Neutrophilic Iron-Oxidizing Bacteria in the Ocean: Their Habitats, Diversity, and Roles in Mineral Deposition, Rock Alteration, and Biomass Production in the Deep-Sea

Edwards, Katrina J.; Bach, Wolfgang; McCollom, T. M.; Rogers, Daniel R.

doi:10.1080/01490450490485863

Cited by 157 publications

(122 citation statements)

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“…Some consistent differences in the membership of dominant organisms were observed between vent fields, chiefly the increased abundance of Alteromonas and Marinobacter populations at Mariner (Sheik et al, 2015; Figure 2). These microbial groups have been shown to be involved in iron uptake (Li et al, 2014b) and iron and manganese oxidation (Edwards et al, 2004;Singer et al, 2011), respectively, and their increased abundance at Mariner correlates with increased iron and manganese concentrations. However, elucidation of abundance of genes associated with iron and manganese oxidation in ELSC plumes was not possible as these genes are highly divergent and are yet to be identified comprehensively and conclusively.…”

Section: Discussionmentioning

confidence: 99%

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

2015

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Microbial processes within deep-sea hydrothermal plumes affect ocean biogeochemistry on global scales. In rising hydrothermal plumes, a combination of microbial metabolism and particle formation processes initiate the transformation of reduced chemicals like hydrogen sulfide, hydrogen, methane, iron, manganese and ammonia that are abundant in hydrothermal vent fluids. Despite the biogeochemical importance of this rising portion of plumes, it is understudied in comparison to neutrally buoyant plumes. Here we use metagenomics and bioenergetic modeling to describe the abundance and genetic potential of microorganisms in relation to available electron donors in five different hydrothermal plumes and three associated background deep-sea waters from the Eastern Lau Spreading Center located in the Western Pacific Ocean. Three hundred and thirty one distinct genomic 'bins' were identified, comprising an estimated 951 genomes of archaea, bacteria, eukarya and viruses. A significant proportion of these genomes is from novel microorganisms and thus reveals insights into the energy metabolism of heretofore unknown microbial groups. Community-wide analyses of genes encoding enzymes that oxidize inorganic energy sources showed that sulfur oxidation was the most abundant and diverse chemolithotrophic microbial metabolism in the community. Genes for sulfur oxidation were commonly present in genomic bins that also contained genes for oxidation of hydrogen and methane, suggesting metabolic versatility in these microbial groups. The relative diversity and abundance of genes encoding hydrogen oxidation was moderate, whereas that of genes for methane and ammonia oxidation was low in comparison to sulfur oxidation. Bioenergetic-thermodynamic modeling supports the metagenomic analyses, showing that oxidation of elemental sulfur with oxygen is the most dominant catabolic reaction in the hydrothermal plumes. We conclude that the energy metabolism of microbial communities inhabiting rising hydrothermal plumes is dictated by the underlying plume chemistry, with a dominant role for sulfur-based chemolithoautotrophy.

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Section: Discussionmentioning

confidence: 99%

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

2015

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“…Taken as a group, the spatial distribution of chemolithotrophs is analogous to their phylogenetic and functional breadth. Chemolithotrophs are essentially ubiquitous, including most terrestrial and aquatic (freshwater and marine) habitats, and notably, the deep sub-surface 6,19,23,24,36,37,52,67,78) . This too provides an indication of the general significance of chemolithotrophy for the dynamics of microbial communities and biogeochemical cycling.…”

Section: A Chemolithotrophs: a Brief Overviewmentioning

confidence: 99%

Chemolithotrohic Bacteria: Distributions, Functions and Significance in Volcanic Environments

King

2007

Microb. Environ.

