Methane oxidation in the waters of a humic-rich boreal lake stimulated by photosynthesis, nitrite, Fe(III) and humics

Abstract

Abstract. Small boreal lakes are known to contribute significantly to global CH4 emissions. Lake Lovojärvi is a eutrophic lake in southern Finland with bottom water CH4 concentrations up to 2 mM. However, the surface water concentration, and thus the diffusive emission potential, was low (< 0.5 µM). We studied the biogeochemical processes involved in CH4 removal by chemical profiling and through incubation experiments. δ13C-CH4 profiling of the water column revealed a methane-oxidation hotspot just below the oxycline and zones of CH4 oxidation within the anoxic water column. In incubation experiments involving the addition of light and/or oxygen, CH4 oxidation rates in the anoxic hypolimnion were enhanced 3-fold, suggesting a major role for photosynthetically fueled aerobic CH4 oxidation. We observed a distinct peak in CH4 concentration at the chlorophyll-a maximum, caused by either in situ CH4 production or other CH4 inputs such as lateral transport from the littoral zone. In the dark anoxic water column at 7 m depth, nitrite seemed to be the key electron acceptor involved in CH4 oxidation, yet additions of Fe(III), anthraquinone-2,6-disulfonate and humic substances also stimulated anoxic CH4 oxidation. Surprisingly, nitrite seemed to inhibit CH4 oxidation at all other depths. Overall, this study shows that photosynthetically fueled CH4 oxidation can be a key process in CH4 removal in the water column of humic, turbid lakes, thereby limiting diffusive CH4 emissions from boreal lakes. Yet, it also highlights the potential importance of a whole suite of alternative electron acceptors, including humics, in these freshwater environments in the absence of light and oxygen.

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

“…Methane being a limiting factor only when oxygen is abundant enough to be potentially inhibiting also suggests that electron acceptors could be a limiting factor for CH 4 oxidation in the lower layers of the studied lakes. This limitation in electron acceptors in CH 4 -rich waters has been suggested by several studies where experimental addition of O 2 or alternative electron acceptors in anoxic water as well as oxygenic photosynthesis have increased CH 4 oxidation rates (Milucka et al, 2015;Oswald et al, 2015Oswald et al, , 2016van Grinsven et al, 2021). Whereas not necessarily related to abundance, these studies showed that the lack of electron acceptors could limit MO metabolism.…”

Redox Zone and Trophic State as Drivers of Methane-Oxidizing Bacterial Abundance and Community Structure in Lake Sediments

“…In addition, several gammaproteobacterial genera (e.g., Methylomonas, Methylobacter, Methylomicrobium) have been shown to directly couple methane oxidation to denitrification under O 2 -limiting conditions (Kits et al, 2015b;Cao et al, 2019;van Grinsven et al, 2020a). Recently, stimulation of bacterial methane oxidation rates by iron (III), manganese (IV), and humic compounds has been shown (Oswald et al, 2016;He et al, 2021;van Grinsven et al, 2021) and that certain strains of Methylomonas (Gammaproteobacteria) and Methylosinus (Alphaproteobacteria) can use ferrihydrite minerals as electron acceptors to oxidize methane (Zheng et al, 2020).…”

Environmental predictors of electroactive bacterioplankton in small boreal lakes

“…Only eight out of 5569 MAGs analyzed here were predicted to encode machinery for methanogenesis, among only 21 archaeal MAGs that passed the quality cutoffs. This, along with dissolved methane measurements in similar systems (Rissanen et al ., 2021; van Grinsven et al ., 2021), suggests that the majority of methanogenesis is occurring in sediments rather than the water column. The observed correlation between iron and methane, both of which are negatively correlated with dissolved oxygen (DO) (Fig 2B), is unsurprising because methanogenesis occurs typically when available iron and other electron acceptors are in the reduced state and Fe(II) is more soluble than Fe(III).…”