Recycled by leaf inhabitants : Terrestrial bacteria drive the mineralization of organic matter in lake water

Abstract

Terrestrial organic matter subsidizes aquatic food webs and plays an important role in carbon cycling in lake ecosystems, where it is decomposed mainly by microbes. However, the contribution of terrestrial and aquatic microbiomes on terrestrial carbon cycling and their effects on the biochemical fate of carbon has remained understudied. Therefore, we explored the microbial carbon utilization of three chemically differing leaf species in lake water in microcosms and quantified the biochemical endpoints of leaf carbon in CO2, CH4, and microbial biomass. Additionally, we identified microbial taxa responsible for leaf carbon recycling and studied the role of epiphytic and endophytic leaf microbiomes in microbial community succession in lake water. Microbially utilized leaf carbon was mainly respired (82.7 ± 1.4%), whereas a small proportion (17.1 ± 1.4%) was assimilated into biomass. Carbon from nitrogen-rich alder leaves was taken up at the fastest rate, whereas birch leaf addition produced the highest concentrations of CH4, suggesting that leaf chemistry affects the decomposition rate and biochemical fate of carbon. In particular, terrestrial bacteria shaped the succession of aquatic bacterial communities. The addition of leaves resulted in the equal contribution of epiphytic and endophytic bacteria in the lake water, whereas epiphytic fungi dominated the fungal community structure. Our results suggest that terrestrial bacteria originating from terrestrial leaves influence the microbiome succession in lake ecosystems and play a key role in linking terrestrial carbon to an aquatic food web and determining the quality of carbon emissions that are released into the atmosphere.