Anthropogenic activities mediate stratification and stability of microbial communities in freshwater sediments

Abstract

Abstract Background As important decomposers on Earth, freshwater sediment microbes play a key role in regulating biogeochemical cycles and controlling greenhouse gas emissions. They often exhibit a highly ordered structure along depth profile. Besides redox effect, sediment stratification could also reflect historical transition. Recently, the Anthropocene as a candidate geological epoch has attracted great concern. Lake sediment is a typical environment for hosting traces that mark the anthropogenic pressure rise in the mid-20th century. However, little is known about the human impact on sediment zonation under cover of natural redox niches. Dam construction is one of the most far-reaching anthropogenic modifications of aquatic ecosystems. Here we attempted to identify the ecological imprint of damming on freshwater sediment microbiome. Results We conducted a year-round survey on sediment profiles of Lake Chaohu, a large shallow lake in China. Depth-discrete shotgun metagenomics, metataxonomics, and geophysiochemical analyses revealed a unique prokaryotic hierarchy contributed by coupling of redox regime and historical damming (labeled by the 137Cs peak in AD 1963). Dam-induced initial differentiation was amplified by nitrogen and methane metabolism, forming an abrupt transition which localized the nitrate-methane transition zone and controlled the depth of methane sequestration. At the transition zone, we observed significant taxonomic differentiation and identified damming-sensitive taxa via a random forest algorithm. Null model analysis showed that damming altered microbial community assembly, from a selection-oriented deterministic process above to a more stochastic, dispersal-limited one below. Temporal investigation revealed that the rapid transition zone acted as an ecotone where the local community exhibited high richness, low stability, and emergent stochasticity. Path analysis showed the emergent stochasticity mainly came from high microbial metabolic flexibility which potentially brought both ecological and statistical neutralities. Conclusions We delineate a picture in which dam-induced changes to the nutrient availability and sedimentation rate modify the microbial metabolic activities and generate great changes in the community structure, assembly and stability of the freshwater sediment microbiome. These findings reflect profound ecological and biogeochemical ramifications of human-Earth system interactions and help re-examine the mainstream views in the formation of sediment microbial stratification.