Microbial Fe(III) oxide reduction potential in Chocolate Pots hot spring, Yellowstone National Park

Abstract

Chocolate Pots hot springs (CP) is a unique, circumneutral pH, iron-rich, geothermal feature in Yellowstone National Park. Prior research at CP has focused on photosynthetically driven Fe(II) oxidation as a model for mineralization of microbial mats and deposition of Archean banded iron formations. However, geochemical and stable Fe isotopic data have suggested that dissimilatory microbial iron reduction (DIR) may be active within CP deposits. In this study, the potential for microbial reduction of native CP Fe(III) oxides was investigated, using a combination of cultivation dependent and independent approaches, to assess the potential involvement of DIR in Fe redox cycling and associated stable Fe isotope fractionation in the CP hot springs. Endogenous microbial communities were able to reduce native CP Fe(III) oxides, as documented by most probable number enumerations and enrichment culture studies. Enrichment cultures demonstrated sustained DIR driven by oxidation of acetate, lactate, and H2 . Inhibitor studies and molecular analyses indicate that sulfate reduction did not contribute to observed rates of DIR in the enrichment cultures through abiotic reaction pathways. Enrichment cultures produced isotopically light Fe(II) during DIR relative to the bulk solid-phase Fe(III) oxides. Pyrosequencing of 16S rRNA genes from enrichment cultures showed dominant sequences closely affiliated with Geobacter metallireducens, a mesophilic Fe(III) oxide reducer. Shotgun metagenomic analysis of enrichment cultures confirmed the presence of a dominant G. metallireducens-like population and other less dominant populations from the phylum Ignavibacteriae, which appear to be capable of DIR. Gene (protein) searches revealed the presence of heat-shock proteins that may be involved in increased thermotolerance in the organisms present in the enrichments as well as porin-cytochrome complexes previously shown to be involved in extracellular electron transport. This analysis offers the first detailed insight into how DIR may impact the Fe geochemistry and isotope composition of a Fe-rich, circumneutral pH geothermal environment.

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

“…This is in contrast to other iron-rich, neutral pH systems including hot and cold springs and groundwater seeps (e.g., Blöthe & Roden, 2009;Fortney et al, 2016;Hegler et al, 2012;Roden et al, 2012). This may partially reflect the relative fluxes of iron oxidation versus organic carbon fixation at OHK; that is, there is insufficient organic carbon being fixed in this environment to fuel substantial iron oxide respiration.…”

“…The majority of Chlorobi sequences found in OHK appear to fall within the Chlorobi order Ignavibacteria, a basal clade of Chlorobi whose known members include versatile heterotrophic metabolisms but no known phototrophy pathways (Iino et al, 2010;Liu, Frigaard et al, 2012). Ignavibacteria appear to be a common component of hot spring microbial communities: these organisms were first isolated from a Japanese hot spring (Iino et al, 2010) and are found at high abundance in Chocolate Pots hot springs in Yellowstone National Park (Fortney et al, 2016). Ignavibacteria appear to be a common component of hot spring microbial communities: these organisms were first isolated from a Japanese hot spring (Iino et al, 2010) and are found at high abundance in Chocolate Pots hot springs in Yellowstone National Park (Fortney et al, 2016).…”

Dual Role of Humic Substances As Electron Donor and Shuttle for Dissimilatory Iron Reduction

“…Experiments with HM and/or glucose had PCC genes mainly assigned to Geobacter and Geothrix, whereas HA reactors had increases in Ignavibacterium/Melioribacter related taxa. The latter taxa are known to be capable of fermentative growth with polysaccharides as well as DIR; 22,23,59 thus the presence of both PCC and CAZyme genes (see Figure 3) attributable to these organisms in the HA cultures suggests that they played a role both in DIR and upstream production of fermentation end-products that served as substrates for DIR. It is notable that our findings reveal for the first time that the previously described DIRB Geothrix 60 contains PCC gene systems for reduction of extracellular electron acceptors (see SI Figure S1 and Supporting Text 1).…”

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

“…The relatively high concentrations of dissolved organic carbon (DOC) measured in Pool 1 (∼1.3 mM) may stimulate heterotrophic activity by the microbial community at Jinata, coupled to aerobic or anaerobic respiration (such as dissimilatory iron reduction, as observed in other iron-rich hot springs, e.g. 33), resulting in the drawdown of DOC downstream. The source of this DOC is unclear; future work will be necessary to determine whether DOC is present in the source water or if it is produced in situ by the microbial community in the Source Pool and Pool 1.…”