Anaerobic methane oxidation in a coastal oxygen minimum zone: spatial and temporal dynamics

Abstract

Summary Coastal waters are a major source of marine methane to the atmosphere. Particularly high concentrations of this potent greenhouse gas are found in anoxic waters, but it remains unclear if and to what extent anaerobic methanotrophs mitigate the methane flux. Here we investigate the long‐term dynamics in methanotrophic activity and the methanotroph community in the coastal oxygen minimum zone (OMZ) of Golfo Dulce, Costa Rica, combining biogeochemical analyses, experimental incubations and 16S rRNA gene sequencing over 3 consecutive years. Our results demonstrate a stable redox zonation across the years with high concentrations of methane (up to 1.7 μmol L−1) in anoxic bottom waters. However, we also measured high activities of anaerobic methane oxidation in the OMZ core (rate constant, k, averaging 30 yr−1 in 2018 and 8 yr−1 in 2019–2020). The OPU3 and Deep Sea‐1 clades of the Methylococcales were implicated as conveyors of the activity, peaking in relative abundance 5–25 m below the oxic–anoxic interface and in the deep anoxic water respectively. Although their genetic capacity for anaerobic methane oxidation remains unexplored, their sustained high relative abundance indicates an adaptation of these clades to the anoxic, methane‐rich OMZ environment, allowing them to play major roles in mitigating methane fluxes.

Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin

“…(Knittel and Boetius, 2009; Wallenius et al ., 2021). In Lake Grevelingen, the bottom water methane concentration was 73 μM, which is up to 100-fold higher than found in comparable ecosystems ((Borges et al ., 2016; Matoušů et al ., 2017; Steinsdóttir et al ., 2022). Here, methane production outpaces methane consumption, likely because of the high sedimentation rate in the Scharendjike basin (∼13 cm yr -1 (Egger et al ., 2016)).…”

“…Nitrate-dependent methanotrophic archaea ( Methanoperedens) were also present in the hypoxic zone at 35 m, which implies a potential for anaerobic removal of methane. However, we estimate the contribution to methane removal by Methanoperedens compared to MOBs to be low, as the abundance of archaea in the water column is 100 times lower than the abundance of bacteria (Thamdrup et al ., 2019; Steinsdóttir et al ., 2022). Overall, the methane-oxygen counter-gradient coinciding with the abundance peak of MOB strongly indicates that an active biofilter is effective in removing a large proportion of the high bottom water methane concentrations and thereby lowers total methane emission to the atmosphere.…”

“…Gamma-MOB can oxidize methane under virtually anoxic conditions, (e.g. by using alternative electron acceptors) (van Grinsven et al ., 2020; Steinsdóttir et al ., 2022). Some aerobic methanotrophs can use e.g.…”

“…Methylomonadaceae under anoxic conditions in sediments and the water column of other aquatic ecosystems (Oswald et al, 2016;Steinsdóttir et al, 2022), the stable isotope signatures of the methane profiles in Lake Grevelingen do not indicate high in situ activity of anaerobic methane removal in the anoxic bottom water (Żygadłowska et al, 2022). However, the surviving strategies of MOB during, and their ability to re-activate methane oxidation after exposure to anoxia is potentially an important feature to mitigate methane emissions during water column turnover (Blees et al, 2014;Mayr, Zimmermann, Dey, et al, 2020).…”

“…The efficiency of this so-called methane-oxidation filter in the sediment can vary over the season and may lead to high benthic CH 4 fluxes (Egger et al ., 2016) and elevated methane concentrations in the water column of hypoxic, stratified coastal waters (Steinle et al ., 2015; Myllykangas et al ., 2020; Martins et al ., 2022). If methane is leaking from the sediment to the bottom water, an active microbial biofilter in the water column can further mitigate methane emissions to the atmosphere, as demonstrated for other coastal ecosystems (Pack et al ., 2015; Matoušů et al ., 2017; Steinsdóttir et al ., 2022).…”