Methanotrophs are the main consumers of methane produced in lake sediments. In shallow lakes suffering from eutrophication, methanogenesis is accelerated by the excess organic carbon input, and thus methanotrophs play a key role in regulating this methane flux as well as carbon cycling. Here, we applied nucleic acid stable isotope probing (SIP) to investigate the active methanotrophic microbial community in sediments of several shallow lakes affected by eutrophication. Our results showed that an active methanotrophic community dominated by gamma-proteobacterial methanotrophs, as well as abundant beta-proteobacterial methanol-utilizers, was involved in methane-derived carbon assimilation. Crenothrix, a filamentous methanotroph, was found to be a key methane consumer in all studied lakes. The ecological role of Crenothrix in lacustrine ecosystems is so far poorly understood, with only limited information on its existence in the water column of stratified lakes. Our results provide a novel ecological insight into this group by revealing a wide distribution of Crenothrix in lake sediments. The active methane assimilation by Crenothrix also suggested that it might represent a so far overlooked but crucial biological sink of methane in shallow lakes.