Plant roots but not hydrology control microbiome composition and methane flux in temperate fen mesocosms

The rewetting of formerly drained peatlands can help to counteract climate change through the reduction of CO₂ emissions. However, this can lead to resuming CH₄ emissions due to changes in the microbiome, favoring CH₄-producing archaea. How plants, hydrology and microbiomes interact as ultimate determinants of CH₄ dynamics is still poorly understood. Using a mesocosm approach, we studied peat microbiomes, below-ground root biomass and CH₄ fluxes with three different water level regimes (stable high, stable low and fluctuating) and four different plant communities (bare peat, Carex rostrata, Juncus inflexus and their mixture) over the course of one growing season. A significant difference in microbiome composition was found between mesocosms with and without plants, while the difference between plant species identity or water regimes was rather weak. A significant difference was also found between the upper and lower peat, with the difference increasing as plants grew. By the end of the growing season, the methanogen relative abundance was higher in the sub-soil layer, as well as in the bare peat and C. rostrata pots, as compared to J. inflexus or mixture pots. This was inversely linked to the larger root area of J. inflexus. The root area also negatively correlated with CH₄ fluxes which positively correlated with the relative abundance of methanogens. Despite the absence or low abundance of methanotrophs in many samples, the integration of methanotroph abundance improved the quality of the correlation with CH₄ fluxes, and methanogens and methanotrophs together determined CH₄ fluxes in a structural equation model. However, water regime showed no significant impact on plant roots and methanogens, and consequently, on CH₄ fluxes. This study showed that plant roots determined the microbiome composition and, in particular, the relative abundance of methanogens and methanotrophs, which, in interaction, drove the CH₄ fluxes.