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Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system

Author

Listed:
  • Karthik Anantharaman

    (University of California)

  • Christopher T. Brown

    (University of California)

  • Laura A. Hug

    (University of California)

  • Itai Sharon

    (University of California)

  • Cindy J. Castelle

    (University of California)

  • Alexander J. Probst

    (University of California)

  • Brian C. Thomas

    (University of California)

  • Andrea Singh

    (University of California)

  • Michael J. Wilkins

    (The Ohio State University)

  • Ulas Karaoz

    (Earth and Environmental Sciences, Lawrence Berkeley National Laboratory)

  • Eoin L. Brodie

    (Earth and Environmental Sciences, Lawrence Berkeley National Laboratory)

  • Kenneth H. Williams

    (Earth and Environmental Sciences, Lawrence Berkeley National Laboratory)

  • Susan S. Hubbard

    (Earth and Environmental Sciences, Lawrence Berkeley National Laboratory)

  • Jillian F. Banfield

    (University of California
    Earth and Environmental Sciences, Lawrence Berkeley National Laboratory)

Abstract

The subterranean world hosts up to one-fifth of all biomass, including microbial communities that drive transformations central to Earth’s biogeochemical cycles. However, little is known about how complex microbial communities in such environments are structured, and how inter-organism interactions shape ecosystem function. Here we apply terabase-scale cultivation-independent metagenomics to aquifer sediments and groundwater, and reconstruct 2,540 draft-quality, near-complete and complete strain-resolved genomes that represent the majority of known bacterial phyla as well as 47 newly discovered phylum-level lineages. Metabolic analyses spanning this vast phylogenetic diversity and representing up to 36% of organisms detected in the system are used to document the distribution of pathways in coexisting organisms. Consistent with prior findings indicating metabolic handoffs in simple consortia, we find that few organisms within the community can conduct multiple sequential redox transformations. As environmental conditions change, different assemblages of organisms are selected for, altering linkages among the major biogeochemical cycles.

Suggested Citation

  • Karthik Anantharaman & Christopher T. Brown & Laura A. Hug & Itai Sharon & Cindy J. Castelle & Alexander J. Probst & Brian C. Thomas & Andrea Singh & Michael J. Wilkins & Ulas Karaoz & Eoin L. Brodie , 2016. "Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms13219
    DOI: 10.1038/ncomms13219
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    Cited by:

    1. Paraskevi Mara & David Geller-McGrath & Virginia Edgcomb & David Beaudoin & Yuki Morono & Andreas Teske, 2023. "Metagenomic profiles of archaea and bacteria within thermal and geochemical gradients of the Guaymas Basin deep subsurface," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Ming Peng & Chun-Yang Li & Xiu-Lan Chen & Beth T. Williams & Kang Li & Ya-Nan Gao & Peng Wang & Ning Wang & Chao Gao & Shan Zhang & Marie C. Schoelmerich & Jillian F. Banfield & J. Benjamin Miller & N, 2022. "Insights into methionine S-methylation in diverse organisms," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Yunxi Liu & R. A. Leo Elworth & Michael D. Jochum & Kjersti M. Aagaard & Todd J. Treangen, 2022. "De novo identification of microbial contaminants in low microbial biomass microbiomes with Squeegee," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Morten Kam Dahl Dueholm & Marta Nierychlo & Kasper Skytte Andersen & Vibeke Rudkjøbing & Simon Knutsson & Mads Albertsen & Per Halkjær Nielsen, 2022. "MiDAS 4: A global catalogue of full-length 16S rRNA gene sequences and taxonomy for studies of bacterial communities in wastewater treatment plants," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Helena Osterholz & Stephanie Turner & Linda J. Alakangas & Eva-Lena Tullborg & Thorsten Dittmar & Birgitta E. Kalinowski & Mark Dopson, 2022. "Terrigenous dissolved organic matter persists in the energy-limited deep groundwaters of the Fennoscandian Shield," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Xianzhe Gong & Álvaro Rodríguez Río & Le Xu & Zhiyi Chen & Marguerite V. Langwig & Lei Su & Mingxue Sun & Jaime Huerta-Cepas & Valerie Anda & Brett J. Baker, 2022. "New globally distributed bacterial phyla within the FCB superphylum," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Marie C. Schoelmerich & Heleen T. Ouboter & Rohan Sachdeva & Petar I. Penev & Yuki Amano & Jacob West-Roberts & Cornelia U. Welte & Jillian F. Banfield, 2022. "A widespread group of large plasmids in methanotrophic Methanoperedens archaea," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    8. Kelly J. Whaley-Martin & Lin-Xing Chen & Tara Colenbrander Nelson & Jennifer Gordon & Rose Kantor & Lauren E. Twible & Stephanie Marshall & Sam McGarry & Laura Rossi & Benoit Bessette & Christian Baro, 2023. "O2 partitioning of sulfur oxidizing bacteria drives acidity and thiosulfate distributions in mining waters," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Natasha K. Dudek & Jesus G. Galaz-Montoya & Handuo Shi & Megan Mayer & Cristina Danita & Arianna I. Celis & Tobias Viehboeck & Gong-Her Wu & Barry Behr & Silvia Bulgheresi & Kerwyn Casey Huang & Wah C, 2023. "Previously uncharacterized rectangular bacterial structures in the dolphin mouth," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    10. S. Emil Ruff & Pauline Humez & Isabella Hrabe Angelis & Muhe Diao & Michael Nightingale & Sara Cho & Liam Connors & Olukayode O. Kuloyo & Alan Seltzer & Samuel Bowman & Scott D. Wankel & Cynthia N. Mc, 2023. "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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