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Lakes are a significant source of atmospheric methane, although methane-oxidizing bacteria consume most methane diffusing upward from anoxic sediments. Diverse methane-oxidizing bacteria form an effective methane filter in the water column of stratified lakes, yet, niche partitioning of different methane-oxidizing bacteria along the oxygen–methane counter gradient remains poorly understood. In our study, we reveal vertical distribution patterns of active methane-oxidizing bacteria along the oxygen–methane counter gradient of four lakes, based on amplicon sequencing analysis of 16S rRNA and pmoA genes, and 16S rRNA and pmoA transcripts, and potential methane oxidation rates. Differential distribution patterns indicated that ecologically different methane-oxidizing bacteria occupied the methane-deficient and oxygen-deficient part above and below the oxygen–methane interface. The interface sometimes harbored additional taxa. Within the dominant Methylococcales, an uncultivated taxon (CABC2E06) occurred mainly under methane-deficient conditions, whereas Crenothrix-related taxa preferred oxygen-deficient conditions. Candidatus Methylomirabilis limnetica (NC10 phylum) abundantly populated the oxygen-deficient part in two of four lakes. We reason that the methane filter in lakes is structured and that methane-oxidizing bacteria may rely on niche-specific adaptations for methane oxidation along the oxygen–methane counter gradient. Niche partitioning of methane-oxidizing bacteria might support greater overall resource consumption, contributing to the high effectivity of the lacustrine methane filter.

Aerobic methane-oxidizing bacteria (MOB) substantially reduce methane fluxes from freshwater sediments to the atmosphere. Their metalloenzyme methane monooxygenase (MMO) catalyses the first oxidation step converting methane to methanol. Its most prevalent form is the copper-dependent particulate pMMO, however, some MOB are also able to express the iron-containing, soluble sMMO under conditions of copper scarcity. So far, the link between copper availability in different forms and biological methane consumption in freshwater systems is poorly understood. Here, we present high-resolution profiles of MOB abundance and pMMO and sMMO functional genes in relation to copper, methane and oxygen profiles across the oxic-anoxic boundary of a stratified lake. We show that even at low nanomolar copper concentrations, MOB species containing the gene for pMMO expression are present at high abundance. The findings highlight the importance of copper as a micronutrient for MOB species and the potential usage of copper acquisition strategies, even under conditions of abundant iron, and shed light on the spatial distribution of these microorganisms.