Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov.

Makita, Hiroko; Tanaka, Emiko; Mitsunobu, Satoshi; Miyazaki, Masaru; Nunoura, Takuro; Uematsu, Katsuyuki; Takaki, Yoshihiro; Nishi, Shinro; Shimamura, Shigeru; Takai, Ken

doi:10.1007/s00203-016-1307-4

Cited by 49 publications

(33 citation statements)

References 44 publications

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“…By 16S rRNA gene identity and %AAI, the CP strains are most closely related to Mariprofundus sp. DIS-1, isolated from a steel coupon incubated in a coastal bay (Mumford et al, 2016), and M. micogutta , isolated from marine hydrothermal sediment ( Table 2 and Figure 3 ; Makita et al, 2016). These close relationships show that Mariprofundus is a cosmopolitan genus that inhabits a variety of environments, coastal and deep sea, as well as planktonic, benthic, and subsurface.…”

Section: Resultsmentioning

confidence: 99%

“…The other Zetaproteobacteria isolated to date primarily originate from deep sea hydrothermal microbial mats and sediments (Emerson et al, 2007; McAllister et al, 2011; Field et al, 2015; Makita et al, 2016), with some from coastal sediment (Laufer et al, 2016, 2017). Zetaproteobacteria sequences have also been found in coastal groundwater and worm burrows (16S rRNA gene analysis; McAllister et al, 2015) and briny terrestrial groundwater (metagenomics; Emerson et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic–Anoxic Transition Zone

et al. 2017

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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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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic–Anoxic Transition Zone

et al. 2017

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“…Phylogeny of the Zetaproteobacteria, rooted with Alphaproteobacteria, built with concatenated ribosomal protein sequences. Data from (80), (85), (105), and other draft genomes available on Genbank. All nodes recovered TBE support values greater than 0.7.…”

Section: Resultsmentioning

confidence: 99%

Geochemical and metagenomic characterization of Jinata Onsen, a Proterozoic-analog hot spring, reveals novel microbial diversity including iron-tolerant phototrophs and thermophilic lithotrophs

Ward

Idei

Nakagawa

et al. 2018

Preprint

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Hydrothermal systems, including terrestrial hot springs, contain diverse geochemical conditions that vary over short spatial scales due to progressive interaction between the reducing hydrothermal fluids, the oxygenated atmosphere, and in some cases seawater. At Jinata Onsen, on Shikinejima Island, Japan, an intertidal, anoxic, iron-rich hot spring mixes with the oxygenated atmosphere and seawater over short spatial scales, creating a diversity of chemical potentials and redox pairs over a distance ~10 m. We characterized the geochemical conditions along the outflow of Jinata Onsen as well as the microbial communities present in biofilms, mats, and mineral crusts along its traverse via 16S rDNA amplicon and genome-resolved shotgun metagenomic sequencing. The microbial community changed significantly downstream as temperatures and dissolved iron concentrations decreased and dissolved oxygen increased. Near the spring source, biomass is limited relative to downstream, and primary productivity may be fueled by oxidation of ferrous iron and molecular hydrogen by members of the Zetaproteobacteria and Aquificae. Downstream, the microbial community is dominated by oxygenic Cyanobacteria. Cyanobacteria are abundant and active even at ferrous iron concentrations of ~150 μM, which challenges the idea that iron toxicity limited cyanobacterial expansion in Precambrian oceans. Several novel lineages of Bacteria are also present at Jinata Onsen, including previously uncharacterized members of the Chloroflexi and Caldithrichaeota phyla, positioning Jinata Onsen as a valuable site for future characterization of these clades.ImportanceHigh temperatures and reducing conditions allow hot springs to support microbial communities that are very different from those found elsewhere on the surface of the Earth today; in some ways, these environments and the communities they support can be similar to environments that existed on the early Earth and that may exist on other planets. Here, we describe a novel hot spring system where hot, iron-rich but oxygen-poor water flows into the ocean, supporting a range of unique microbial communities. Metagenomic sequencing recovered many novel microbial lineages, including deep-branching and uniquely thermotolerant members of known groups. Comparison of the biological communities in the upstream part of the hot spring, potentially supported by biological iron and hydrogen oxidizing metabolisms, to downstream microbial mats, supported by oxygenic photosynthesis, provides insight into the potential productivity of life during Proterozoic time and on other planets where oxygenic photosynthesis is not possible.

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“…Mariprofundus is the sole member of the class Zetaproteobacteria in the phylum Proteobacteria . Several cultured members (JV-1, PV-1) of Fe-oxidizing Mariprofundus were isolated from deep-sea hydrothermal fields (Singer et al, 2011; Makita et al, 2017). The genus of Mariprofundus were observed as only abundant FeOM group (relative abundance over 1%) in the chimney samples JL90, JL94D, and JL94H, except in JL95 with 0.705 (Table 3), indicating that Fe-oxidizing bacteria within Mariprofundus were common at the Longqi field and probably played a major role in Fe oxidation.…”

Section: Discussionmentioning

confidence: 99%

Microbial Community Structure of Deep-sea Hydrothermal Vents on the Ultraslow Spreading Southwest Indian Ridge

et al. 2017

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Southwest Indian Ridge (SWIR) is a typical oceanic ultraslow spreading ridge with intensive hydrothermal activities. The microbial communities in hydrothermal fields including primary producers to support the entire ecosystem by utilizing geochemical energy generated from rock-seawater interactions. Here we have examined the microbial community structures on four hydrothermal vents from SWIR, representing distinct characteristics in terms of temperature, pH and metal compositions, by using Illumina sequencing of the 16S small subunit ribosomal RNA (rRNA) genes, to correlate bacterial and archaeal populations with the nature of the vents influenced by ultraslow spreading features. Epsilon-, Gamma-, Alpha-, and Deltaproteobacteria and members of the phylum Bacteroidetes and Planctomycetes, as well as Thaumarchaeota, Woesearchaeota, and Euryarchaeota were dominant in all the samples. Both bacterial and archaeal community structures showed distinguished patterns compared to those in the fast-spreading East Pacific Ridge or the slow-spreading Mid-Atlantic Ridge as previously reported. Furthermore, within SWIR, the microbial communities are highly correlated with the local temperatures. For example, the sulfur-oxidizing bacteria were dominant within bacteria from low-temperature vents, but were not represented as the dominating group recovered from high temperature (over 300°C) venting chimneys in SWIR. Meanwhile, Thaumarchaeota, the ammonium oxidizing archaea, only showed high relative abundance of amplicons in the vents with high-temperature in SWIR. These findings provide insights on the microbial community in ultraslow spreading hydrothermal fields, and therefore assist us in the understanding of geochemical cycling therein.

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Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov.

Cited by 49 publications

References 44 publications

Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic–Anoxic Transition Zone

Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic–Anoxic Transition Zone

Geochemical and metagenomic characterization of Jinata Onsen, a Proterozoic-analog hot spring, reveals novel microbial diversity including iron-tolerant phototrophs and thermophilic lithotrophs

Microbial Community Structure of Deep-sea Hydrothermal Vents on the Ultraslow Spreading Southwest Indian Ridge

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