Preprints
https://doi.org/10.5194/bg-2023-174
https://doi.org/10.5194/bg-2023-174
29 Sep 2023
 | 29 Sep 2023
Status: this preprint is currently under review for the journal BG.

Crystalline Iron Oxides Stimulate Methanogenesis Under Sulfate Reducing Conditions in the Terrestrial Subsurface

Brandon C. Enalls, Mon Oo Yee, Amrita Bhattacharya, Kristine Cabugao Grace, Sara Gushgari-Doyle, Terry C. Hazen, and Romy Chakraborty

Abstract. Microbial methane production is intimately linked to the biogeochemical cycling of iron, sulfur, and carbon in sedimentary environments. Sulfate-reducing microbes often outcompete methanogens for shared substrates. However, in a prior study at our field site, the Oak Ridge Reservation Field Research Center (ORR FRC) in Oak Ridge, TN, we observed co-occurring sulfate reduction and methanogenesis at 100–150 cm depth where iron (Fe) oxides of varying crystallinities were also detected. Fe oxides are known to act as electron conduits for direct interspecies electron transport (DIET) between syntrophic partners and can connect the metabolisms of methanogens with syntrophic Fe-reducing microbes in nature. However, whether the nature of Fe oxides can influence electron transfer reactions between sulfate-reducing microbes and methanogens is less understood. In this study, we utilized a microbial community enriched from ORR FRC vadose zone sediment to demonstrate the effects of Fe oxides of varying crystallinities on sulfate reduction and methanogenesis. We hypothesized that more crystalline Fe oxides facilitate the co-existence of sulfate-reducers and methanogens. Communities enriched from subsurface sediments produced methane when amended with crystalline hematite but not when amended with the amorphous, short range-ordered (SRO) ferrihydrite. Furthermore, Fe reduction occurred only in incubations amended with SRO ferrihydrite, indicating how poorly crystalline Fe oxides potentially contribute to the dynamic redox nature of the subsurface sediments. Microbial communities enriched during these incubations were composed of several taxa commonly associated with iron and sulfate reduction, fermentation, and methanogenesis, consistent with our geochemical data. Overall, the results from this work deepen our understanding of the role of Fe oxides in extracellular electron transfer, thereby mediating anaerobic metabolisms in the terrestrial subsurface environment.

Brandon C. Enalls, Mon Oo Yee, Amrita Bhattacharya, Kristine Cabugao Grace, Sara Gushgari-Doyle, Terry C. Hazen, and Romy Chakraborty

Status: final response (author comments only)

Comment types: AC – author | RC – referee | CC – community | EC – editor | CEC – chief editor | : Report abuse
  • CC1: 'Comment on bg-2023-174', David Aromokeye, 01 Oct 2023
    • CC2: 'Reply on CC1', Brandon C Enalls, 05 Oct 2023
  • CC3: 'Comment on bg-2023-174', Liang Shi, 13 Oct 2023
  • RC1: 'Comment on bg-2023-174', Anonymous Referee #1, 06 Nov 2023
    • AC1: 'Reply on RC1', Brandon C Enalls, 03 Jan 2024
  • RC2: 'Comment on bg-2023-174', Anonymous Referee #2, 07 Nov 2023
    • AC2: 'Reply on RC2', Brandon C Enalls, 03 Jan 2024
Brandon C. Enalls, Mon Oo Yee, Amrita Bhattacharya, Kristine Cabugao Grace, Sara Gushgari-Doyle, Terry C. Hazen, and Romy Chakraborty
Brandon C. Enalls, Mon Oo Yee, Amrita Bhattacharya, Kristine Cabugao Grace, Sara Gushgari-Doyle, Terry C. Hazen, and Romy Chakraborty

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Short summary
Methanogenic and sulfate-reducing microbes compete for resources in sediments. At our field site, methanogens and sulfate reducers co-exist along with conductive iron oxides, which can transfer electrons between microbes, reducing resource limitation. We incubated microbes with iron oxides of varying crystallinities to test whether they stimulate simultaneous methane production and sulfate reduction. Our results highlight the direct influences mineralogy has on microbial biogeochemistry.
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