Thermophilic Lithotrophy and Phototrophy in an Intertidal, Iron-rich, Geothermal Spring

Abstract

Hydrothermal systems, including terrestrial hot springs, contain diverse and systematic arrays of 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- and hydrogen-rich hot spring mixes with the oxygenated atmosphere and sulfate-rich seawater over short spatial scales, creating an enormous range of redox environments 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 amplicon and shotgun metagenomic sequencing. The microbial community changed significantly downstream as temperatures and dissolved iron concentrations dropped and dissolved oxygen rose. Near the spring source, primary productivity appears limited, and is fueled primarily by oxidation of ferrous iron and molecular hydrogen by members of the Zetaproteobacteria and Aquificae, while downstream the microbial community is dominated by oxygenic Cyanobacteria. At Jinata Onsen, Cyanobacteria are abundant and productive even at ferrous iron concentrations of ~150 μM, which challenges the idea that iron toxicity limited cyanobacterial expansion in the 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.

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