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      Microbial metabolisms in an abyssal ferromanganese crust from the Takuyo-Daigo Seamount as revealed by metagenomics

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          Abstract

          Rocky outcrops covered with thick Fe and Mn oxide coatings, which are known as ferromanganese (Fe-Mn) crusts, are commonly found on slopes of aged seamounts in bathyal and abyssal zones. Although the presence of diverse microorganisms on these Fe-Mn crusts has been reported, little is known about their metabolism. Here, we report the metabolic potential of the microbial community in an abyssal crust collected in the Takuyo-Daigo Seamount, in the north-western Pacific. We performed shotgun metagenomic sequencing of the Fe-Mn crust, and detected putative genes involved in dissolution and precipitation of Fe and Mn, nitrification, sulfur oxidation, carbon fixation, and decomposition of organics in the metagenome. In addition, four metagenome-assembled genomes (MAGs) of abundant members in the microbial community were recovered from the metagenome. The MAGs were affiliated with Thaumarchaeota, Alphaproteobacteria, and Gammaproteobacteria, and were distantly related to previously reported genomes/MAGs of cultured and uncultured species. Putative genes involved in the above reactions were also found in the crust MAGs. Our results suggest that crust microbial communities play a role in biogeochemical cycling of C, N, S, Fe, and Mn, and imply that they contribute to the growth of Fe-Mn crusts.

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          Archaea in coastal marine environments.

          E Delong (1992)
          Archaea (archaebacteria) are a phenotypically diverse group of microorganisms that share a common evolutionary history. There are four general phenotypic groups of archaea: the methanogens, the extreme halophiles, the sulfate-reducing archaea, and the extreme thermophiles. In the marine environment, archaeal habitats are generally limited to shallow or deep-sea anaerobic sediments (free-living and endosymbiotic methanogens), hot springs or deep-sea hydrothermal vents (methanogens, sulfate reducers, and extreme thermophiles), and highly saline land-locked seas (halophiles). This report provides evidence for the widespread occurrence of unusual archaea in oxygenated coastal surface waters of North America. Quantitative estimates indicated that up to 2% of the total ribosomal RNA extracted from coastal bacterioplankton assemblages was archaeal. Archaeal small-subunit ribosomal RNA-encoding DNAs (rDNAs) were cloned from mixed bacterioplankton populations collected at geographically distant sampling sites. Phylogenetic and nucleotide signature analyses of these cloned rDNAs revealed the presence of two lineages of archaea, each sharing the diagnostic signatures and structural features previously established for the domain Archaea. Both of these lineages were found in bacterioplankton populations collected off the east and west coasts of North America. The abundance and distribution of these archaea in oxic coastal surface waters suggests that these microorganisms represent undescribed physiological types of archaea, which reside and compete with aerobic, mesophilic eubacteria in marine coastal environments.
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            Age, spreading rates, and spreading asymmetry of the world's ocean crust

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              Archaeal nitrification in the ocean.

              Marine Crenarchaeota are the most abundant single group of prokaryotes in the ocean, but their physiology and role in marine biogeochemical cycles are unknown. Recently, a member of this clade was isolated from a sea aquarium and shown to be capable of nitrification, tentatively suggesting that Crenarchaeota may play a role in the oceanic nitrogen cycle. We enriched a crenarchaeote from North Sea water and showed that its abundance, and not that of bacteria, correlates with ammonium oxidation to nitrite. A time series study in the North Sea revealed that the abundance of the gene encoding for the archaeal ammonia monooxygenase alfa subunit (amoA) is correlated with a decline in ammonium concentrations and with the abundance of Crenarchaeota. Remarkably, the archaeal amoA abundance was 1-2 orders of magnitude higher than those of bacterial nitrifiers, which are commonly thought to mediate the oxidation of ammonium to nitrite in marine environments. Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1-3 orders of magnitude higher than those of bacterial amoA. Our data thus suggest a major role for Archaea in oceanic nitrification.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 November 2019
                2019
                : 14
                : 11
                : e0224888
                Affiliations
                [1 ] Submarine Resources Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa, Japan
                [2 ] Japan Collection of Microorganisms (JCM), RIKEN BioResource Research Center, Tsukuba, Ibaraki, Japan
                [3 ] Research and Development Center for Marine Biosciences, JAMSTEC, Yokosuka, Kanagawa, Japan
                University of Trento, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-4175-0532
                Article
                PONE-D-19-16016
                10.1371/journal.pone.0224888
                6839870
                31703093
                6bb64184-35c0-4862-8504-3e77cd5c298c
                © 2019 Kato et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 June 2019
                : 23 October 2019
                Page count
                Figures: 7, Tables: 1, Pages: 22
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 19H03310
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002770, Cabinet Office, Government of Japan;
                Award ID: SIP Zipangu-in-the-ocean project
                Award Recipient :
                This research was supported by the Cabinet Office, Government of Japan, through the Next-generation Technology for Ocean Resources Exploration (known as Zipangu-in-the-ocean project) in the Cross-ministerial Strategic Innovation Promotion Program (SIP) to SK and KS, and by a Grant-in-Aid for Scientific Research (B) (#19H03310) from the Japan Society for the Promotion of Science(JSPS), The Ministry of Education,Culture,Sports,Science and Technology(MEXT) to SK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Genetics
                Genomics
                Metagenomics
                Physical Sciences
                Chemistry
                Chemical Reactions
                Oxidation
                Physical Sciences
                Materials Science
                Materials
                Coatings
                Engineering and Technology
                Manufacturing Processes
                Surface Treatments
                Coatings
                Physical Sciences
                Chemistry
                Chemical Elements
                Manganese
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Non-coding RNA
                Ribosomal RNA
                Biology and life sciences
                Biochemistry
                Ribosomes
                Ribosomal RNA
                Biology and life sciences
                Cell biology
                Cellular structures and organelles
                Ribosomes
                Ribosomal RNA
                Physical Sciences
                Chemistry
                Chemical Compounds
                Ammonia
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Physical Sciences
                Chemistry
                Chemical Elements
                Sulfur
                Custom metadata
                All sequence data are available from the DDBJ database (accession numbers BFAR01000001–BFAR01000180, BFAS01000001–BFAS01000378, BFAT01000001–BFAT01000343, BFAU01000001–BFAU01000244), and FigShare ( https://doi.org/10.6084/m9.figshare.5857878.v2)

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