Aerobic methane oxidation under copper scarcity in a stratified lake

Abstract

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.

Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

“…The availability of Cu as a co-factor of pMMO's active site can restrict enzymatic activity in MOB communities and thus limit their growth (Semrau et al, 2010(Semrau et al, , 2018. Previous work on the role of Cu for MOB in Rotsee has already established a likely role of Cu scarcity and competition for Cu in the lake (Guggenheim et al, 2019). The present work provides additional evidence for Cu as an important factor controlling MOB community assembly: we observed positive correlations of MOB with changing importance of Cu-species along the depth gradient of Rotsee.…”

“…Under these conditions Cu DGT and Cu Part correlated mostly with type Ia and Methylobacter OTUs (Figures 4, 5). It is thought that Cu DGT is the bioavailable Cu fraction, whereas Cu Part mainly represents Cu incorporated into biomass (Guggenheim et al, 2019). Cu DGT concentrations decrease substantially from the oxycline toward the oxidation zone (Supplementary Figure S1).…”

“…Such methane oxidation zones migrate within the water column as stratification progresses (Carini et al, 2005). Competitiveness under specific oxygen, methane, copper and iron concentrations can be a factor leading to MOB niche differentiation (Knief, 2015;Chidambarampadmavathy et al, 2017;Guggenheim et al, 2019;Mayr et al, 2019;Reis et al, 2020). This is thought to be partially coupled to the composition and property of the expressed methane monooxygenase (MMO), which initiates the methane oxidation process and exists in two main forms (Sirajuddin and Rosenzweig, 2015).…”

Lake mixing regime selects apparent methane oxidation kinetics of the methanotroph assemblage

“…Lakes are an important source of greenhouse gases; methane is a major contributor to the climate impact of the greenhouse gas emissions from lakes (DelSontro et al, 2018). The oxidation of the strong greenhouse gas methane in freshwater lakes is mainly achieved by methane-oxidizing bacteria (MOB), which have the unique ability to use methane as their sole carbon and energy source (Hanson and Hanson, 1996). In seasonally stratified lakes, large amounts of methane, which is produced as a final product of anaerobic organic matter degradation, can accumulate in the oxygen-depleted hypolimnion (Conrad, 2009;Steinsberger et al, 2017).…”

“…A subset of MOB encode the soluble MMO (sMMO) that has a lower methane affinity than pMMO and has been hypothesized to be used by MOB under high methane concentration conditions; this is due to the fact that MOB biomass is assumed to be higher under such conditions, leading to copper limitation and a switch to copper-free sMMO (Semrau et al, 2018). The abundance of the sMMO gene has been found to be low in Lake Rotsee (Guggenheim et al, 2019), but relative transcription between the epi-and hypolimnion has not been investigated so far.…”