Microbial diversity and iron oxidation at Okuoku‐hachikurou Onsen, a Japanese hot spring analog of Precambrian iron formations

Abstract

Banded iron formations (BIFs) are rock deposits common in the Archean and Paleoproterozoic (and regionally Neoproterozoic) sedimentary successions. Multiple hypotheses for their deposition exist, principally invoking the precipitation of iron via the metabolic activities of oxygenic, photoferrotrophic, and/or aerobic iron‐oxidizing bacteria. Some isolated environments support chemistry and mineralogy analogous to processes involved in BIF deposition, and their study can aid in untangling the factors that lead to iron precipitation. One such process analog system occurs at Okuoku‐hachikurou (OHK) Onsen in Akita Prefecture, Japan. OHK is an iron‐ and CO2‐rich, circumneutral hot spring that produces a range of precipitated mineral textures containing fine laminae of aragonite and iron oxides that resemble BIF fabrics. Here, we have performed 16S rRNA gene amplicon sequencing of microbial communities across the range of microenvironments in OHK to describe the microbial diversity present and to gain insight into the cycling of iron, oxygen, and carbon in this ecosystem. These analyses suggest that productivity at OHK is based on aerobic iron‐oxidizing Gallionellaceae. In contrast to other BIF analog sites, Cyanobacteria, anoxygenic phototrophs, and iron‐reducing micro‐organisms are present at only low abundances. These observations support a hypothesis where low growth yields and the high stoichiometry of iron oxidized per carbon fixed by aerobic iron‐oxidizing chemoautotrophs like Gallionellaceae result in accumulation of iron oxide phases without stoichiometric buildup of organic matter. This system supports little dissimilatory iron reduction, further setting OHK apart from other process analog sites where iron oxidation is primarily driven by phototrophic organisms. This positions OHK as a study area where the controls on primary productivity in iron‐rich environments can be further elucidated. When compared with geological data, the metabolisms and mineralogy at OHK are most similar to specific BIF occurrences deposited after the Great Oxygenation Event, and generally discordant with those that accumulated before it.

Phototrophic Methane Oxidation in a Member of the Chloroflexi Phylum

“…Hydroxylamine could rapidly react with dissolved Fe 2+ found in the environment from which Ca. C. photoalkanotrophicum was recovered (Ward et al 2017a), but this organism also encodes genes for cytochrome c552 nitrite reductase which is capable of reducing hydroxylamine to ammonia (Einsle et al 1999); genes for this enzyme appear to have been acquired via HGT, and may be an adaptation to avoid hydroxylamine toxicity due to incidental ammonia oxidation-a strategy observed in some denitrifying methanotrophs (e.g. Skennerton et al 2015).…”

“…The metagenome-assembled genome described here was derived from shotgun metagenomic sequencing of microbial communities of Okuoku-hachikurou Onsen (OHK) in Akita, Prefecture, Japan. OHK is an iron-carbonate hot spring (Takashima et al 2011, Ward et al 2017a). This spring is remarkable for its unique iron-oxidizing microbial community and the accumulation of iron-rich tufa (authigenic mineral cement) that has some textural features in common with sedimentary iron formations deposited during Precambrian time (Ward et al 2017a).…”

“…OHK is an iron-carbonate hot spring (Takashima et al 2011, Ward et al 2017a). This spring is remarkable for its unique iron-oxidizing microbial community and the accumulation of iron-rich tufa (authigenic mineral cement) that has some textural features in common with sedimentary iron formations deposited during Precambrian time (Ward et al 2017a). In brief, the geochemistry of OHK derives from source waters supersaturated in CO 2 , anoxic, pH 6.8, ~45 °C, and containing ~22 Samples for shotgun metagenomic sequencing were collected in September 2016 from the "Shallow Source" and "Canal" sites described in (Ward et al 2017a).…”

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

“…Hot springs, with their varied chemical compositions, provide reservoirs of novel microbial diversity, where environmental and geochemical conditions select for lineages and metabolisms distinct from other Earth-surface environments (e.g. 4, 10, 28, 130, 131). In addition to their value as sources of microbial diversity, hot springs also provide valuable test beds for understanding microbial community processes driven by different suites of metabolisms (e.g.…”

“…In contrast to most surface ecosystems which are fueled almost entirely by oxygenic photosynthesis by plants, algae, and Cyanobacteria, hot spring microbial communities are commonly supported by lithotrophic or anoxygenic phototrophic organisms that derive energy and electrons for carbon fixation by oxidizing geologically sourced electron donors such as Fe 2+ , sulfide, arsenite, and molecular hydrogen (e.g. 36, 65, 71, 109, 130). These communities may therefore provide insight into the function of microbial communities on the early Earth or other planets, in which oxygenic photosynthesis may be absent or less significant and anoxygenic photosynthetic or lithotrophic metabolisms may play a larger role, resulting in overall lower rates of primary productivity (e.g.…”