Ecological functions of fungal and bacterial decomposers vary with environmental conditions. However, the response of these decomposers to particulate organic matter (POM) quality, which varies widely in aquatic ecosystems, remains poorly understood. Here we investigated how POM pools of substrates of different qualities determine the relative contributions of aquatic fungi and bacteria to terrigenous carbon (C) turnover. To this end, surface sediments were incubated with different POM pools of algae and/or leaf litter. 13C stable-isotope measurements of C mineralization were combined with phospholipid analysis to link the metabolic activities and substrate preferences of fungal and bacterial heterotrophs to dynamics in their abundance. We found that the presence of labile POM greatly affected the dominance of bacteria over fungi within the degrader communities and stimulated the decomposition of beech litter primarily through an increase in metabolic activity. Our data indicated that fungi primarily contribute to terrigenous C turnover by providing litter C for the microbial loop, whereas bacteria determine whether the supplied C substrate is assimilated into biomass or recycled back into the atmosphere in relation to phosphate availability. Thus, this study provides a better understanding of the role of fungi and bacteria in terrestrial-aquatic C cycling in relation to environmental conditions.