No 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.

The hemlock woolly adelgid (HWA) is an insect native to Asia and likely western North America. First reported in eastern North America in 1951, it has devastated eastern hemlock (Tsuga canadensis) populations. Loss of hemlock will greatly affect the structure and function of eastern forests. Susceptibility to adelgid infestation varies within eastern hemlocks and across other hemlock species. Our study was conducted to determine whether eastern hemlocks share a similar stem (phyllosphere) microbial community with other co‐occurring hemlocks and whether community‐level shifts are associated within trees of the same species based on HWA infestation. Surprisingly, we found no difference in microbial community composition or diversity between trees of the same species based on the level of HWA infestation. However, microbial communities varied significantly across the four hemlock trees sampled, native T. canadensis and three non‐natives: Tsuga chinensis, Tsuga dumosa, and Tsuga sieboldii. Within these tree hosts, microbial communities from T. dumosa and T. chinensis clustered together, and microbial communities from T. canadensis and T. sieboldii clustered separately from all other tree species. Additionally, specific indicator taxa were identified for all the tree species sampled. These results indicate that Asian hemlocks might not fill the same niche in eastern forests as the native eastern hemlock. Further work should be conducted to determine how differences in hemlock species and associated microbial communities might scale up to alter organismal interactions involving hemlocks.

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.