The in situ physiology of the filamentous bacterium Microthrix parvicella was investigated in anaerobic-aerobic dynamic phases in activated sludge with focus on the uptake of long chain fatty acids (LCFA) and growth. When 14C-labeled oleic acid was added to activated sludge with an excessive growth of M. parvicella, only little 14C-CO2 was produced under anaerobic conditions while a lot was produced under aerobic conditions. Microautoradiographic studies revealed that M. parvicella took up oleic acid under both anaerobic and aerobic conditions, while only a few floc formers were able to take it up under anaerobic conditions. Extraction and separation of the radioactive biomass into different lipid fractions showed that the oleic acid was stored mainly as neutral lipids under anaerobic conditions, whereas conversion to membrane phospholipids occurred almost exclusively under aerobic conditions, indicating growth. The surface properties of M. parvicella and other bacteria were characterized by hydrophobic fluorescent microspheres, which showed that M. parvicella was relatively hydrophobic. Furthermore, a surface-associated extracellular lipase activity was observed, indicating the ability of M. parvicella to degrade lipids near the filament surface. The results support the hypothesis that uptake and storage of LCFA as lipids under anaerobic conditions provide an effective competition strategy against bacteria that can only take up LCFA under aerobic conditions. Thus, M. parvicella seems to be a specialized lipid consumer with a physiological potential analogous to PAOs and GAOs being able to take up LCFA (but not short chain fatty acids or glucose) under anaerobic conditions and subsequently use the storage material for growth when nitrate or oxygen are available as electron acceptors.