Metagenomic investigation of microbial dark carbon fixation, viral interactions, and horizonal gene transfer within a convergent margin subsurface ecosystem

Convergent margins are geological regions where two or more tectonic plates collide, and the denser “subducting slab” is pushed beneath the less dense overriding plate. As the slab descends, it devolatilizes under higher temperatures and pressures, allowing dissolved inorganic carbon (DIC) and redox active volatile rich fluids to cycle between the upper crust and Earth’s mantle. These fluids migrate through cracks and fissures in the upper mantle and crust, fueling chemolithoautotrophy-based microbial ecosystems in the subsurface before they are expelled on the surface in the form of hydrothermal seeps and springs. Chemolithoautotrophic ecosystems, such as those in the Costa Rican convergent margin, generate substantial amounts of organic matter with up to 24 mM dissolved organic carbon (DOC), and may sequester 1.4 x 109 to 1.4 x 1010 molC/year. However, the rate at which DIC is biologically sequestered is dependent on the geochemistry of the system, the chemolithoautotrophic species present therein, the carbon fixation pathways (CFPs) they possess, as well as potential viral-host integrations and the effects of horizontal gene transfer (HGT).

In this work, we first review the current knowledge on the geochemical constraints on and the evolutionary adaptations of chemolithoautotrophs and the CFP’s they contain within DIC rich, intermediate, and limited terrestrial subsurface ecosystems. Next, using approaches that combine co-located metagenome sequences and geochemical data, we describe the distribution of chemolithoautotrophs across the Costa Rican convergent margin. Then, we use metagenomic data from the hot springs of Costa Rica and Panama to describe the viral-host interactions within the Central American subduction zone as well as the distribution of viral auxiliary metabolic genes. Finally, we describe a case of HGT in which it appears that uncultured members of the bacteria class Syntrophia have acquired a key gene of the reductive citric acid cycle, a micro-aerophilic CFP, from the archaeal clade AMNE-I.