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Published August 14, 2019 | Submitted + Published + Supplemental Material
Journal Article Open

Geochemical and metagenomic characterization of Jinata Onsen, a Proterozoic-analog hot spring, reveals novel microbial diversity including iron-tolerant phototrophs and thermophilic lithotrophs

Abstract

Hydrothermal systems, including terrestrial hot springs, contain diverse geochemical conditions that vary over short spatial scales due to progressive interactions between 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 diverse chemical potentials and redox pairs over a distance of ~10 m. We characterized geochemical conditions along the outflow of Jinata Onsen as well as the microbial communities present in biofilms, mats, and mineral crusts along its traverse using 16S rRNA gene amplicon and genome-resolved shotgun metagenomic sequencing. Microbial communities significantly changed downstream as temperatures and dissolved iron concentrations decreased and dissolved oxygen increased. Biomass was more limited near the spring source than downstream, and primary productivity appeared to be fueled by the oxidation of ferrous iron and molecular hydrogen by members of Zetaproteobacteria and Aquificae. The microbial community downstream was 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 phyla Chloroflexi and Calditrichaeota, positioning Jinata Onsen as a valuable site for the future characterization of these clades.

Additional Information

© 2019 by Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received February 1, 2019; Accepted May 22, 2019; Published online August 14, 2019. LMW acknowledges support from NASA NESSF (#NNX16AP39H), NSF (#OISE 1639454), NSF GROW (#DGE 1144469), the Lewis and Clark Fund for Exploration and Field Research in Astrobiology, the ELSI Origins Network, and an Agouron Institute postdoctoral fellowship. WWF acknowledged the support of NASA Exobiology award #NNX16AJ57G and the Simons Foundation Collaboration on the Origins of Life. MN and YU acknowledge the support of the Japan Society for the Promotion of Science (JP17K14412, JP17H06105). Data availability: Raw 16S rRNA gene amplicon data, raw metagenomic sequence data, and MAGs have been uploaded and made publicly available on NCBI under Project Number PRJNA392119 (genome accession numbers are found in Table S6).

Attached Files

Published - 34_278.pdf

Submitted - 428698.full.pdf

Supplemental Material - 34_ME18091_1.pdf

Supplemental Material - media-1.docx

Supplemental Material - media-2.xls

Supplemental Material - media-3.xlsx

Supplemental Material - media-4.xlsx

Supplemental Material - media-5.pdf

Supplemental Material - media-6.pdf

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Additional details

Created:
August 19, 2023
Modified:
October 20, 2023