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

Ward, Lewis M. and Idei, Airi and Nakagawa, Mayuko and Ueno, Yuichiro and Fischer, Woodward W. and McGlynn, Shawn E. (2019) Geochemical and metagenomic characterization of Jinata Onsen, a Proterozoic-analog hot spring, reveals novel microbial diversity including iron-tolerant phototrophs and thermophilic lithotrophs. Microbes and Environments . ISSN 1342-6311. (In Press) http://resolver.caltech.edu/CaltechAUTHORS:20190130-121936697

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1264/jsme2.ME19017DOIArticle
https://doi.org/10.1101/428698DOIDiscussion Paper
ORCID:
AuthorORCID
Ward, Lewis M.0000-0002-9290-2567
Fischer, Woodward W.0000-0002-8836-3054
McGlynn, Shawn E.0000-0002-8199-7011
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. 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).
Funders:
Funding AgencyGrant Number
NASA Earth and Space Science FellowshipNNX16AP39H
NSFOISE-1639454
NSF Graduate Research FellowshipDGE-1144469
Lewis and Clark Fund for Exploration and Field Research in AstrobiologyUNSPECIFIED
ELSI Origins NetworkUNSPECIFIED
Agouron InstituteUNSPECIFIED
NASANNX16AJ57G
Simons FoundationUNSPECIFIED
Japan Society for the Promotion of Science (JSPS)JP17K14412
Japan Society for the Promotion of Science (JSPS)JP17H06105
Subject Keywords:geomicrobiology, Proterozoic, microaerobic, astrobiology, ferruginous, thermophiles
Record Number:CaltechAUTHORS:20190130-121936697
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190130-121936697
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92524
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:31 Jan 2019 00:15
Last Modified:19 Aug 2019 17:01

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