic transition zones. To determine the known diversity of the Zetaproteobacteria, we have used 16S rRNA gene sequences to define 59 operational taxonomic units (OTUs), at 97% similarity. While some Zetaproteobacteria taxa appear to be cosmopolitan, others are enriched by specific habitats. OTU networks show that certain Zetaproteobacteria co-exist, sharing compatible niches. These niches may correspond with adaptations to O2, H2 and nitrate availability, based on genomic analyses of metabolic potential. Also, a putative Fe(II) oxidation gene has been found in diverse Zetaproteobacteria taxa, suggesting that the Zetaproteobacteria evolved as Fe(II) oxidation specialists. In all, studies suggest that Zetaproteobacteria are widespread, and therefore may have a broad influence on marine and saline terrestrial Fe cycling.
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Project description:The discovery of the novel Zetaproteobacteria class greatly expanded our understanding of neutrophilic, microaerophilic microbial Fe(II) oxidation in marine environments. Despite molecular techniques demonstrating their global distribution, relatively few isolates exist, especially from low-Fe(II) environments. Furthermore, the Fe(II) oxidation pathways used by Zetaproteobacteria remain poorly understood. Here, we present the genomes (>99% genome completeness) of two Zetaproteobacteria, which are the only cultivated isolates originating from typical low-Fe [porewater Fe(II), 70 to 100 μM] coastal marine sediments. The two strains share <90% average nucleotide identity (ANI) with each other and <80% ANI with any other Zetaproteobacteria genome. The closest relatives were Mariprofundus aestuarium strain CP-5 and Mariprofundus ferrinatatus strain CP-8 (96 to 98% 16S rRNA gene sequence similarity). Fe(II) oxidation of strains KV and NF is most likely mediated by the putative Fe(II) oxidase Cyc2. Interestingly, the genome of strain KV also encodes a putative multicopper oxidase, PcoAB, which could play a role in Fe(II) oxidation, a pathway found only in two other Zetaproteobacteria genomes (Ghiorsea bivora TAG-1 and SCGC AB-602-C20). The strains show potential adaptations to fluctuating O2 concentrations, indicated by the presence of both cbb3- and aa3-type cytochrome c oxidases, which are adapted to low and high O2 concentrations, respectively. This is further supported by the presence of several oxidative-stress-related genes. In summary, our results reveal the potential Fe(II) oxidation pathways employed by these two novel chemolithoautotrophic Fe(II)-oxidizing species and the lifestyle adaptations which enable the Zetaproteobacteria to survive in coastal environments with low Fe(II) and regular redox fluctuations.IMPORTANCE Until recently, the importance and relevance of Zetaproteobacteria were mainly thought to be restricted to high-Fe(II) environments, such as deep-sea hydrothermal vents. The two novel Mariprofundus isolates presented here originate from typical low-Fe(II) coastal marine sediments. As well as being low in Fe(II), these environments are often subjected to fluctuating O2 concentrations and regular mixing by wave action and bioturbation. The discovery of two novel isolates highlights the importance of these organisms in such environments, as Fe(II) oxidation has been shown to impact nutrients and trace metals. Genome analysis of these two strains further supported their lifestyle adaptation and therefore their potential preference for coastal marine sediments, as genes necessary for surviving dynamic O2 concentrations and oxidative stress were identified. Furthermore, our analyses also expand our understanding of the poorly understood Fe(II) oxidation pathways used by neutrophilic, microaerophilic Fe(II) oxidizers.
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