Methane oxidation coupled to oxygenic photosynthesis in anoxic waters

Abstract

Freshwater lakes represent large methane sources that, in contrast to the Ocean, significantly contribute to non-anthropogenic methane emissions to the atmosphere. Particularly mixed lakes are major methane emitters, while permanently and seasonally stratified lakes with anoxic bottom waters are often characterized by strongly reduced methane emissions. The causes for this reduced methane flux from anoxic lake waters are not fully understood. Here we identified the microorganisms and processes responsible for the near complete consumption of methane in the anoxic waters of a permanently stratified lake, Lago di Cadagno. Interestingly, known anaerobic methanotrophs could not be detected in these waters. Instead, we found abundant gamma-proteobacterial aerobic methane-oxidizing bacteria active in the anoxic waters. In vitro incubations revealed that, among all the tested potential electron acceptors, only the addition of oxygen enhanced the rates of methane oxidation. An equally pronounced stimulation was also observed when the anoxic water samples were incubated in the light. Our combined results from molecular, biogeochemical and single-cell analyses indicate that methane removal at the anoxic chemocline of Lago di Cadagno is due to true aerobic oxidation of methane fuelled by in situ oxygen production by photosynthetic algae. A similar mechanism could be active in seasonally stratified lakes and marine basins such as the Black Sea, where light penetrates to the anoxic chemocline. Given the widespread occurrence of seasonally stratified anoxic lakes, aerobic methane oxidation coupled to oxygenic photosynthesis might have an important but so far neglected role in methane emissions from lakes.

Methanotrophy under Versatile Conditions in the Water Column of the Ferruginous Meromictic Lake La Cruz (Spain)

“…Such photosynthesis-linked MO has been observed in other shallow lake systems with deep light penetration (Milucka et al, 2015; Oswald et al, 2015; Brand et al, 2016) and seems to be a plausible explanation for aerobic MO in the anoxic parts of Lake La Cruz. Laboratory and field evidence suggests that the lower PAR threshold for oxygenic photosynthesis in freshwater is 0.09 μE m −2 s −1 (Gibson, 1985) to 0.34 μE m −2 s −1 (Brand et al, 2016), respectively.…”

“…The first three were most closely related to uncultured species from other freshwater lakes, reservoirs, and sediments: Lake Mizugaki (Kojima et al, 2009; Tsutsumi et al, 2011), Feitsui Reservoir (Kojima et al, 2014), Lake Cadagno (Milucka et al, 2015), Lake Kinneret (Junier et al, 2010), Lake Schoehsee (unpublished), Lake Constance (Pester et al, 2004), and lakes on the Yunnan Plateau (Liu et al, 2015). The fourth cluster was closely related to an uncultured Methylococcus species from a wetland in northeast China (Yun et al, 2013) and an uncultured bacterium from lake sediments (Liu et al, 2015).…”

“…However, MO in the absence of detectable O 2 coinciding with populations of predominantly aerobic MOB below the oxycline has been reported for several stratified lakes (Schubert et al, 2010; Biderre-Petit et al, 2011; Blees et al, 2014; Oswald et al, 2016). In shallow lakes with light penetration below the oxycline, aerobic MO may be coupled to in situ production of oxygen by photosynthesis (Milucka et al, 2015; Oswald et al, 2015; Brand et al, 2016). Additionally, MO (by facultative aerobic MOB) may be coupled to denitrification under oxygen limitation (Kits et al, 2015a,b).…”

Exceptional summer warming leads to contrasting outcomes for methane cycling in small Arctic lakes of Greenland

“…Under warm conditions in 2012, not only were CH 4 concentrations in sediments and anoxic waters elevated but the percentage of CH 4 oxidized was also higher. Several studies suggest that MOx is important for mitigating CH 4 emissions to the atmosphere Milucka et al, 2015;Segarra et al, 2015). However, despite the likelihood that MOx was more efficient in 2012 under warmer conditions, CH 4 concentrations in the stored pool were higher in 2012 than in 2013.…”

Methylotrophs in natural habitats: current insights through metagenomics

“…While the ability to denitrify presents one mechanism for coping with hypoxia (Kits et al 2015), active Methylococcaceae have also been detected in anoxic environments devoid of nitrate. In this case, methane oxidation was proposed to be linked to oxygenic photosynthesis (Milucka et al 2015).…”