Rates and Microbial Players of Iron-Driven Anaerobic Oxidation of Methane in Methanic Marine Sediments

Abstract

The flux of methane, a potent greenhouse gas, from the seabed is largely controlled by anaerobic oxidation of methane (AOM) coupled to sulfate reduction (S-AOM) in the sulfate methane transition (SMT). S-AOM is estimated to oxidize 90% of the methane produced in marine sediments and is mediated by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria. An additional methane sink, i.e., iron oxide coupled AOM (Fe-AOM), has been suggested to be active in the methanic zone of marine sediments. Geochemical signatures below the SMT such as high dissolved iron, low to undetectable sulfate and high methane concentrations, together with the presence of iron oxides are taken as prerequisites for this process. So far, Fe-AOM has neither been proven in marine sediments nor have the governing key microorganisms been identified. Here, using a multidisciplinary approach, we show that Fe-AOM occurs in iron oxide-rich methanic sediments of the Helgoland Mud Area (North Sea). When sulfate reduction was inhibited, different iron oxides facilitated AOM in longterm sediment slurry incubations but manganese oxide did not. Especially magnetite triggered substantial Fe-AOM activity and caused an enrichment of ANME-2a archaea. Methane oxidation rates of 0.095 ± 0.03 nmol cm −3 d −1 attributable to Fe-AOM were obtained in short-term radiotracer experiments. The decoupling of AOM from sulfate reduction in the methanic zone further corroborated that AOM was iron oxide-driven below the SMT. Thus, our findings prove that Fe-AOM occurs in methanic marine sediments containing mineral-bound ferric iron and is a previously overlooked but likely important component in the global methane budget. This process has the potential to sustain microbial life in the deep biosphere.

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

“…There are indications for microbial iron reduction in the deep methanic zone highlighted by the detection of dissolved Fe 2+ in pore water [6][7][8][9][10][11][12][13]19]. Of the various microbial processes that could hypothetically fuel iron reduction in the deep methanic zone, iron oxide dependent anaerobic oxidation of methane (AOM) has been demonstrated [19]. Likewise, dissimilatory iron reduction is feasible but requires similar electron donors (acetate and H 2 ) as methanogenesis [20,21].…”

“…Previously, we investigated the Helgoland Mud Area (HMA) in the North Sea, which is characterized by high accumulation of fine-grained sediments with elevated Fe 2+ pore-water concentrations in the methanic zone [6,19,28]. We characterised the composition of the bio-available fraction of the organic matter utilized by the microbial communities therein [29].…”

Data report: solid-phase major and minor elements and iron and sulfur species in sediments of the Anholt Basin, Baltic Sea collected during IODP Expedition 347

“…The methane peak in the methanic zone of Unit VII coincides with high amounts of all Fe oxide fractions and pyrite (Figures F2, F3). Because Fe 2+ concentrations increase with depth throughout Unit VI, methane is potentially consumed by the anaerobic oxidation with Fe oxides (e.g., Egger et al, 2015bEgger et al, , 2017Aromokeye et al, 2020). The availability of pyrite at the Unit VII/VI boundary may indicate that sulfate and Fe oxides have been concurrently reduced during the anaerobic oxidation of methane, resulting in the formation of pyrite via metastable Fe monosulfides.…”

“…The abundance of Fe sulfides in anoxic sediments is mostly dependent on the availability of (1) pore water sulfide released during organoclastic sulfate reduction and through AOM with sulfate and, concomitantly, (2) pore water Fe released during organoclastic Fe oxide reduction and through Fe-mediated AOM as well as the content of reactive solid-phase Fe as scavengers for the produced pore water sulfide (e.g., Goldhaber and Kaplan, 1974;Jørgensen, 1977Jørgensen, , 1982Berner, 1984;Egger et al, 2015bEgger et al, , 2017Oni et al, 2015;Aromokeye et al, 2020). Via the accumulation of intermediate metastable Fe monosulfides (mackinawite and greigite) (Rickard, 1995), pyrite can be formed through the reaction of Fe monosulfides with sulfides (Rickard, 1997;Thiel et al, 2019), polysulfides, and S 0 (Berner, 1970;Rickard, 1975;Luther, 1991).…”

Enrichment of novelVerrucomicrobia, BacteroidetesandKrumholzibacteriain an oxygen-limited, methane- and iron-fed bioreactor inoculated with Bothnian Sea sediments

“…Iron oxides are globally distributed in marine costal sediments (4). Anaerobic oxidation of methane coupled to iron reduction (Fe-AOM) is hypothesized to account for elevated dissolved iron concentrations in methanic zones, particularly in the Baltic and Bothnian Sea, North Sea and Black Sea (4). However, despite strong biogeochemical evidence for Fe-AOM (5-7), this remains one of the least elucidated methane-cycling metabolisms.…”