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pmid:31911466

Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment.

Zhichao Zhou · Yang Liu · Wei Xu · Jie Pan · Zhu-Hua Luo · Meng Li

mSystems · 2020 doi:10.1128/mSystems.00795-19

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title
Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment.
doi
10.1128/mSystems.00795-19
pmid
31911466
authors array · 6 items
[0]
Zhichao Zhou
[1]
Yang Liu
[2]
Wei Xu
[3]
Jie Pan
[4]
Zhu-Hua Luo
[5]
Meng Li
journal
mSystems
year
2020
abstract
Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as Hydrothermarchaeota) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and the surrounding sulfur-rich sediments on the South Atlantic Mid-Ocean Ridge and publicly available data sets (the Integrated Microbial Genomes system of the U.S. Department of Energy-Joint Genome Institute and NCBI SRA data sets). Genomic analysis suggested a wide carbon metabolic diversity of Hydrothermarchaeota members, including the utilization of proteins, lactate, and acetate; the anaerobic degradation of aromatics; the oxidation of C1 compounds (CO, formate, and formaldehyde); the utilization of methyl compounds; CO2 incorporation by the tetrahydromethanopterin-based Wood-Ljungdahl pathway; and participation in the type III ribulose-1,5-bisphosphate carboxylase/oxygenase-based Calvin-Benson-Bassham cycle. These microbes also potentially oxidize sulfur, arsenic, and hydrogen and engage in anaerobic respiration based on sulfate reduction and denitrification. Among the 140 MAGs reconstructed from the black smoker chimney microbial community (including Hydrothermarchaeota MAGs), community-level metabolic predictions suggested a redundancy of carbon utilization and element cycling functions and interactive syntrophic and sequential utilization of substrates. These processes might make various carbon and energy sources widely accessible to the microorganisms. Further, the analysis suggested that Hydrothermarchaeota members contained important functional components obtained from the community via lateral gene transfer, becoming a distinctive clade. This might serve as a niche-adaptive strategy for metabolizing heavy metals, C1 compounds, and reduced sulfur compounds. Collectively, the analysis provides comprehensive metabolic insights into the Hydrothermarchaeota IMPORTANCE This study provides comprehensive metabolic insights into the Hydrothermarchaeota from comparative genomics, evolution, and community-level perspectives. Members of the Hydrothermarchaeota synergistically participate in a wide range of carbon-utilizing and element cycling processes with other microorganisms in the community. We expand the current understanding of community interactions within the hydrothermal sediment and chimney, suggesting that microbial interactions based on sequential substrate metabolism are essential to nutrient and element cycling.
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The P value and odds ratios were calculated by Fisher’s exact test.
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Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18. DATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.
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sections[21] "Data availability." paragraphs 1-3
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Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18. DATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.
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Hydrothermarchaeota is a novel archaeal phylum.
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Overview of genomic statistics for archaeal MAGs constructed in the current study and reference and NCBI SRA depositsa
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Value for the following Hydrothermarchaeota MAG:
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SZUA-158 (TVG10)
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JdFR-17
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JdFR-18
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[7]
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99
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[7]
141
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98.13
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80.43
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1.76
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1.87
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35.29
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49.64
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39.14
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40.02
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4.50
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1.54
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1.98
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84.96
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Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18. DATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.
