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Chemolithoautotroph distributions across the subsurface of a convergent margin

The ISME Journal volume 17, pages 140–150 (2023)Cite this article

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Abstract

Subducting oceanic crusts release fluids rich in biologically relevant compounds into the overriding plate, fueling subsurface chemolithoautotrophic ecosystems. To understand the impact of subsurface geochemistry on microbial communities, we collected fluid and sediments from 14 natural springs across a ~200 km transect across the Costa Rican convergent margin and performed shotgun metagenomics. The resulting 404 metagenome-assembled genomes (MAGs) cluster into geologically distinct regions based on MAG abundance patterns: outer forearc-only (25% of total relative abundance), forearc/arc-only (38% of total relative abundance), and delocalized (37% of total relative abundance) clusters. In the outer forearc, Thermodesulfovibrionia, Candidatus Bipolaricaulia, and Firmicutes have hydrogenotrophic sulfate reduction and Wood-Ljungdahl (WL) carbon fixation pathways. In the forearc/arc, Anaerolineae, Ca. Bipolaricaulia, and Thermodesulfovibrionia have sulfur oxidation, nitrogen cycling, microaerophilic respiration, and WL, while Aquificae have aerobic sulfur oxidation and reverse tricarboxylic acid carbon fixation pathway. Transformation-based canonical correspondence analysis shows that MAG distribution corresponds to concentrations of aluminum, iron, nickel, dissolved inorganic carbon, and phosphate. While delocalized MAGs appear surface-derived, the subsurface chemolithoautotrophic, metabolic, and taxonomic landscape varies by the availability of minerals/metals and volcanically derived inorganic carbon. However, the WL pathway persists across all samples, suggesting that this versatile, energy-efficient carbon fixation pathway helps shape convergent margin subsurface ecosystems.

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Fig. 1: General convergent margin geological structure and sample sites spanning the Costa Rican convergent margin.
Fig. 2: Heatmap of metagenomic read recruitment to each MAG and hierarchical clustering based on Spearman rank correlations between MAGs (vertical clusters) and sample sites (horizontal clusters) shows the separation of MAGs into those found mostly in the forearc/arc, the outer forearc, or delocalized across geological provinces.
Fig. 3: Average read abundance (GCPM) per site of MAGs with metabolic pathways for redox reactions and carbon fixation pathways.
Fig. 4: Nitrogen, sulfur, and hydrogen cycling pathways in MAGs with carbon fixation pathways from the outer forearc and the forearc/arc.
Fig. 5: Transformation-based canonical correspondence analysis showing variables most closely correlated with MAG abundance distribution at each site and site distribution of each MAG (scaling = 2).
Fig. 6: Schematic cross-section (to scale) of the 3D distribution of subsurface microbial communities and their metabolisms across the Costa Rica convergent margin, showing a shallowing of potential habitable area from the outer forearc to the arc.

Data availability

Metagenomic data are available in the NCBI SRA with project ID PRJNA627197. All MAGs analyzed in this study are also included under the same BioProject. BioSample accessions for each MAG are included in Supplementary Table S1. The full environmental dataset along with the R scripts for this analysis is available at https://github.com/TJrogers86/Costa-Rica-2017.git and released as a permanent version (v1.0.0) using Zenodo under https://doi.org/10.5281/zenodo.6259294.

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Acknowledgements

The authors acknowledge the Biology Meets Subduction Project, funded by the Alfred P. Sloan Foundation and the Deep Carbon Observatory (G-2016-7206) to PHB, JMdM, DG, and KGL, with DNA sequencing from the Census of Deep Life. Additional support came from NSF FRES (Award# 21211637) to PHB, JMdM and KGL. U. S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Genomic Science Program (DE-SC0020369 to KGL) and FONDECYT Grant 11191138 (ANID Chile) and COPAS COASTAL ANID FB210021 to GLJ. DG, AC, and MS were partially supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program Grant Agreement No. 948972—COEVOLVE—ERC-2020-STG.

Author information

Authors and Affiliations

  1. University of Tennessee, Knoxville, TN, USA

    Timothy J. Rogers, James A. Fordyce & Karen G. Lloyd

  2. Division of Natural Sciences, Maryville College, Maryville, TN, USA

    Joy Buongiorno

  3. Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile

    Gerdhard L. Jessen

  4. Center for Oceanographic Research COPAS COASTAL, Universidad de Concepción, Valdivia, Chile

    Gerdhard L. Jessen

  5. Michigan State University, East Lansing, MI, USA

    Matthew O. Schrenk

  6. National University of Costa Rica, Heredia, Costa Rica

    J. Maarten de Moor

  7. University of New Mexico, Albuquerque, NM, USA

    J. Maarten de Moor

  8. Servicio Geológico Ambiental, Heredia, Costa Rica

    Carlos J. Ramírez

  9. Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Peter H. Barry

  10. Institute of Marine Sciences, Middle East Technical University, Erdemli, Turkey

    Mustafa Yücel

  11. Department of Biology, University of Naples ―Federico II, Naples, Italy

    Matteo Selci, Angela Cordone & Donato Giovannelli

  12. Department of Marine and Coastal Science, Rutgers University, Rutgers, NJ, USA

    Donato Giovannelli

  13. Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo, Japan

    Donato Giovannelli

  14. National Research Council – Institute of Marine Biological Resources and Biotechnologies – CNR-IRBIM, Ancona, Italy

    Donato Giovannelli

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Contributions

Conceptualization and funding acquisition were performed by PHB, JMdM, DG and KGL. Investigations and data acquisition were performed by TJR, KGL, DG, JB, GLJ, MOS, JAF, JMdM, CR, PHB, MY, MS, and AC. TJR performed data analysis, visualization, and drafted the paper with edits and feedback of from KGL, DG, JB, GLJ, MOS, JAF, JMdM, CR, PHB, MY, MS, and AC.

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Correspondence to Karen G. Lloyd.

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Rogers, T.J., Buongiorno, J., Jessen, G.L. et al. Chemolithoautotroph distributions across the subsurface of a convergent margin. ISME J 17, 140–150 (2023). https://doi.org/10.1038/s41396-022-01331-7

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  • DOI: https://doi.org/10.1038/s41396-022-01331-7

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