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A mosaic of environments comprises most volcanic ecosystems. Whether terrestrial or submarine, many of these environments contain large deposits of reduced minerals, or experience large fluxes of reduced substrates, especially sulfur-containing compounds. These systems, which also are typically characterized by temperature and pH extremes, have yielded a rich variety of chemolithotrophic bacteria, and contributed much to our understanding of chemolithotroph ecology and physiology. However, volcanic ecosystems also consist of environments where inorganic and organic substrates are limiting. In these cases, chemolithotrophs may still play important roles by scavenging carbon monoxide, hydrogen or both. These gases can support metabolism of facultative chemolithotrophs, a functional group that includes many nitrogen-fixing bacteria. Facultative chemolithotrophs may not only represent important early colonists on fresh volcanic substrates (e.g., basalts lacking sulfides), they may also contribute significantly to ecosystem succession through nitrogen fixation and interactions with vascular plants. Analyses of CO and hydrogen consumption by recent deposits on Kilauea volcano show that both substrates support significant activity, while molecular approaches show a high diversity of lithotrophs. Collectively, these and other observations indicate that chemolithotrophic metabolism is more widespread than generally acknowledged, and likely to play fundamental roles in shaping ecosystem dynamics.

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“…Fe(II) oxidation in natural environments occurs at the oxic-anoxic interface by chemically reacting with atmospheric O 2 or by aerobic Fe(II)-oxidizing bacteria (Emerson and Revsbech, 1994;Edwards et al, 2004). In the deeper layers of the sediment, Fe(II) oxidation is known to happen in the rhizosphere of plants by root released O 2 (Frenzel et al, 1999;Neubauer et al, 2007;Weiss et al, 2007) or in the sediment by nitrate-dependent Fe(II) oxidation by organisms growing either autotrophically or heterotrophically (Straub et al, 1996;Benz et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Chemolithotrophic nitrate-dependent Fe(II)-oxidizing nature of actinobacterial subdivision lineage TM3

et al. 2013

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Anaerobic nitrate-dependent Fe(II) oxidation is widespread in various environments and is known to be performed by both heterotrophic and autotrophic microorganisms. Although Fe(II) oxidation is predominantly biological under acidic conditions, to date most of the studies on nitrate-dependent Fe(II) oxidation were from environments of circumneutral pH. The present study was conducted in Lake Grosse Fuchskuhle, a moderately acidic ecosystem receiving humic acids from an adjacent bog, with the objective of identifying, characterizing and enumerating the microorganisms responsible for this process. The incubations of sediment under chemolithotrophic nitratedependent Fe(II)-oxidizing conditions have shown the enrichment of TM3 group of uncultured Actinobacteria. A time-course experiment done on these Actinobacteria showed a consumption of Fe(II) and nitrate in accordance with the expected stoichiometry (1:0.2) required for nitratedependent Fe(II) oxidation. Quantifications done by most probable number showed the presence of 1 Â 10 4 autotrophic and 1 Â 10 7 heterotrophic nitrate-dependent Fe(II) oxidizers per gram fresh weight of sediment. The analysis of microbial community by 16S rRNA gene amplicon pyrosequencing showed that these actinobacterial sequences correspond to B0.6% of bacterial 16S rRNA gene sequences. Stable isotope probing using 13 CO 2 was performed with the lake sediment and showed labeling of these Actinobacteria. This indicated that they might be important autotrophs in this environment. Although these Actinobacteria are not dominant members of the sediment microbial community, they could be of functional significance due to their contribution to the regeneration of Fe(III), which has a critical role as an electron acceptor for anaerobic microorganisms mineralizing sediment organic matter. To the best of our knowledge this is the first study to show the autotrophic nitrate-dependent Fe(II)-oxidizing nature of TM3 group of uncultured Actinobacteria.

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Neutrophilic Iron-Oxidizing Bacteria in the Ocean: Their Habitats, Diversity, and Roles in Mineral Deposition, Rock Alteration, and Biomass Production in the Deep-Sea

Cited by 157 publications

References 61 publications

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center

Chemolithotrohic Bacteria: Distributions, Functions and Significance in Volcanic Environments

Chemolithotrophic nitrate-dependent Fe(II)-oxidizing nature of actinobacterial subdivision lineage TM3

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