Detritus-hosted methanogenesis sustains the methane paradox in an alpine lake

Accumulation of methane in oxic waters of lakes and the ocean has been widely reported. Despite the importance for the greenhouse gas budget, mechanistic controls of such "methane paradox" remain elusive. Here, we use a combination of CH4 concentration and isotopic (delta C-13(CH4), delta D-H2O and delta O-18(H2O)) measurements, plankton incubations and microbial community assessments to demonstrate the existence of the methane paradox in oxygenated waters of a meromictic lake (Lake Cadagno, Switzerland). Following mass dynamics using water isotopes, we exclude the possibility that the accumulation of CH4 at the thermocline results solely from lateral transport. Interannual variability in the magnitude of the methane paradox (between 0.5 and 5 mu mol L-1) is associated to stratification patterns, changes in zooplankton biomass and planktonic detritus accumulation along density gradients, as well as fluctuating microbial cell numbers. The links between hydrodynamic conditions, aggregation of planktonic detritus and its microbiome, as well as the accumulation of CH4 in the water column are further supported by high-resolution echosounder revealing backscatter maxima at the top of the thermocline, where detritus is effectively trapped, and by oxic incubations showing that CH4 is produced in zooplankton detritus (0.046 nmol L-1 to 0.095 CH4 mg dry mass L-1 d(-1)). Our results also show that detritus-hosted methanogenesis is stimulated through the addition of methylphosphonate, suggesting that zooplankton-associated microbiomes exploit organic phosphorus compounds to release CH4. Understanding the variability of the methane paradox in relation to changing hydrodynamics and plankton communities will be crucial to predict the future role of lakes in the global methane budget.