• Energy Research

AbstractHydrothermal systems, including terrestrial hot springs, contain diverse geochemical conditions that vary over short spatial scales due to progressive interaction between the reducing hydrothermal fluids, the oxygenated atmosphere, and in some cases seawater. At Jinata Onsen, on Shikinejima Island, Japan, an intertidal, anoxic, iron-rich hot spring mixes with the oxygenated atmosphere and seawater over short spatial scales, creating a diversity of chemical potentials and redox pairs over a distance ~10 m. We characterized the geochemical conditions along the outflow of Jinata Onsen as well as the microbial communities present in biofilms, mats, and mineral crusts along its traverse via 16S rDNA amplicon and genome-resolved shotgun metagenomic sequencing. The microbial community changed significantly downstream as temperatures and dissolved iron concentrations decreased and dissolved oxygen increased. Near the spring source, biomass is limited relative to downstream, and primary productivity may be fueled by oxidation of ferrous iron and molecular hydrogen by members of the Zetaproteobacteria and Aquificae. Downstream, the microbial community is dominated by oxygenic Cyanobacteria. Cyanobacteria are abundant and active even at ferrous iron concentrations of ~150 μM, which challenges the idea that iron toxicity limited cyanobacterial expansion in Precambrian oceans. Several novel lineages of Bacteria are also present at Jinata Onsen, including previously uncharacterized members of the Chloroflexi and Caldithrichaeota phyla, positioning Jinata Onsen as a valuable site for future characterization of these clades.ImportanceHigh temperatures and reducing conditions allow hot springs to support microbial communities that are very different from those found elsewhere on the surface of the Earth today; in some ways, these environments and the communities they support can be similar to environments that existed on the early Earth and that may exist on other planets. Here, we describe a novel hot spring system where hot, iron-rich but oxygen-poor water flows into the ocean, supporting a range of unique microbial communities. Metagenomic sequencing recovered many novel microbial lineages, including deep-branching and uniquely thermotolerant members of known groups. Comparison of the biological communities in the upstream part of the hot spring, potentially supported by biological iron and hydrogen oxidizing metabolisms, to downstream microbial mats, supported by oxygenic photosynthesis, provides insight into the potential productivity of life during Proterozoic time and on other planets where oxygenic photosynthesis is not possible.

Carbon and other volatiles in the form of gases, fluids or mineral phases are transported from Earth's surface into the mantle at convergent margins, where the oceanic crust subducts beneath the continental crust. The efficiency of this transfer has profound implications for the nature and scale of geochemical heterogeneities in Earth's deep mantle and shallow crustal reservoirs, as well as Earth's oxidation state. However, the proportions of volatiles released from the forearc and backarc are not well constrained compared to fluxes from the volcanic arc front. Here we use helium and carbon isotope data from deeply sourced springs along two cross-arc transects to show that about 91 per cent of carbon released from the slab and mantle beneath the Costa Rican forearc is sequestered within the crust by calcite deposition. Around an additional three per cent is incorporated into the biomass through microbial chemolithoautotrophy, whereby microbes assimilate inorganic carbon into biomass. We estimate that between 1.2 × 108 and 1.3 × 1010 moles of carbon dioxide per year are released from the slab beneath the forearc, and thus up to about 19 per cent less carbon is being transferred into Earth's deep mantle than previously estimated.