It has been shown that reactive soil minerals, specifically iron(III) (oxyhydr)oxides, can trap organic carbon in soils overlying intact permafrost, and may limit carbon mobilization and degradation as it is observed in other environments. However, the use of iron(III)-bearing minerals as terminal electron acceptors in permafrost environments, and thus their stability and capacity to prevent carbon mobilization during permafrost thaw, is poorly understood. We have followed the dynamic interactions between iron and carbon using a space-for-time approach across a thaw gradient in Abisko (Sweden), where wetlands are expanding rapidly due to permafrost thaw. We show through bulk (selective extractions, EXAFS) and nanoscale analysis (correlative SEM and nanoSIMS) that organic carbon is bound to reactive Fe primarily in the transition between organic and mineral horizons in palsa underlain by intact permafrost (41.8 ± 10.8 mg carbon per g soil, 9.9 to 14.8% of total soil organic carbon). During permafrost thaw, water-logging and O₂limitation lead to reducing conditions and an increase in abundance of Fe(III)-reducing bacteria which favor mineral dissolution and drive mobilization of both iron and carbon along the thaw gradient. By providing a terminal electron acceptor, this rusty carbon sink is effectively destroyed along the thaw gradient and cannot prevent carbon release with thaw.

Summary: Iron is the most abundant redox‐active metal in the Earth's crust. The one electron transfer between the two most common redox states, Fe(II) and Fe(III), plays a role in a huge range of environmental processes from mineral formation and dissolution to contaminant remediation and global biogeochemical cycling. It has been appreciated for more than a century that microorganisms can harness the energy of this Fe redox transformation for their metabolic benefit. However, this is most widely understood for anaerobic Fe(III)‐reducing or aerobic and microaerophilic Fe(II)‐oxidizing bacteria. Only in the past few decades have we come to appreciate that bacteria also play a role in the anaerobic oxidation of ferrous iron, Fe(II), and thus can act to form Fe(III) minerals in anoxic settings. Since this discovery, our understanding of the ecology of these organisms, their mechanisms of Fe(II) oxidation and their role in environmental processes has been increasing rapidly. In this article, we bring these new discoveries together to review the current knowledge on these environmentally important bacteria, and reveal knowledge gaps for future research.

Preservation of organic carbon (OC) in marine and terrestrial deposits is enhanced by bonding with reactive iron (Fe_R). Association of OC with Fe_R (OC‐Fe_R) provides physical protection and hinders microbiological degradation. Roughly 20% of all OC stored in unconsolidated marine sediments and 40% of all OC present in Quaternary terrestrial deposits is preserved as OC‐Fe_R, but this value varies from 10% to 80% across global depositional environments. Here, we provide a new assessment of global OC‐Fe_R burial rates in both marine and terrestrial environments, using published estimates of OC associated with Fe_R, carbon burial, and probabilistic modeling. We estimate the marine OC‐Fe_R sink between 31 and 70 Mt C yr⁻¹ (average 52 Mt C yr⁻¹), and the terrestrial OC‐Fe_R sink at between 146 and 917 Mt C yr⁻¹ (average 446 Mt C yr⁻¹). In marine environments, continental shelves (average 17 Mt C yr⁻¹) and deltaic/estuarine environments (average 11 Mg C yr⁻¹) are the primary settings of OC‐Fe_R burial. On land, croplands (279 Mt C yr⁻¹) and grasslands (121 Mt C yr⁻¹) dominate the OC‐Fe_R burial budget. Changes in the Earth system through geological time impact the OC‐Fe_R pools, particularly in marine settings. For example, periods of intense explosive volcanism may lead to increased net OC‐Fe_R burial in marine sediments. Our work highlights the importance of OC‐Fe_R in marine carbon burial and demonstrates how OC‐Fe_R burial rates may be an order of magnitude greater in terrestrial environments, but here OC‐Fe_R stocks are most sensitive to the anthropogenic impacts of climatic change.