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Complete file
{"sci_version": "1.0", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:31911466", "kind": "science-record", "revision": 4, "content_hash": "sha256:4c3477611d73a2aeffb0537332fcbf2374734c415ab51a82f94dab84209ad962", "created_at": "2026-11-01T15:40:54Z", "updated_at": "2026-11-01T21:22:48Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment.", "doi": "10.1128/mSystems.00795-19", "pmid": "31911466", "authors": ["Zhichao Zhou", "Yang Liu", "Wei Xu", "Jie Pan", "Zhu-Hua Luo", "Meng Li"], "journal": "mSystems", "year": 2020, "abstract": "Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as Hydrothermarchaeota) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and the surrounding sulfur-rich sediments on the South Atlantic Mid-Ocean Ridge and publicly available data sets (the Integrated Microbial Genomes system of the U.S. Department of Energy-Joint Genome Institute and NCBI SRA data sets). Genomic analysis suggested a wide carbon metabolic diversity of Hydrothermarchaeota members, including the utilization of proteins, lactate, and acetate; the anaerobic degradation of aromatics; the oxidation of C1 compounds (CO, formate, and formaldehyde); the utilization of methyl compounds; CO2 incorporation by the tetrahydromethanopterin-based Wood-Ljungdahl pathway; and participation in the type III ribulose-1,5-bisphosphate carboxylase/oxygenase-based Calvin-Benson-Bassham cycle. These microbes also potentially oxidize sulfur, arsenic, and hydrogen and engage in anaerobic respiration based on sulfate reduction and denitrification. Among the 140 MAGs reconstructed from the black smoker chimney microbial community (including Hydrothermarchaeota MAGs), community-level metabolic predictions suggested a redundancy of carbon utilization and element cycling functions and interactive syntrophic and sequential utilization of substrates. These processes might make various carbon and energy sources widely accessible to the microorganisms. Further, the analysis suggested that Hydrothermarchaeota members contained important functional components obtained from the community via lateral gene transfer, becoming a distinctive clade. This might serve as a niche-adaptive strategy for metabolizing heavy metals, C1 compounds, and reduced sulfur compounds. Collectively, the analysis provides comprehensive metabolic insights into the Hydrothermarchaeota IMPORTANCE This study provides comprehensive metabolic insights into the Hydrothermarchaeota from comparative genomics, evolution, and community-level perspectives. Members of the Hydrothermarchaeota synergistically participate in a wide range of carbon-utilizing and element cycling processes with other microorganisms in the community. We expand the current understanding of community interactions within the hydrothermal sediment and chimney, suggesting that microbial interactions based on sequential substrate metabolism are essential to nutrient and element cycling.", "claims": [{"id": "claim-method", "statement": "The P value and odds ratios were calculated by Fisher’s exact test.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:31911466", "locator": "sections[10] \"Clade-distinctive LGT.\" paragraph 4", "quote": "The P value and odds ratios were calculated by Fisher’s exact test."}], "state": "complete"}, {"id": "claim-data-access", "statement": "Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18.\nDATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. 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Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.", "structure": {"repository": "GEO", "access_route": "GEO accession URL", "access_statement_verbatim": "Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18.\nDATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.", "access_statement_kind": "data_availability_statement", "sample_accessions": [], "sample_count": null, "group_sizes": null, "group_sizes_basis": null, "platform": null, "taxon": null, "title": null, "resolution_checked_at": "2026-10-31T18:35:43Z", "resolution_check": "identifier_resolution_only_no_download_no_licence_read", "downloaded": false, "licence_read": false}}, {"id": "asset:table:pmid:31911466:1", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:fcbeab0f28ba19cfef40467aff285c2d7d304abb326ff071e1b7079da2660455", "bytes": 1510, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[3]/table-wrap[1]#tab1", "version": null, "note": "Overview of genomic statistics for archaeal MAGs constructed in the current study and reference and NCBI SRA depositsa", "structure": {"pmcid": "PMC6946796", "section_index": 3, "section_title": "Hydrothermarchaeota is a novel archaeal phylum.", "row_count": 19, "column_count": 8}, "table": {"label": "TABLE 1", "caption": "Overview of genomic statistics for archaeal MAGs constructed in the current study and reference and NCBI SRA depositsa", "rows": [["Characteristic", "Value