Katherine M. Fullerton, Matthew O Schrenk, Mustafa Yücel, Elena Manini, Marco Basili, Timothy J. Rogers, Daniele Fattorini, Marta Di Carlo, Giuseppe d’Errico, Francesco Regoli, Mayuko Nakagawa, Costantino Vetriani, Francesco Smedile, Carlos Ramírez, Heather Miller, Shaunna M. Morrison, Joy Buongiorno, Gerdhard L. Jessen, María Martínez, J. Maarten de Moor, Peter H. Barry, Donato Giovannelli, Karen G. Lloyd

The deep subsurface is one of Earth’s largest biomes. Here, microorganisms modify volatiles moving between the deep and surface Earth. However, it is unknown whether large-scale tectonic processes affect the distribution of microorganisms across this subterranean landscape. We sampled subsurface microbial ecosystems in deeply-sourced springs across the Costa Rican convergent margin. Noble gases, inorganic and organic carbon isotopes, and photosynthetic biomarkers demonstrate negligible surficial input. Total bacterial community compositions correlate with the major cation and anion compositions of subsurface fluids that are driven by underlying tectonic processes. Co-occurrence networks identify microbial cliques correlating with dissolved carbon compounds, dominated by likely chemolithoautotrophs using the reverse tricarboxylic acid (rTCA) cycle. Metagenomic abundances of rTCA cycle genes also correlate with dissolved inorganic carbon (DIC) across the convergent margin, supporting carbon isotopic evidence3 that fixation of slab-derived CO2 into biomass forms the base of a complex subsurface ecosystem. We conclude that subsurface microbial distribution across this convergent margin is ultimately controlled by slab dip angle, tectonic stress regime, carbon volatilization from the slab/mantle source, and the extent of deep subsurface calcite precipitation. Our work establishes a complex feedback whereby the biological processes that alter deep volatile outputs are themselves driven by large-scale tectonic processes.