Abstract

Earth’s mantle releases 38.7 ± 2.9 Tg/yr CO2 along with other reduced and oxidized gases to the atmosphere shaping microbial metabolism at volcanic sites across the globe, yet little is known about its impact on microbial life under non-thermal conditions. Here, we perform comparative metagenomics coupled to geochemical measurements of deep subsurface fluids from a cold-water geyser driven by mantle degassing. Key organisms belonging to uncultivated Candidatus Altiarchaeum show a global biogeographic pattern and site-specific adaptations shaped by gene loss and inter-kingdom horizontal gene transfer. Comparison of the geyser community to 16 other publicly available deep subsurface sites demonstrate a conservation of chemolithoautotrophic metabolism across sites. In silico replication measures suggest a linear relationship of bacterial replication with ecosystems depth with the exception of impacted sites, which show near surface characteristics. Our results suggest that subsurface ecosystems affected by geological degassing are hotspots for microbial life in the deep biosphere.

Highlights

  • Earth’s mantle releases 38.7 ± 2.9 Tg/yr CO2 along with other reduced and oxidized gases to the atmosphere shaping microbial metabolism at volcanic sites across the globe, yet little is known about its impact on microbial life under non-thermal conditions

  • The community composition based on ribosomal protein S3 sequences assembled from the metagenome displayed a fairly restricted diversity consisting of 52 organisms, which spanned twelve phyla (Fig. 1)

  • The core community was composed of 15 organisms detected via ribosomal protein S3 (rpS3) across all three metagenomes (Fig. 1), and they accounted for 42.8% (1.3% SD) of the total relative abundance of the community

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Summary

Introduction

Earth’s mantle releases 38.7 ± 2.9 Tg/yr CO2 along with other reduced and oxidized gases to the atmosphere shaping microbial metabolism at volcanic sites across the globe, yet little is known about its impact on microbial life under non-thermal conditions. We perform comparative metagenomics coupled to geochemical measurements of deep subsurface fluids from a cold-water geyser driven by mantle degassing. Our results suggest that subsurface ecosystems affected by geological degassing are hotspots for microbial life in the deep biosphere. Subsurface lithoautotrophic microbial communities[8] have been reported for many terrestrial ecosystems including the Fennoscandian Shield[9], the Columbia River Basalt[8], the Witwatersrand Basin[10], and subsurface fluids discharged by Crystal Geyser[11]. While these subsurface ecosystems are usually dominated by bacteria, one exception are archaea belonging to the Alti-1 clade of the Ca. Altiarchaeota[5,12,13]. Altiarchaeota live autotrophically using the Wood-Ljungdahl carbon fixation pathway[16], which was the most dominant carbon fixation pathway prior to the evolution of photosynthesis[17,18]

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Results
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