Annually, the oceans absorb about one fourth of the anthropogenically produced atmospheric carbon dioxide (CO2) resulting in a drop in surface water pH, a process termed ocean acidification (OA). Surprisingly little is known about how OA affects physiology as well as food web interactions of heterotrophic bacteria when essential nutrients are limited, since most previous experiments were carried out during productive phases or even after nutrient additions to stimulate algal blooms. Therefore, we conducted an in situ large-volume mesocosm (~55 m3) experiment in the Baltic Sea by simulating different fugacities of CO2 (fCO2) extending from present to future conditions. The study was carried out after the spring-bloom in July–August to maintain low-nutrient conditions throughout the experiment, which resulted in a small-sized phytoplankton community dominated by picophytoplankton. Several positive as well as negative effects on free-living (FL) and particle-associated (PA) bacterial protein production (BPP) and biovolume (BV) could be related to fCO2-induced differences in phytoplankton composition and subsequent the availability of phytoplankton-derived organic matter. However, dynamics of BV and cell-specific BPP (csBPP) of FL heterotrophic bacteria could not be explained exclusively by the availability of phytoplankton-derived organic carbon. The dynamics were also related to enhanced grazing on DNA rich (HDNA) bacterial cells at higher fCO2 as revealed by flow cytometry. Additionally, a decoupling of autotrophic production and heterotrophic consumption during the last third of the experiment resulted in low, but significantly higher accumulation of DOC at enhanced fCO2. Interestingly we could not detect any consistent and direct fCO2-induced effect on BPP, csBPP nor BV of either FL or PA heterotrophic bacteria. In contrast, our results reveal several indirect fCO2-induced effects on BPP and bacterial BV with potential consequences for oceanic carbon cycling, in particular in a low nutrient and high fCO2 future ocean.