Periodic Reporting for period 4 - MERIR (Methane related iron reduction processes in sediments: Hidden couplings and their significance for carbon and iron cycles)
Okres sprawozdawczy: 2023-10-01 do 2025-03-31
In many aquatic sediments, significant iron oxide reduction is observed deep below its expected redox zone, at the methanogenic zone. Sometimes, that methane related iron reduction (MERIR) is accompanied by decreases in the concentrations of methane, and can attenuate the release of this greenhouse gas to the atmosphere. This project aimed to: (1) Identify and quantify MERIR in various natural methanogenic sedimentary profiles, (2) Characterize the process mechanism, (3) Investigate the reactivity of various iron oxides, and the role of magnetite as an electron acceptor and as an authigenic byproduct, and (4) Compare the dominant MERIR types and mechanisms among the various environments.
We focused on two striking, yet unexplained phenomena observed in our preliminary study: (1) the active involvement of aerobic methanotrophs in the observed iron-coupled anaerobic oxidation of methane (Fe-AOM), and (2) the unusual reactivity of iron minerals toward reduction, and the potential precipitation of authigenic magnetite with its paleomagnetic implications.
Despite the considerable challenges of conducting field-based research across multiple continents during two years of COVID-related restrictions and an ongoing war, we successfully achieved all proposed objectives. The results are comprehensively presented in 16 manuscripts—13 published, one accepted, and two currently archived. These findings were presented in several invited talks, seminars, workshops and media releases. Unfortunately, the pandemic prevented the planned workshop and several associated outreach activities. I am deeply grateful to the ERC for their support, which made it possible to carry out this exciting and impactful research.
We focused on two striking, yet unexplained phenomena observed in our preliminary study: (1) the active involvement of aerobic methanotrophs in the observed iron-coupled anaerobic oxidation of methane (Fe-AOM), and (2) the unusual reactivity of iron minerals toward reduction, and the potential precipitation of authigenic magnetite with its paleomagnetic implications.
Despite the considerable challenges of conducting field-based research across multiple continents during two years of COVID-related restrictions and an ongoing war, we successfully achieved all proposed objectives. The results are comprehensively presented in 16 manuscripts—13 published, one accepted, and two currently archived. These findings were presented in several invited talks, seminars, workshops and media releases. Unfortunately, the pandemic prevented the planned workshop and several associated outreach activities. I am deeply grateful to the ERC for their support, which made it possible to carry out this exciting and impactful research.
Significant MERIR was observed in our marine and lacustrine profiles (Amiel et al., 2020; Elul et al., 2021; Yorshansky et al., 2022; Liang et al., 2022; Pellerin et al., 2022; Zemach et al., 2024; Rivlin et al., 2025). These profiles indicate reactivation and reduction of iron oxides in the methanogenic zone. The main iron reduction processes were quantified based on profiles, incubation experiments, advanced microbial work, diagenetic and bioenergetic models. The experiments used different manipulations, and usually also stable isotope probing and advanced measurements of the dissolved products, specific lipid compounds and DNA. They were conducted on sediments, enriched sediment cultures and pure cultures close to natural conditions.
We show that iron reduction can be coupled thermodynamically with the oxidation of acetate, hydrogen, methane and ammonium. Among the iron oxides, the reduction of amorphous iron oxyhydroxide and ferrihydrite are the most favorable reactions for generating biomass in the methanogenic sediments at both lacustrine and marine sites (Vigderovich et al., 2022; Lotem et al., 2023; Neumann Wallheimer et al., 2025; Rivlin et al., 2025). The comparison between both environments (WP4) in our bioenergetic model (Neumann Wallheimer et al., 2025) shows that the most probable iron oxide reduction process in our tested lake sites is hydrogen oxidation, followed by methane oxidation. On the other hand, in the diffusive controlled marine sites iron oxide reduction is most probably coupled to the oxidation of ammonium (Feammox) to molecular nitrogen but not to methane oxidation. Our model results fit nicely our observations, which show significant Fe-AOM in lake sediments (Elul et al., 2021; Vigderovich et al., 2022; Lotem et al., 2022; Vigderovich et al., 2023; Gafni et al., 2024) but not in marine sediments (Yorshansky et al., 2022; Liang et al., 2022; Rivlin et al., 2025), even when performed under high pressures (Liang et al., 2022).
