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Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the southern mariana trough.

ABSTRACT: Microbial community structures in deep-sea hydrothermal vents fields are constrained by available energy yields provided by inorganic redox reactions, which are in turn controlled by chemical composition of hydrothermal fluids. In the past two decades, geochemical and microbiological studies have been conducted in deep-sea hydrothermal vents at three geographically different areas of the Southern Mariana Trough (SMT). A variety of geochemical data of hydrothermal fluids and an unparalleled microbiological dataset of various samples (i.e., sulfide structures of active vents, iron-rich mats, borehole fluids, and ambient seawater) are available for comparative analyses. Here, we summarize the geochemical and microbiological characteristics in the SMT and assess the relationship between the microbial community structures and the fluid geochemistry in the SMT by thermodynamic modeling. In the high temperature vent fluids, aerobic sulfide-oxidation has the potential to yield large amounts of bioavailable energy in the vent fluids, which is consistent with the detection of species related to sulfide-oxidizing bacteria (such as Thiomicrospira in the Gammaproteobacteria and Sulfurimonas in the Epsilonproteobacteria). Conversely, the bioavailable energy yield from aerobic iron-oxidation reactions in the low-temperature fluids collected from man-made boreholes and several natural vents were comparable to or higher than those from sulfide-oxidation. This is also consistent with the detection of species related to iron-oxidizing bacteria (Mariprofundus in the Zetaproteobacteria) in such low-temperature samples. The results of combination of microbiological, geochemical, and thermodynamic analyses in the SMT provide novel insights into the presence and significance of iron-based microbial ecosystems in deep-sea hydrothermal fields.

SUBMITTER: Kato S

PROVIDER: S-EPMC3304087 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the southern mariana trough.

Kato Shingo S Nakamura Kentaro K Toki Tomohiro T Ishibashi Jun-Ichiro J Tsunogai Urumu U Hirota Akinori A Ohkuma Moriya M Yamagishi Akihiko A

Frontiers in microbiology 20120315

Microbial community structures in deep-sea hydrothermal vents fields are constrained by available energy yields provided by inorganic redox reactions, which are in turn controlled by chemical composition of hydrothermal fluids. In the past two decades, geochemical and microbiological studies have been conducted in deep-sea hydrothermal vents at three geographically different areas of the Southern Mariana Trough (SMT). A variety of geochemical data of hydrothermal fluids and an unparalleled micro ...[more]

PMID: 22435065

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Project description:The abundance, diversity, activity, and composition of microbial communities in sulfide structures both of active and inactive vents were investigated by culture-independent methods. These sulfide structures were collected at four hydrothermal fields, both on- and off-axis of the back-arc spreading center of the Southern Mariana Trough. The microbial abundance and activity in the samples were determined by analyzing total organic content, enzymatic activity, and copy number of the 16S rRNA gene. To assess the diversity and composition of the microbial communities, 16S rRNA gene clone libraries including bacterial and archaeal phylotypes were constructed from the sulfide structures. Despite the differences in the geological settings among the sampling points, phylotypes related to the Epsilonproteobacteria and cultured hyperthermophilic archaea were abundant in the libraries from the samples of active vents. In contrast, the relative abundance of these phylotypes was extremely low in the libraries from the samples of inactive vents. These results suggest that the composition of microbial communities within sulfide structures dramatically changes depending on the degree of hydrothermal activity, which was supported by statistical analyses. Comparative analyses suggest that the abundance, activity and diversity of microbial communities within sulfide structures of inactive vents are likely to be comparable to or higher than those in active vent structures, even though the microbial community composition is different between these two types of vents. The microbial community compositions in the sulfide structures of inactive vents were similar to those in seafloor basaltic rocks rather than those in marine sediments or the sulfide structures of active vents, suggesting that the microbial community compositions on the seafloor may be constrained by the available energy sources. Our findings provide helpful information for understanding the biogeography, biodiversity and microbial ecosystems in marine environments.

