Abstract
Eutrophication is expected to increase methane production in freshwater sediments worldwide over the coming decades. Methane-oxidizing bacteria (MOB) consume a significant fraction of this sedimentary methane, but the factors that control their distributions and activities are not understood. By combining genetic approaches (pmoA, 16S rRNA gene, metagenomics) with geochemical and sedimentological analyses, we investigate the role of trophic state, electron acceptors, oxygen (O2) and methane fluxes, and potential methylotrophic partner organisms in driving the distributions, abundances, and community compositions of MOB across five lakes in central Switzerland. Although methane fluxes were highest in the eutrophic lakes, methanotrophic abundances peaked in oxic and anoxic sediments of an oligotrophic lake. In all lakes, Type I gammaproteobacterial Methylococcaceae dominated oxic and suboxic bottom water and surface sediments, showing strong correlations with abundances of putatively methylotrophic Methylophilaceae, whereas Type II alphaproteobacterial Methylocystaceae increased in deeper, anoxic sediment layers. Methanotrophic bacteria belonging to the NC10 phylum were predominantly detected within denitrifying sediment of the oligotrophic lake, matching their presumed nitrite-dependent lifestyle. While dominant MOB taxa at the genus-level follow vertical distributions of different aerobic and anaerobic respiration reactions, trophic state at the time of sediment deposition was the best predictor of MOB community structure at the operational taxonomic unit (OTU) level. Elevated methane fluxes combined with low MOB abundances in surface sediments of eutrophic lakes, moreover, support the notion that in eutrophic lakes a major portion of sedimentary methane bypasses the biological methane filter and escapes to overlying water.
Highlights
IntroductionFreshwater lakes account for 6–16% of natural emissions of the greenhouse gas methane (CH4) to the atmosphere (Bastviken et al, 2004)
Across five lakes in central Switzerland that range in present-day trophic state from highly eutrophic to oligotrophic, and differ significantly in trophic histories, we observe the highest pmoA copy numbers and contributions of MOB to total microbial communities under oligotrophic conditions
This observation is remarkable given the higher methane fluxes in the eutrophic lakes and considering that O2 fluxes into sediments vastly exceed the amount required for complete mineralization of methane at most stations
Summary
Freshwater lakes account for 6–16% of natural emissions of the greenhouse gas methane (CH4) to the atmosphere (Bastviken et al, 2004). Most of this methane is biologically produced in lake sediments. Anthropogenic increases in nutrient inputs that enhance primary production and organic carbon loading (eutrophication), can increase methane emissions from lakes (Beaulieu et al, 2019). The more rapid depletion of these electron acceptors in lake sediments, combined with the higher OM availability, promotes microbial methane production (methanogenesis) (Fiskal et al, 2019) and results in increased sedimentary methane release under eutrophic conditions (Beaulieu et al, 2019; Sanches et al, 2019)
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