Iron-Coupled Anaerobic Oxidation of Methane Performed by a Mixed Bacterial-Archaeal Community Based on Poorly Reactive Minerals

Abstract

Anaerobic oxidation of methane (AOM) was shown to reduce methane emissions by over 50% in freshwater systems, its main natural contributor to the atmosphere. In these environments iron oxides can become main agents for AOM, but the underlying mechanism for this process has remained enigmatic. By conducting anoxic slurry incubations with lake sediments amended with C-labeled methane and naturally abundant iron oxides the process was evidenced by significantC-enrichment of the dissolved inorganic carbon pool and most pronounced when poorly reactive iron minerals such as magnetite and hematite were applied. Methane incorporation into biomass was apparent by strong uptake of C into fatty acids indicative of methanotrophic bacteria, associated with increasing copy numbers of the functional methane monooxygenase pmoA gene. Archaea were not directly involved in full methane oxidation, but their crucial participation, likely being mediators in electron transfer, was indicated by specific inhibition of their activity that fully stopped iron-coupled AOM. By contrast, inhibition of sulfur cycling increasedC-methane turnover, pointing to sulfur species involvement in a competing process. Our findings suggest that the mechanism of iron-coupled AOM is accomplished by a complex microbe-mineral reaction network, being likely representative of many similar but hidden interactions sustaining life under highly reducing low energy conditions.

Gammaproteobacterial methanotrophs dominate methanotrophy in aerobic and anaerobic layers of boreal lake waters

“…lakes with a temporary or permanently anoxic hypolimnion) of the temperate zone strongly suggests that aerobic MOBs dominate CH 4 oxidation in both oxic and anoxic water layers (Biderre-Petit et al 2011, Blees et al 2014, Oswald et al 2015, 2016a. Aerobic MOBs were also recently seen to dominate anaerobic CH 4 oxidation in sub-arctic and temperate lake sediments (Bar-Or et al 2017, Martinez-Cruz et al 2017. Under oxygen limitation, MOBs may efficiently use the limited O 2 to activate CH 4 and are suggested to further support their metabolism by fermentation (Kaly uzhnaya et al 2013) or by anaerobic respiration using alternative EAs, i.e.…”

“…Recently, it has been suggested that in situ oxygen production by photosynthetic algae or episodic oxygen introduction, events from the surface waters (Blees et al 2014) could fuel MOBs in the anoxic waters. However, indirect evidence from lake sediments suggests that MOBs could also drive AOM independently of any external O 2 source (Bar-Or et al 2017, Martinez-Cruz et al 2017.…”

Microbial interactions in the anaerobic oxidation of methane: model simulations constrained by process rates and activity patterns

“…Subsequently anaerobic methanotrophic archaea (ANME) were visualized in sediments and shown to form multicelled aggregations with deltaproteobacteria bacteria, spanning from micron‐scale aggregates to mats covering meter‐scale reef‐like structures (Boetius et al, ; Orphan et al, ; Orphan et al, ; Michaelis et al, ). Since then, our understanding of the diversity of ANME archaea and bacteria involved in this process has expanded along with a growing list of terminal electron acceptors coupled to methane oxidation, including nitrate (Haroon et al, ; Raghoebarsing et al, ); iron and manganese (Beal et al, ; Ettwig et al, ; Barr‐Or et al, ); and humic acid analogs (Scheller et al, ).…”

Rates and pathways of CH4 oxidation in ferruginous Lake Matano, Indonesia

“…In some cases, SO 4 is present, but AOM appears partially or entirely decoupled from sulfate reduction (Beal, House, & Orphan, 2009;Gupta et al, 2013;Segarra, Comerford, Slaughter, & Joye, 2013;Segarra et al, 2015;Sivan, Antler, Turchyn, Marlow, & Orphan, 2014). Despite the growing number of reports on Fe-dependent CH 4 oxidation (Bar-Or et al, 2017;Cai et al, 2018;Egger et al, 2015;Ettwig et al, 2016;Fu et al, 2016;Gao et al, 2017;Nordi et al, 2013;Roland et al, 2018;Scheller, Yu, Chadwick, Mcglynn, & Orphan, 2016), the pathway remains unsubstantiated through pure culture experiments and its broader ecological importance is as yet unknown. Lake Matano, Sulawesi Island, Indonesia, is situated near the equator and hosts the largest, deepest, and oldest known ferruginous basin on Earth (Crowe, Jones, et al, 2008;.…”