Genomic insights into the uncultivated marine Zetaproteobacteria at Loihi Seamount

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

Section: Coexistence Of Different Physiological Types Of Fe(ii) Oxidimentioning

confidence: 99%

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

Laufer

Nordhoff

Røy

et al. 2016

“…Type I RubisCO is less O 2 sensitive and has a higher affinity for CO 2 than type II (42). Most of the other zetaproteobacterial genomes only have type II RubisCO (37).…”

Section: Discussionmentioning

confidence: 99%

“…It has previously been noted that among oxygen-dependent FeOB there is a lack of the most well-recognized genes involved in defense against ROS (37,43). For example, to date, the gene for catalase, the most commonly occurring enzyme that breaks down hydrogen peroxide (H 2 O 2 ) (44), has not been found in the genomes of any of the cultured zetaproteobacteria.…”

Section: Discussionmentioning

confidence: 99%

“…The cell pellet was extracted using a MoBio PowerSoil DNA extraction kit, and approximately 1 g of DNA was recovered. Preparation of DNA for sequencing was done as described by Field et al (37), and the sequencing of 150-by 2-bp paired-end reads was done on an Illumina Nextgen instrument at the Single Cell Genomic Center at Bigelow Laboratory. The assembled sequence had 57 contigs with an N50 of 101 kb.…”

Section: Methodsmentioning

confidence: 99%

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Peeking under the Iron Curtain: Development of a Microcosm for Imaging the Colonization of Steel Surfaces by Mariprofundus sp. Strain DIS-1, an Oxygen-Tolerant Fe-Oxidizing Bacterium

Mumford

Adaktylou

Emerson

2016

Self Cite

Microbially influenced corrosion (MIC) is a major cause of damage to steel infrastructure in the marine environment. Despite their ability to grow directly on Fe(II) released from steel, comparatively little is known about the role played by neutrophilic iron-oxidizing bacteria (FeOB). Recent work has shown that FeOB grow readily on mild steel (1018 MS) incubated in situ or as a substrate for pure cultures in vitro; however, details of how they colonize steel surfaces are unknown yet are important for understanding their effects. In this study, we combine a novel continuously upwelling microcosm with confocal laser scanning microscopy (CLSM) to determine the degree of colonization of 1018 MS by the marine FeOB strain DIS-1. 1018 MS coupons were incubated with sterile seawater (pH 8) inoculated with strain DIS-1. Incubations were performed both under oxic conditions and in an anoxic-to-oxic gradient. Following incubations of 1 to 10 days, the slides were removed from the microcosms and stained to visualize both cells and stalk structures. Stained coupons were visualized by CLSM after being mounted in a custom frame to preserve the three-dimensional structure of the biofilm. The incubation of 1018 MS coupons with strain DIS-1 under oxic conditions resulted in initial attachment of cells within 2 days and nearly total coverage of the coupon with an ochre film within 5 days. CLSM imaging revealed a nonadherent biofilm composed primarily of the Fe-oxide stalks characteristic of strain DIS-1. When incubated with elevated concentrations of Fe(II), DIS-1 colonization of 1018 MS was inhibited. IMPORTANCEThese experiments describe the growth of a marine FeOB in a continuous culture system and represent direct visualizations of steel colonization by FeOB. We anticipate that these experiments will lay the groundwork for studying the mechanisms by which FeOB colonize steel and help to elucidate the role played by marine FeOB in MIC. These observations of the interaction between an FeOB, strain DIS-1, and steel suggest that this experimental system will provide a useful model for studying the interactions between microbes and solid substrates. Microbially influenced corrosion (MIC) is a major contributor to the degradation of structural steel in the marine environment, and the resultant damages are estimated to be in the billions of dollars per year (1). Recent studies have demonstrated that microbial activity can result in corrosion rates up to 3-fold higher than would otherwise be expected (2, 3). An especially pervasive form of marine corrosion is accelerated low-water corrosion (ALWC), which occurs close to the tidal low water mark on permanent structures like piers and bridges (2). Microbial involvement is known to be a factor in ALWC. The result of these processes is the need for more frequent maintenance of structures, such as piers, bridges, and pipelines, as well as an increased risk of catastrophic failure. The majority of the existing literature suggests that MIC is primarily a result of surface colonizatio...

“…The obtained reads were quality-trimmed, digitally normalized, and assembled in SPAdes v2.2.1 according to the method of Bankevich et al (10), as described by Wilkins et al (11). Potential contaminant contigs were removed after tetramer frequency evaluation, and principal component analysis (PCA) identified outliers (12), as well as BLAST comparisons to the NCBI nr database and between samples sequenced together, as described in further detail by Field et al (13). Genome size estimates were calculated using both arCOG (14) and CheckM (15) analysis.…”

mentioning

confidence: 99%

Nanoarchaeota, Their Sulfolobales Host, and Nanoarchaeota Virus Distribution across Yellowstone National Park Hot Springs

Munson-McGee

Field

Bateson

et al. 2015

Self Cite

e Nanoarchaeota are obligate symbionts with reduced genomes first described from marine thermal vent environments. Here, both community metagenomics and single-cell analysis revealed the presence of Nanoarchaeota in high-temperature (ϳ90°C), acidic (pH Ϸ 2.5 to 3.0) hot springs in Yellowstone National Park (YNP) (United States). Single-cell genome analysis of two cells resulted in two nearly identical genomes, with an estimated full length of 650 kbp. Genome comparison showed that these two cells are more closely related to the recently proposed Nanobsidianus stetteri from a more neutral YNP hot spring than to the marine Nanoarchaeum equitans. Single-cell and catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) analysis of environmental hot spring samples identified the host of the YNP Nanoarchaeota as a Sulfolobales species known to inhabit the hot springs. Furthermore, we demonstrate that Nanoarchaeota are widespread in acidic to near neutral hot springs in YNP. An integrated viral sequence was also found within one Nanoarchaeota single-cell genome and further analysis of the purified viral fraction from environmental samples indicates that this is likely a virus replicating within the YNP Nanoarchaeota.