Carbon translocation and methane emission in flooded rice microcosms with a manipulated root microbiome

Wetlands are important sources and sinks of effective greenhouse gases including carbon dioxide (CO2) and methane (CH4). Rhizodeposition by plants plays an essential role in carbon and nutrient supply for the soil microbiota and stimulates anaerobic decomposition of organic material by hydrolytic, fermenting and methanogenic microorganisms. However, little is known about the biotic and abiotic factors influencing the carbon turnover in the rhizosphere of wetland plants. This thesis focuses on the biogeochemical processes involved in carbon cycling of complex plant-soil systems to link microbial community structure to ecosystem functioning. Flooded rice microcosms were generated based on sand-vermiculite inoculated with seven soils from different ecosystems to manipulate the root microbiome. Using 13C pulse-labeling and molecular analyses, the carbon translocation from the atmosphere through the plant into the soil and back to the atmosphere as well as the microbial communities were studied in order to explore the impact of rice growth stages on C translocation and CH4 emission in Italian paddy soil in comparison to reduced soil content and sterile soil, and to evaluate the effect of the seven soils on plant biomass production and carbon cycling. The application of isotopic pulse-labeling allowed tracing the carbon that exclusively derived from recent plant photosynthates. Overall, the majority of freshly assimilated C remained in aboveground plant biomass, about 10% was allocated into the roots and less than 2% was recovered in soil organic matter independently from the soil type; however, sterile soil strongly inhibited belowground 13C translocation. The 13C enrichment in the different C pools was affected by the soil content and the plant growth stage and revealed that recently plant-assimilated carbon was an important source for methanogenesis accounting for up to 7% of the total CH4 emitted within five days depending on soil type. Rice biomass production was affected by the soil type and was positively correlated with CH4 emission in Italian paddy soil. The abundance of archaeal communities changed in response to plant developmental growth stage and was correlated with the amount of emitted 13CH4 that was exclusively derived from fresh photosynthates. These findings indicate that rhizodeposition and microbial abundances in the rhizosphere were critical for the emission of methane especially during the late vegetative and reproductive stages of rice plants. The seven soils covering five different ecosystem types not only differed in the main soil characteristics, but also contained distinct archaeal (16S rRNA) and methanogenic (mcrA) populations and exhibited different CH4 production potentials. Multivariate analyses demonstrated that the archaeal and methanogenic fingerprints were also distinct in the rice rhizosphere when soils were used for generating rice-planted microcosms. The root microbiome was characterized by a highly diverse community where characteristic archaeal and methanogenic groups were detected in the rice rhizosphere. These microorganisms were not detected in the original soils and thus could be critical for the different rates of emitted 13CH4 observed. Canonical correspondence analysis indicated that the differences in methanogenic communities colonizing the rice rhizosphere were mainly attributed to the carbon and nutrient content of the inoculated soils and to the plant biomass. These results suggest that plant and soil factors cooperatively shape the root microbiome and affect methane emission from fresh photosynthates. Collectively, the study revealed that allocation of freshly assimilated carbon in submerged rice plants, C translocation into the rhizosphere and gas emission to the atmosphere were affected by both the plant growth stage, and also by the amount and type of soil in which the rice plants grew. The soil-inhabiting microorganisms as principle drivers of global nutrient cycles have an important impact on carbon translocation between hydrophytic plants and wetland soils and influence the emission of the climate-relevant trace gases CO2 and CH4.