Abstract
Methanotrophs are of major importance in limiting methane emissions from lakes. They are known to preferably inhabit the oxycline of stratified water columns, often assumed due to an intolerance to atmospheric oxygen concentrations, but little is known on the response of methanotrophs to different oxygen concentrations as well as their preference for different electron acceptors. In this study, we enriched a methanotroph of the Methylobacter genus from the oxycline and the anoxic water column of a stratified lake, which was also present in the oxic water column in the winter. We tested the response of this Methylobacter-dominated enrichment culture to different electron acceptors, i.e., oxygen, nitrate, sulfate, and humic substances, and found that, in contrast to earlier results with water column incubations, oxygen was the preferred electron acceptor, leading to methane oxidation rates of 45–72 pmol cell−1 day−1. Despite the general assumption of methanotrophs preferring microaerobic conditions, methane oxidation was most efficient under high oxygen concentrations (>600 μM). Low (<30 μM) oxygen concentrations still supported methane oxidation, but no methane oxidation was observed with trace oxygen concentrations (<9 μM) or under anoxic conditions. Remarkably, the presence of nitrate stimulated methane oxidation rates under oxic conditions, raising the methane oxidation rates by 50% when compared to oxic incubations with ammonium. Under anoxic conditions, no net methane consumption was observed; however, methanotroph abundances were two to three times higher in incubations with nitrate and sulfate compared to anoxic incubations with ammonium as the nitrogen source. Metagenomic sequencing revealed the absence of a complete denitrification pathway in the dominant methanotroph Methylobacter, but the most abundant methylotroph Methylotenera seemed capable of denitrification, which can possibly play a role in the enhanced methane oxidation rates under nitrate-rich conditions.
Highlights
Methane is the second most important greenhouse gas on earth, and a direct reduction in methane emissions is needed to keep global temperatures below the goal of 1.5◦C above pre-industrial levels (Rogelj et al, 2018)
The most abundant methanotroph of Lacamas Lake, a seasonally stratified lake, is a Methylobacter species; it was detected in the oxic water column in the winter and in the microoxic oxycline and the anoxic hypolimnion in the summer
Most bacteria falling in the Methylobacter group are known as aerobic methanotrophs, it has recently been suggested that specific species contain the genomic potential to perform anaerobic methane oxidation, or methane oxidation under strong oxygen limitation, by coupling methane oxidation to nitrate reduction (Svenning et al, 2011; Smith et al, 2018) or by using a fermentation pathway
Summary
Methane is the second most important greenhouse gas on earth, and a direct reduction in methane emissions is needed to keep global temperatures below the goal of 1.5◦C above pre-industrial levels (Rogelj et al, 2018). A consortium of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria using sulfate as the electron acceptor for methane oxidation is responsible for this process (Boetius et al, 2000). Methane-oxidizing bacteria (MOB) are often detected in freshwater systems, at the oxic–anoxic interface and, more rarely, in the anoxic water column (e.g., Rudd and Hamilton, 1975; Harrits and Hanson, 1980; Biderre-Petit et al, 2011; Blees et al, 2014; Milucka et al, 2015; Oswald et al, 2016; Michaud et al, 2017). Organic matter and humic substances, which are shown to be able to function as both an electron donor and acceptor (Lovley et al, 1996; Klüpfel et al, 2014; Valenzuela et al, 2019), have been suggested to play a role in AOM in lakes (Saxton et al, 2016; Reed et al, 2017), but have so far only been shown to impact aquatic AOM performed by ANME in marine (Scheller et al, 2016) and tropical wetland systems (Valenzuela et al, 2017, 2019)
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