Anthropogenic and Environmental Constraints on the Microbial Methane Cycle in Coastal Sediments

Abstract

Large amounts of methane, a potent greenhouse gas, are produced in anoxic sediments by methanogenic archaea. Nonetheless, over 90% of the produced methane is oxidized via sulfate-dependent anaerobic oxidation of methane (S-AOM) in the sulfate-methane transition zone (SMTZ) by consortia of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). Coastal systems account for the majority of total marine methane emissions and typically have lower sulfate concentrations, hence S-AOM is less significant. However, alternative electron acceptors such as metal oxides or nitrate could be used for AOM instead of sulfate. The availability of electron acceptors is determined by the redox zonation in the sediment, which may vary due to changes in oxygen availability and the type and rate of organic matter inputs. Additionally, eutrophication and climate change can affect the microbiome, biogeochemical zonation, and methane cycling in coastal sediments. This review summarizes the current knowledge on the processes and microorganisms involved in methane cycling in coastal sediments and the factors influencing methane emissions from these systems. In eutrophic coastal areas, organic matter inputs are a key driver of bottom water hypoxia. Global warming can reduce the solubility of oxygen in surface waters, enhancing water column stratification, increasing primary production, and favoring methanogenesis. ANME are notoriously slow growers and may not be able to effectively oxidize methane upon rapid sedimentation and shoaling of the SMTZ. In such settings, ANME-2d (Methanoperedenaceae) and ANME-2a may couple iron- and/or manganese reduction to AOM, while ANME-2d and NC10 bacteria (Methylomirabilota) could couple AOM to nitrate or nitrite reduction. Ultimately, methane may be oxidized by aerobic methanotrophs in the upper millimeters of the sediment or in the water column. The role of these processes in mitigating methane emissions from eutrophic coastal sediments, including the exact pathways and microorganisms involved, are still underexplored, and factors controlling these processes are unclear. Further studies are needed in order to understand the factors driving methane-cycling pathways and to identify the responsible microorganisms. Integration of the knowledge on microbial pathways and geochemical processes is expected to lead to more accurate predictions of methane emissions from coastal zones in the future.

Keywords: climate change; eutrophication; greenhouse gases; marine microbiology; methane oxidation; methanogenesis; sediment.

FIGURE 1

Schematic presentation of microbial processes and microorganisms (left) and reaction equations with different electron acceptors (right) involved in methane cycling. N-AOM can couple either nitrate (ANME-2d) or nitrite (NC-10) to methane oxidation. MO, methane oxidation; N-AOM, nitrate/nitrite-dependent anaerobic oxidation of methane; Mn-AOM, manganese-dependent anaerobic oxidation of methane; Fe-AOM, iron-dependent anaerobic oxidation of methane; S-AOM, sulfate-dependent anaerobic oxidation of methane. References for the Gibbs free energies are the following: aerobic MO (Regnier et al., 2011), N-AOM (In’ t Zandt et al., 2018), Mn-AOM and Fe-AOM (Sturm et al., 2019), and S-AOM (Meulepas et al., 2010).

FIGURE 2

The effect of eutrophication on the depth of the sulfate-methane transition zone (SMTZ) in coastal sediment and the potential for Fe-AOM. Upon increase of organic matter load, the depth of sulfate penetration decreases due to organic matter degradation coupled to sulfate reduction. This shifts the SMTZ upward and allows the presence of iron oxides at deeper depths, creating a niche for Fe-AOM. Fe-AOM, iron-dependent anaerobic oxidation of methane; S-AOM, sulfate-dependent anaerobic oxidation of methane.