Abstract
ANaerobic MEthanotrophic (ANME) archaea remove the greenhouse gas methane from anoxic environments and diminish its flux to the atmosphere. High methane removal efficiencies are well documented in marine environments, whereas anaerobic oxidation of methane (AOM) was only recently indicated as an important methane sink in freshwater systems. Freshwater AOM-mediating microorganisms lack taxonomic identification and only little is known about metabolic adaptions to prevailing biogeochemical conditions. One of the first study sites providing information about AOM activity in freshwater sediment is Lake Ørn, a low-sulfate, iron-rich Danish lake. With the aim to identify freshwater AOM-mediating archaea, we incubated AOM-active anoxic, nitrate-free freshwater sediment from Lake Ørn with 13C-labeled methane (13CCH4) and 13C-labeled bicarbonate (13CDIC) and followed the assimilation of 13C into RNA by stable isotope probing. While AOM was active, 13CCH4 and probably also 13CDIC were incorporated into uncultured archaea of the Methanosarcinales-related cluster ANME-2d, whereas other known ANME lineages were not detected. This finding strongly suggests that ANME-2d archaea perform AOM coupled to sulfate and/or iron reduction and may have the capability of mixed assimilation of CH4 and DIC. ANME-2d archaea may thus play an important role in controlling methane emissions from nitrate-depleted and low-sulfate freshwater systems.
Highlights
As a major sink of the greenhouse gas methane (CH4), anaerobic oxidation of methane (AOM) is a significant regulator of the global methane cycle (Knittel and Boetius, 2009)
During sulfate-dependent AOM, ANaerobic MEthanotrophic (ANME) strains were often observed in consortia with sulfatereducing bacteria (Boetius et al, 2000) and currently three concepts allowing reducing equivalent transfer are discussed: (1) an obligate syntrophic process between the partners involving an interspecies electron carrier (e.g., Meulepas et al, 2010), (2) direct electron transfer by conductive pili providing cell-to-cell contact (McGlynn et al, 2015; Wegener et al, 2015) or (3) ANME carrying out both methane oxidation and sulfate reduction and excreting zero-valent sulfur compounds that are further disproportionated by the associated bacterial partners (Milucka et al, 2012)
We focus on the biogeochemical results from these incubations here (Figures 2, 3), while the results of the 13C-labeled bicarbonate (13CDIC) core and 13CCH4 slurry incubations are displayed in Supplementary Figures S1, S2
Summary
As a major sink of the greenhouse gas methane (CH4), anaerobic oxidation of methane (AOM) is a significant regulator of the global methane cycle (Knittel and Boetius, 2009). During sulfate-dependent AOM, ANME strains were often observed in consortia with sulfatereducing bacteria (Boetius et al, 2000) and currently three concepts allowing reducing equivalent transfer are discussed: (1) an obligate syntrophic process between the partners involving an interspecies electron carrier (e.g., Meulepas et al, 2010), (2) direct electron transfer by conductive pili (nanowires) providing cell-to-cell contact (McGlynn et al, 2015; Wegener et al, 2015) or (3) ANME carrying out both methane oxidation and sulfate reduction and excreting zero-valent sulfur compounds that are further disproportionated by the associated bacterial partners (Milucka et al, 2012) In contrast to this puzzling diversity of pathways, a nitrate-reducing ANME strain named ‘Candidatus Methanoperedens nitroreducens’ was shown to have the enzymatic capability to perform reverse methanogenesis while reducing nitrate on its own (Haroon et al, 2013). A strain closely related to ‘Cand. M. nitroreducens’ from a freshwater enrichment culture was shown to couple AOM to the reduction of soluble and nanoparticulate forms of ferric iron (Ettwig et al, 2016)
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