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

Abstract

Lakes represent a considerable natural source of methane to the atmosphere compared to their small global surface area. Methanotrophs in sediments and in the water column largely control methane fluxes from these systems, yet the diversity, electron accepting capacity, and nutrient requirements of these microorganisms have only been partially identified. Here, we investigated the role of electron acceptors alternative to oxygen and sulfate in microbial methane oxidation at the oxycline and in anoxic waters of the ferruginous meromictic Lake La Cruz, Spain. Active methane turnover in a zone extending well below the oxycline was evidenced by stable carbon isotope-based rate measurements. We observed a strong methane oxidation potential throughout the anoxic water column, which did not vary substantially from that at the oxic/anoxic interface. Both in the redox-transition and anoxic zones, only aerobic methane-oxidizing bacteria (MOB) were detected by fluorescence in situ hybridization and sequencing techniques, suggesting a close coupling of cryptic photosynthetic oxygen production and aerobic methane turnover. Additions of nitrate, nitrite and to a lesser degree iron and manganese oxides also stimulated bacterial methane consumption. We could not confirm a direct link between the reduction of these compounds and methane oxidation and we cannot exclude the contribution of unknown anaerobic methanotrophs. Nevertheless, our findings from Lake La Cruz support recent laboratory evidence that aerobic methanotrophs may be able to utilize alternative terminal electron acceptors under oxygen limitation.

Millions of Boreal Shield Lakes can be used to Probe Archaean Ocean Biogeochemistry

“…Metabolism of gammaproteobacterial methanotrophs that are present in high abundance in the anoxic zone has been suggested to be coupled to oxygen produced by cyanobacteria at the same depth2837, but it is also possible that this process may be coupled to the reduction of alternative electron acceptors, such as newly oxidized iron by photoferrotrophs. Very recently, methanotrophs of the same taxonomic group as we found in L227 and L442 were found thriving in the anoxic zones of Lake La Cruz and meromictic Lake Zug, Switzerland and able to oxidize methane without oxygen in the absence of light1638. Further, these methanotrophs were stimulated by the addition of oxidized iron and manganese1638.…”

“…Very recently, methanotrophs of the same taxonomic group as we found in L227 and L442 were found thriving in the anoxic zones of Lake La Cruz and meromictic Lake Zug, Switzerland and able to oxidize methane without oxygen in the absence of light1638. Further, these methanotrophs were stimulated by the addition of oxidized iron and manganese1638. Iron reduction coupled to anaerobic methane oxidation has also been reported in an archaeal enrichment culture, showing the validity of this redox process in the natural environment39.…”

Biogeochemical and physical controls on methane fluxes from two ferruginous meromictic lakes

“…Low (but detectable) O 2 concentrations, a peak in the relative abundance of aerobic MOB, and a consistent shift to higher δ 13 C CH4 isotopes indicate a role for aerobic MOB in CH 4 oxidation at the oxycline. Canyon Lake displays similar trends in CH 4 , δ 13 C CH4 , and aerobic MOB in June 2017. Notable in June 2017 was an extreme + 72 ‰ shift between 16 and 13.5 m. Similar observations in the δ 13 C CH4 isotope profiles have been attributed to aerobic MOB at the oxic–anoxic boundary in other lakes (e.g., Blees et al, ; Oswald, Jegge, et al, ; Schubert et al, ).…”

“…These processes are also envisioned to have impacted the carbon cycle in ferruginous oceans (Posth, Konhauser, & Kappler, ). Recent work in these lakes has highlighted the utility of such lakes to investigate microbiological and geochemical aspects of CH 4 cycling (e.g., Crowe et al, ; Dupuis et al, ; Lopes et al, ; Oswald, Jegge, et al, ; Savvichev et al, ). The CH 4 cycle in ferruginous lakes has been most thoroughly discussed in the context of Indonesian Lake Matano and has given rise to active debate surrounding organic matter preservation in ferruginous oceans (Crowe et al, ; Kuntz, Laakso, Schrag, & Crowe, ; Laakso & Schrag, ).…”

“…There is a general decrease in CH 4 concentration from the sediment- the δ 13 C CH4 isotope profiles have been attributed to aerobic MOB at the oxic-anoxic boundary in other lakes (e.g., Blees et al, 2014;Oswald, Jegge, et al, 2016a;Schubert et al, 2006). (Norði, Thamdrup, & Schubert, 2013;Weber, Thamdrup, & Habicht, 2016).…”