Here, we present results from sediments collected in the Argentine Basin, a non-steady state depositional marine system characterized by abundant oxidized iron within methane-rich layers due to sediment reworking followed by rapid deposition. Our comprehensive inorganic data set shows that iron reduction in these sulfate and sulfide-depleted sediments is best explained by a microbially mediated process-implicating anaerobic oxidation of methane coupled to iron reduction (Fe-AOM) as the most likely major mechanism. Although important in many modern marine environments, iron-driven AOM may not consume similar amounts of methane compared with sulfate-dependent AOM. Nevertheless, it may have broad impact on the deep biosphere and dominate both iron and methane cycling in sulfate-lean marine settings. Fe-AOM might have been particularly relevant in the Archean ocean, >2.5 billion years ago, known for its production and accumulation of iron oxides (in iron formations) in a biosphere likely replete with methane but low in sulfate. Methane at that time was a critical greenhouse gas capable of sustaining a habitable climate under relatively low solar luminosity, and relationships to iron cycling may have impacted if not dominated methane loss from the biosphere.

Microorganisms in marine subsurface sediments substantially contribute to global biomass. Sediments warmer than 40°C account for roughly half the marine sediment volume, but the processes mediated by microbial populations in these hard-to-access environments are poorly understood. We investigated microbial life in up to 1.2-kilometer-deep and up to 120°C hot sediments in the Nankai Trough subduction zone. Above 45°C, concentrations of vegetative cells drop two orders of magnitude and endospores become more than 6000 times more abundant than vegetative cells. Methane is biologically produced and oxidized until sediments reach 80° to 85°C. In 100° to 120°C sediments, isotopic evidence and increased cell concentrations demonstrate the activity of acetate-degrading hyperthermophiles. Above 45°C, populated zones alternate with zones up to 192 meters thick where microbes were undetectable.

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.

The Cretaceous period (~145-65 m.y. ago) was characterized by intervals of enhanced organic carbon burial associated with increased primary production under greenhouse conditions. The global consequences of these perturbations, oceanic anoxic events (OAEs), lasted up to 1 m.y., but short-term nutrient and climatic controls on widespread anoxia are poorly understood. Here, we present a high-resolution reconstruction of oceanic redox and nutrient cycling as recorded in subtropical shelf sediments from Tarfaya, Morocco, spanning the initiation of OAE2. Iron-sulfur systematics and biomarker evidence demonstrate previously undescribed redox cyclicity on orbital time scales, from sulfidic to anoxic ferruginous (Fe-rich) water-column conditions. Bulk geochemical data and sulfur isotope modeling suggest that ferruginous conditions were not a consequence of nutrient or sulfate limitation, despite overall low sulfate concentrations in the proto-North Atlantic. Instead, fluctuations in the weathering influxes of sulfur and reactive iron, linked to a dynamic hydrological cycle, likely drove the redox cyclicity. Despite the potential for elevated phosphorus burial in association with Fe oxides under ferruginous conditions on the Tarfaya shelf, porewater sulfide generation drove extensive phosphorus recycling back to the water column, thus maintaining widespread open-ocean anoxia.