Project description:When its hydrothermal supply ceases, hydrothermal sulfide chimneys become inactive and commonly experience oxidative weathering on the seafloor. However, little is known about the oxidative weathering of inactive sulfide chimneys, nor about associated microbial community structures and their succession during this weathering process. In this work, an inactive sulfide chimney and a young chimney in the early sulfate stage of formation were collected from the Main Endeavor Field of the Juan de Fuca Ridge. To assess oxidative weathering, the ultrastructures of secondary alteration products accumulating on the chimney surface were examined and the presence of possible Fe-oxidizing bacteria (FeOB) was investigated. The results of ultrastructure observation revealed that FeOB-associated ultrastructures with indicative morphologies were abundantly present. Iron oxidizers primarily consisted of members closely related to Gallionella spp. and Mariprofundus spp., indicating Fe-oxidizing species likely promote the oxidative weathering of inactive sulfide chimneys. Abiotic accumulation of Fe-rich substances further indicates that oxidative weathering is a complex, dynamic process, alternately controlled by FeOB and by abiotic oxidization. Although hydrothermal fluid flow had ceased, inactive chimneys still accommodate an abundant and diverse microbiome whose microbial composition and metabolic potential dramatically differ from their counterparts at active vents. Bacterial lineages within current inactive chimney are dominated by members of α-, δ-, and γ-Proteobacteria and they are deduced to be closely involved in a diverse set of geochemical processes including iron oxidation, nitrogen fixation, ammonia oxidation and denitrification. At last, by examining microbial communities within hydrothermal chimneys at different formation stages, a general microbial community succession can be deduced from early formation stages of a sulfate chimney to actively mature sulfide structures, and then to the final inactive altered sulfide chimney. Our findings provide valuable insights into the microbe-involved oxidative weathering process and into microbial succession occurring at inactive hydrothermal sulfide chimney after high-temperature hydrothermal fluids have ceased venting.

Project description:Foraminifera are single-celled eukaryotes (protists) of large ecological importance, as well as environmental and paleoenvironmental indicators and biostratigraphic tools. In addition, they are capable of surviving in anoxic marine environments where they represent a major component of the benthic community. However, the cellular adaptations of Foraminifera to the anoxic environment remain poorly constrained. We sampled an oxic-anoxic transition zone in marine sediments from the Namibian shelf, where the genera Bolivina and Stainforthia dominated the Foraminifera community, and use metatranscriptomics to characterize Foraminifera metabolism across the different geochemical conditions. Relative Foraminifera gene expression in anoxic sediment increased an order of magnitude, which was confirmed in a 10-day incubation experiment where the development of anoxia coincided with a 20-40-fold increase in the relative abundance of Foraminifera protein encoding transcripts, attributed primarily to those involved in protein synthesis, intracellular protein trafficking, and modification of the cytoskeleton. This indicated that many Foraminifera were not only surviving but thriving, under the anoxic conditions. The anaerobic energy metabolism of these active Foraminifera was characterized by fermentation of sugars and amino acids, fumarate reduction, and potentially dissimilatory nitrate reduction. Moreover, the gene expression data indicate that under anoxia Foraminifera use the phosphogen creatine phosphate as an ATP store, allowing reserves of high-energy phosphate pool to be maintained for sudden demands of increased energy during anaerobic metabolism. This was co-expressed alongside genes involved in phagocytosis and clathrin-mediated endocytosis (CME). Foraminifera may use CME to utilize dissolved organic matter as a carbon and energy source, in addition to ingestion of prey cells via phagocytosis. These anaerobic metabolic mechanisms help to explain the ecological success of Foraminifera documented in the fossil record since the Cambrian period more than 500 million years ago.

Dataset Information

Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the southern mariana trough.

Publications

Iron-based microbial ecosystem on and below the seafloor: a case study of hydrothermal fields of the southern mariana trough.

Similar Datasets

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