Atmospheric levels of carbon dioxide are tightly linked to the depth at which sinking particulate organic carbon (POC) is remineralised in the ocean. Rapid attenuation of downward POC flux typically occurs in the upper mesopelagic (top few hundred metres of the water column), with much slower loss rates deeper in the ocean. Currently, we lack understanding of the processes that drive POC attenuation, resulting in large uncertainties in the mesopelagic carbon budget. Attempts to balance the POC supply to the mesopelagic with respiration by zooplankton and microbes rarely succeed. Where a balance has been found, depth-resolved estimates reveal large compensating imbalances in the upper and lower mesopelagic. In particular, it has been suggested that respiration by free-living microbes and zooplankton in the upper mesopelagic are too low to explain the observed flux attenuation of POC within this layer. We test the hypothesis that particle-associated microbes contribute significantly to community respiration in the mesopelagic, measuring particle-associated microbial respiration of POC in the northeast Atlantic through shipboard measurements on individual marine snow aggregates collected at depth (36–500 m). We find very low rates of both absolute and carbon-specific particle-associated microbial respiration (< 3%d-1), suggesting that this term cannot solve imbalances in the upper mesopelagic POC budget. The relative importance of particle-associated microbial respiration increases with depth, accounting for up to 33% of POC loss in the mid-mesopelagic (128–500 m). We suggest that POC attenuation in the upper mesopelagic (36–128 m) is driven by the transformation of large, fast-sinking particles to smaller, slow-sinking and suspended particles via processes such as zooplankton fragmentation and solubilisation, and that this shift to non-sinking POC may help to explain imbalances in the mesopelagic carbon budget.