Here we explore strategies of resource utilization and allocation of algal versus terrestrially derived carbon (C) by lake bacterioplankton. We quantified the consumption of terrestrial and algal dissolved organic carbon, and the subsequent allocation of these pools to bacterial growth and respiration, based on the δ(13)C isotopic signatures of bacterial biomass and respiratory carbon dioxide (CO2). Our results confirm that bacterial communities preferentially remove algal C from the terrestrially dominated organic C pool of lakes, but contrary to current assumptions, selectively allocate this autochthonous substrate to respiration, whereas terrestrial C was preferentially allocated to biosynthesis. The results provide further evidence of a mechanism whereby inputs of labile, algal-derived organic C may stimulate the incorporation of a more recalcitrant, terrestrial C pool. This mechanism resulted in a counterintuitive pattern of high and relatively constant levels of allochthony (~76%) in bacterial biomass across lakes that otherwise differ greatly in productivity and external inputs.