The reduction of iron is performed by iron reducing bacteria, but surprisingly also by methanogens as methanosarcinalles (Elul et al., 2021). Eliani Russak et al. (2023) showed that pure cultures of Methanosarcinalles Barkeri can indeed reduce all natural iron oxides found in our sites close to the natural conditions (amorphous iron>goethite>magnetite> hematite). Moreover, this iron reduction inhibits methane production and increases with the addition of electron shuttles as phenazines, supporting the advantage of reducing iron by these methanogens thanks to their methanophenzines with known electron shuttling abilities (and fitting the measured metabolites).
The iron reduction by methane oxidation, shown in our lake sites, is performed by two mechanisms: 1) direct Fe-AOM the methanogens and 2) complex cryptic redox coupling between aerobic methanotrophs, iron reducing bacteria and methanogens. Our comprehensive studies from Lake Kinneret methanogenic sediments show that both mechanisms are significant in the sediments (Elul et al., 2021; Vigderovich et al., 2022) and responsible each to consume 5-8% of the produced methane (Vigderovich et al., 2022). In thermokarst lakes formed by permafrost thawing, it seems that the role of AOM is smaller and that it may not attenuate the increase in methanogenesis in a warming climate and aging of the lakes (Lotem et al., 2023; Gerera et al., 2025). Moreover, surprisingly, we observed methane net release also from dry upland permafrost thawing sites (Walter Anthony et al., 2024), even with active aerobic and anaerobic methane oxidation (Bergman et al., 2025), which should be further explored.
The co-appearance and survival of these aerobe and anaerobe microbes together in highly reduced lake sediment systems occur through complex fascinating interactions that need to be further investigated. They involve Mnammox, Feammox, dark oxygen production, fast consumption of the oxygen by methanotrophs and stimulation of iron reduction by the methanotrophs.
We also show that magnetite appears and can serve as an electron acceptor in both environments (Vigderovich et al., 2022; Rivlin et al., 2025) and in pure cultures (Eliani Russak et al., 2023). However, in terms of biomass production, it is much less favorable than amorphous iron and ferrihydrite (Neumann Wallheimer et al., 2025), which strengthens the need for iron recycling presented above. Iron reduction and recycling can involve also authigenic precipitation of magnetite. Indeed, our results from combined multi approaches (57Fe isotope labeling, metagenome and magnetic FORC and Verway transition) suggest its precipitation also as an authigenic byproduct in the methanogenic zone, with important implications to sedimentary magnetism (Amiel et al., 2020; Rivlin et al., 2025). Rivlin et al. (2025) emphasize the need to use multi approaches to obtain solid information regarding magnetite changes.
We show that iron reduction can be coupled thermodynamically with the oxidation of acetate, hydrogen, methane and ammonium. Among the iron oxides, the reduction of amorphous iron oxyhydroxide and ferrihydrite are the most favorable reactions for generating biomass in the methanogenic sediments at both lacustrine and marine sites (Vigderovich et al., 2022; Lotem et al., 2023; Neumann Wallheimer et al., 2025; Rivlin et al., 2025). The comparison between both environments (WP4) in our bioenergetic model (Neumann Wallheimer et al., 2025) shows that the most probable iron oxide reduction process in our tested lake sites is hydrogen oxidation, followed by methane oxidation. On the other hand, in the diffusive controlled marine sites iron oxide reduction is most probably coupled to the oxidation of ammonium (Feammox) to molecular nitrogen but not to methane oxidation. Our model results fit nicely our observations, which show significant Fe-AOM in lake sediments (Elul et al., 2021; Vigderovich et al., 2022; Lotem et al., 2022; Vigderovich et al., 2023; Gafni et al., 2024) but not in marine sediments (Yorshansky et al., 2022; Liang et al., 2022; Rivlin et al., 2025), even when performed under high pressures (Liang et al., 2022).
