Severe cyanobacteria accumulation potentially induces methylotrophic methane producing pathway in eutrophic lakes

Although cyanobacteria blooms lead to an increase in methane (CH₄) emissions in eutrophic lakes have been intensively studied, the methane production pathways and driving mechanisms of the associated CH₄ emissions are still unclear. In this study, the hypereutrophic Lake Taihu, which has extreme cyanobacteria accumulation, was selected to test hypothesis of a potential methylotrophic CH₄ production pathway. Field observation displayed that the CH₄ emission flux from the area with cyanobacteria accumulation was 867.01 μg m^-2·min^-1, much higher than the flux of 3.44 μg m^-2·min^-1 in the non-cyanobacteria accumulation area. The corresponding abundance of methane-producing archaea (MPA) in the cyanobacteria-concentrated area was 77.33% higher than that in the non-concentrated area via RT-qPCR technologies. Synchronously, sediments from these areas were incubated in anaerobic bottles, and results exhibited the high CH₄ emission potential of the cyanobacteria concentrated area versus the non-concentrated area (1199.26 vs. 205.76 μmol/L) and more active biological processes (CO₂ emission, 2072.8 vs. -714.62 μmol/L). We also found evidence for the methylotrophic methane producing pathway, which contributed to the high CH₄ emission flux from the cyanobacteria accumulation area. Firstly, cyanobacteria decomposition provided the prerequisite of abundant methyl thioether substances, including DMS, DMDS, and DMTS. Results showed that the content of methyl thioethers increased with the biomass of cyanobacteria, and the released DMS, DMDS, and DMTS was up to 96.35, 3.22 and 13.61 μg/L, respectively, in the highly concentrated 25000 g/cm³ cyanobacteria treatment. Then, cyanobacteria decomposition created anaerobic microenvironments (DO 0.06 mg/L and Eh -304.8Mv) for methylotrophic methane production. Lastly, the relative abundance of Methanosarcinales was increased from 7.67% at the initial stage to 36.02% at the final stage within a sediment treatment with 10 mmol/L N(CH₃)₃. Quantitatively, the proportion of the methylotrophic methane production pathway was as high as 32.58%. This finding is crucial for accurately evaluating the methane emission flux, and evaluating future management strategies of eutrophic lakes.