Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands

Abstract

Significance Given the current pressing need to more fully understand the methane cycle on Earth, in particular, unidentified sinks for methane, identifying and quantifying novel sinks for methane is fundamental importance. Here, we provide previously unidentified direct evidence for the nitrite-dependent anaerobic methane oxidation (n-damo) process as a previously overlooked microbial methane sink in wetlands by stable isotope measurements, quantitative PCR assays, and 16S rRNA and particulate methane monooxygenase gene clone library analyses. It is estimated that n-damo could consume 4.1–6.1 Tg of CH 4 m −2 per year in wetlands under anaerobic conditions, which is roughly 2–6% of current worldwide CH 4 flux estimates for wetlands. Given the worldwide increase in nitrogen pollution, this methane sink may become more important in the future.

High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions

“…This and other evidence of AOM in FWW without anthropogenically-enhanced nitrogen levels indicate an as-yet-unidentified electron acceptor 2,20 . While nitrite has been shown to support AOM in some nitrogen enriched wetlands 5,36 , the evidence for nitratedependent anaerobic methane oxidation (n-damo) in this study is weak. AOM was not significantly correlated with nitrite concentrations in Florida or Georgia.…”

“…In contrast, a dominant electron acceptor for freshwater AOM has not been identified. Experimental evidence suggest sulphate is not the sole electron acceptor for AOM in freshwater sediments and peat 2,9,15,20 , and AOM in low-sulphate environments has been linked to the reduction of nitrate, nitrite, iron and manganese 4,5,12,13,16,33 . The geochemical and rate profiles in the wetlands studied here support a linkage between SR and AOM.…”

“…Thus, while AOM in Maine and Florida may be coupled to SR, at least some fraction of AOM activity in Georgia must be supported by alternative electron acceptor(s). Such alternative electron acceptors (for example, nitrate, nitrite, iron oxides or manganese oxides) were readily available in these sediments (Table 1; Supplementary Table 2) and may support AOM in FWW 5,9,13 . The production of reduced iron at depth in Georgia ( Supplementary Fig.…”

“…Few studies have examined anaerobic oxidation of methane (AOM) in FWW [2][3][4][5] and AOM was largely regarded as inconsequential in these environments until recently. Instead, aerobic methane oxidation was assumed to be the dominant mode of methane consumption in FWW 6 .…”

“…Yet, despite low sulphate concentrations, FWW support a dynamic sulphur cycle and high rates of sulphate reduction 9 (SR) are maintained by rapid recycling of reduced sulphur species 10 . Moreover, studies of freshwater AOM have indicated several electron acceptors for methane oxidation, including sulphate 11 , nitrate/nitrite 5,[12][13][14][15] , iron 16 and manganese 17 . Geochemical profiles 4,18,19 , stable isotope geochemistry 16,18,19 , potential methane oxidation assays 2,4,5,20 and long-term enrichments 4 have provided tantalizing evidence of AOM in FWW, but environmentally relevant, in vitro, rate measurements are rare 9 .…”