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Effect of tectonic processes on biosphere–geosphere feedbacks across a convergent margin

Abstract

The subsurface is among Earth’s largest biomes, but the extent to which microbial communities vary across tectonic plate boundaries or interact with subduction-scale geological processes remains unknown. Here we compare bacterial community composition with deep-subsurface geochemistry from 21 hot springs across the Costa Rican convergent margin. We find that cation and anion compositions of the springs reflect the dip angle and position of the underlying tectonic structure and also correlate with the bacterial community. Co-occurring microbial cliques related to cultured chemolithoautotrophs that use the reverse tricarboxylic acid cycle (rTCA) as well as abundances of metagenomic rTCA genes correlate with concentrations of slab-volatilized carbon. This, combined with carbon isotope evidence, suggests that fixation of slab-derived CO2 into biomass may support a chemolithoautotrophy-based subsurface ecosystem. We calculate that this forearc subsurface biosphere could sequester 1.4 × 109 to 1.4 × 1010 mol of carbon per year, which would decrease estimates of the total carbon delivered to the mantle by 2 to 22%. Based on the observed correlations, we suggest that distribution and composition of the subsurface bacterial community are probably affected by deep tectonic processes across the Costa Rican convergent margin and that, by sequestering carbon volatilized during subduction, these chemolithoautotrophic communities could in turn impact the geosphere.

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Fig. 1: Sites span the Costa Rican convergent margin, with organic matter produced from chemolithoautotrophy of deep-slab inorganic carbon.
Fig. 2: Clustering of the sites based on microbial community diversity and geochemical characteristics.
Fig. 3: Bacterial cliques each have different relationships to subduction zone geochemistry.
Fig. 4: Metagenome-derived genes from the same carbon-fixation pathway correlate with each other and with subduction zone geochemistry.

Data availability

This Targeted Locus Study project has been deposited at DDBJ/EMBL/GenBank under the accession KEBJ00000000, with project ID PRJNA579365. The version described in this paper is the first version, KEBJ01000000. Metagenomic data are in the NCBI SRA with project ID PRJNA627197. The full environmental dataset is available at https://github.com/dgiovannelli/SubductCR_16S-diversity.git and released as a permanent version (v1.0) using Zenodo under https://doi.org/10.5281/zenodo.4553845. Source data are provided with this paper.

Code availability

A complete R script containing all the steps to reproduce our analysis, including the full environmental dataset, is available at https://github.com/dgiovannelli/SubductCR_16S-diversity.git and released as a permanent version (v1.0) using Zenodo under https://doi.org/10.5281/zenodo.4553845, https://doi.org/10.5281/zenodo.3483104.

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Acknowledgements

This work is part of the Biology Meets Subduction project, a collaboration of 46 researchers from 19 institutions from 9 nationalities. We thank P. Barcala Dominguez for assistance with figure illustrations, and T. Hoehler for advice. Principal support came from the Alfred P. Sloan Foundation and the Deep Carbon Observatory (G-2016-7206) to P.H.B., J.M.d.M, D.G. and K.G.L., with DNA sequencing from the Census of Deep Life. Additional support came from NSF OCE-1431598, NASA Exobiology NNX16AL59G and Simons Foundation 404586 to K.G.L., NSF 1144559 to P.H.B., NSF 1850699 to J.M.d.M., NSF MCB 15–17567 to D.G. and C.V., ELSI Origins Network (EON) Research Fellowship from the John Templeton Foundation to D.G., Deep Life Modeling and Visualization Fellowship from the Deep Carbon Observatory to D.G., FONDECYT Grant 11191138 (ANID Chile) to G.L.J., ENIGMA (NASA Astrobiology Institute cycle 8, 80NSSC18M0093) to D.G., S.M.M. and J.B, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research (DE-SC0020369) to A.D.S. and K.G.L., JSPS KAKENHI grants JP17K14412, JP17H06105 and JP17H02989 to M.N. and DEKOSIM grant BAP-08-11-DPT.2012K120880, financed by the Strategy and Budget Ministry of Turkey, to M.Y. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the John Templeton Foundation.

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K.M.F. and K.G.L. wrote the original draft and performed initial data analyses. Conceptualization and funding acquisition were performed by P.H.B., J.M.d.M., D.G. and K.G.L. Formal analysis and visualization were performed by K.M.F. and D.G. Investigations and data acquisition were performed by K.M.F., M.Y., E.M., G.D., D.F., M.D.C., F.R., M.N., F.S., H.M., S.M.M., T.J.R., M.B., J.B., A.D.S. and D.G. Writing and editing of the final draft was performed by M.O.S., M.Y., M.N., C.V., C.R., G.L.J., H.M., T.J.R., M.M., J.B., J.M.d.M., P.H.B., A.D.S., D.G. and K.G.L.

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Correspondence to Donato Giovannelli or Karen G. Lloyd.

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Supplementary information

Supplementary Information

Supplementary Tables 1–17 and Figures 1–12.

Source data

Source Data Fig. 1

Source data for Fig. 1.

Source Data Fig. 2

Source data for the NMDS and ternary plots appearing in Fig. 2.

Source Data Fig. 3

Source data for the network analysis and the correlation of the cliques appearing in Fig. 3.

Source Data Fig. 4

Source data for the network analysis and the correlation of the gene-cliques appearing in Fig. 4.

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Fullerton, K.M., Schrenk, M.O., Yücel, M. et al. Effect of tectonic processes on biosphere–geosphere feedbacks across a convergent margin. Nat. Geosci. 14, 301–306 (2021). https://doi.org/10.1038/s41561-021-00725-0

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