for the following Hydrothermarchaeota MAG:"], ["SZUA-158 (TVG10)", "SZUA-236 (TVG13)", "SZUA-237 (TVG13)", "JdFR-16", "JdFR-17", "JdFR-18", "HyVt-292"], ["No. of copies of individual markers", "", "", "", "", "", "", ""], ["0", "9", "21", "49", "99", "87", "2", "30"], ["1", "139", "128", "136", "25", "59", "145", "141"], ["2", "1", "0", "3", "25", "29", "2", "17"], ["3", "0", "0", "0", "0", "12", "0", "0"], ["4", "0", "0", "0", "0", "1", "0", "0"], ["5+", "0", "0", "0", "0", "0", "0", "0"], ["Completeness (%)", "92.53", "84.97", "65.82", "31.93", "53.87", "98.13", "80.43"], ["Contamination (%)", "0.93", "0.00", "1.76", "13.55", "25.15", "1.87", "9.06"], ["Strain heterogeneity (%)", "0.00", "0.00", "33.33", "84.00", "71.83", "0.00", "35.29"], ["Bin size (bp)", "1,749,358", "1,270,198", "1,228,833", "1,353,114", "2,178,134", "2,062,134", "1,426,722"], ["N50 (bp)", "9,590", "6,219", "3,825", "6,267", "7,687", "149,032", "5,600"], ["Mean scaffold length (bp)", "7,706.42", "5,747.50", "3,510.95", "5,614.58", "6,331.78", "93,733.36", "4,988.54"], ["No. of scaffolds", "227", "221", "350", "241", "344", "22", "286"], ["GC (%)", "38.99", "47.58", "45.76", "49.68", "49.64", "39.14", "40.02"], ["GC SD (%)", "1.91", "1.99", "2.89", "3.92", "4.50", "1.54", "1.98"], ["Coding density (%)", "84.96", "91.48", "84.96", "91.98", "91.94", "92.12", "89.88"]], "row_count": 19, "column_count": 8, "numeric_cells": 126, "header_rows": 2, "locator": "section[3]/table-wrap[1]#tab1"}}], "gaps": ["asset:data:geo:PRJNA385762 not downloaded", "asset:data:geo:PRJNA385762 licence not read", "asset:data:geo:PRJNA480137 not downloaded", "asset:data:geo:PRJNA480137 licence not read", "asset:data:geo:SRR7786998 not downloaded", "asset:data:geo:SRR7786998 licence not read"]}, "analysis": {"state": "partial", "methods": [{"id": "method-1", "family": null, "specific": null, "label": "Fisher’s exact test", "dsl_operations": [], "missing_operations": [], "expressible": null, "parameters": {}, "data_shapes": [], "evidence": {"score": 1.0, "band": "verbatim", "quote": "The P value and odds ratios were calculated by Fisher’s exact test."}}], "targets": [], "gaps": ["method.reader_named_unmapped"]}, "capability": {"state": "complete", "requirements": [{"capability_id": "capability:computational_analysis", "label": "Computational analysis platform", "assay_families": ["meta_analysis", "machine_learning", "survival_analysis", "statistical_regression", "pca", "molecular_docking", "network_analysis", "differential_expression", "gwas"], "availability_state": "owned", "tier_unlocked": "R1", "candidate": "Automated Assays Laravel application and simulated adapters"}], "gaps": []}, "readiness": {"state": "blocked", "tier": "R4", "blocking_axis": "data", "blocked_on": "data:accession_absent", "axes": {"method": {"tier": "R4", "expressible": false, "required_operations": [], "missing_operations": [], "basis": "The reader quoted the method the paper names (Fisher’s exact test), but the corpus's method extractor could not map it onto a DSL operation, so the method is published but not expressible."}, "capability": {"tier": "R1", "capability_id": "capability:computational_analysis", "availability_state": "owned", "basis": "The computational analysis is owned. The physical bench the paper used is not, so a physical validation cannot be run here."}, "data": {"tier": "R4", "reachable": false, "accessions": ["PRJNA385762", "PRJNA480137", "SRR7786998"], "resolved_accessions": [], "statements": ["Accession numbers for the initial assemblies were as follows: IMG accession number 3300003886 for TVG10 and IMG accession number 3300003885 for TVG13. Accession numbers for the second-round assemblies were as follows: IMG accession number 3300020233 for TVG10 and IMG accession number 3300020236 for TVG13. The MAGs that were resolved in the current study are deposited in NCBI under BioProject accession numbers PRJNA385762 and PRJNA480137. Detailed genomic parameters of the assembled genomes are summarized in Text S1. The NCBI and IMG genome accession numbers for the MAGs that were used in this study are NCBI accession number GCA_003230355.1 for SZUA-236, NCBI accession number GCA_003229275.1 for SZUA-237, NCBI accession number GCA_003229935.1 for SZUA-158, NCBI accession number SRR7786998 for HyVt-292, IMG accession number 2728369317 for JdFR-16, IMG accession number 2728369322 for JdFR-17, and IMG accession number 2728369320 for JdFR-18.\nDATA SET S1Metabolic profile of seven Hydrothermarchaeota MAGs. Download Data Set S1, XLSX file, 0.8 MB.Copyright © 2020 Zhou et al.This content is distributed under the terms of the Creative Commons Attribution 4.0 International license."], "basis": "The paper names PRJNA385762, PRJNA480137, SRR7786998, but the accession does not resolve in the repository (not_in_ncbi_bioproject, not_in_ncbi_bioproject, not_in_ncbi_sra), so the data cannot be reached from here. 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