The reduction of iron is performed by iron reducing bacteria, but surprisingly also by methanogens as methanosarcinalles (Elul et al., 2021). Eliani Russak et al. (2023) showed that pure cultures of Methanosarcinalles Barkeri can indeed reduce all natural iron oxides found in our sites close to the natural conditions (amorphous iron>goethite>magnetite> hematite). Moreover, this iron reduction inhibits methane production and increases with the addition of electron shuttles as phenazines, supporting the advantage of reducing iron by these methanogens thanks to their methanophenzines with known electron shuttling abilities (and fitting the measured metabolites).
The iron reduction by methane oxidation, shown in our lake sites, is performed by two mechanisms: 1) direct Fe-AOM the methanogens and 2) complex cryptic redox coupling between aerobic methanotrophs, iron reducing bacteria and methanogens. Our comprehensive studies from Lake Kinneret methanogenic sediments show that both mechanisms are significant in the sediments (Elul et al., 2021; Vigderovich et al., 2022) and responsible each to consume 5-8% of the produced methane (Vigderovich et al., 2022). In thermokarst lakes formed by permafrost thawing, it seems that the role of AOM is smaller and that it may not attenuate the increase in methanogenesis in a warming climate and aging of the lakes (Lotem et al., 2023; Gerera et al., 2025). Moreover, surprisingly, we observed methane net release also from dry upland permafrost thawing sites (Walter Anthony et al., 2024), even with active aerobic and anaerobic methane oxidation (Bergman et al., 2025), which should be further explored.
The co-appearance and survival of these aerobe and anaerobe microbes together in highly reduced lake sediment systems occur through complex fascinating interactions that need to be further investigated. They involve Mnammox, Feammox, dark oxygen production, fast consumption of the oxygen by methanotrophs and stimulation of iron reduction by the methanotrophs.
We also show that magnetite appears and can serve as an electron acceptor in both environments (Vigderovich et al., 2022; Rivlin et al., 2025) and in pure cultures (Eliani Russak et al., 2023). However, in terms of biomass production, it is much less favorable than amorphous iron and ferrihydrite (Neumann Wallheimer et al., 2025), which strengthens the need for iron recycling presented above. Iron reduction and recycling can involve also authigenic precipitation of magnetite. Indeed, our results from combined multi approaches (57Fe isotope labeling, metagenome and magnetic FORC and Verway transition) suggest its precipitation also as an authigenic byproduct in the methanogenic zone, with important implications to sedimentary magnetism (Amiel et al., 2020; Rivlin et al., 2025). Rivlin et al. (2025) emphasize the need to use multi approaches to obtain solid information regarding magnetite changes.
1) Finding a complex aerobic and anaerobic microbial community that co-exists, interacts, performs Fe-AOM in methanogenic lake sediments and stimulates iron reduction. This is in cryptic cycles that can involved dark oxygen production.
2) Showing the significant effect of microbial iron reduction in methanogenic marine sediments on magnetic parameters.
3) Constraining methanogenesis and AOM rates in yedoma’s thermokarst lakes in the Arctic using combined short-term (using radioactive labeling) and long-term incubations.
4) Finding methane net release to the atmosphere from dry upland permafrost thawing sites, even with active aerobic and anaerobic methane oxidation.
5) Showing the ability of methanogens to reduce natural iron oxides in sediments.
2) Showing the significant effect of microbial iron reduction in methanogenic marine sediments on magnetic parameters.
3) Constraining methanogenesis and AOM rates in yedoma’s thermokarst lakes in the Arctic using combined short-term (using radioactive labeling) and long-term incubations.
4) Finding methane net release to the atmosphere from dry upland permafrost thawing sites, even with active aerobic and anaerobic methane oxidation.
5) Showing the ability of methanogens to reduce natural iron oxides in sediments.