Microalgae are naturally adapted to fluctuating availability of phosphorus (P) being capable to opportunistically uptake large amounts of inorganic phosphate (Pi) and safely store it in the cell as polyphosphate. Hence, many microalgal species are remarkably resilient to high concentrations of external Pi. Here we report on an exception from this pattern comprised by a failure of the high Pi-resilience in a strain Micractinium simplicissimum IPPAS C-2056 normally coping with a very high Pi concentrations. This phenomenon occurred after abrupt re-supplementation of Pi to the M. simplicissimum culture pre-starved of P. This was the case even if Pi was re-supplemented in a concentration far below the level toxic to the P-sufficient culture. We hypothesize that this effect can be mediated by a rapid formation of the potentially toxic short-chain polyphosphate following the mass influx of Pi into the P-starved cell. A possible reason for this is that the preceding P starvation impairs the capacity of the cell of converting the newly absorbed Pi into a “safe” storage form of long-chain polyphosphate. We believe that findings of this study can help to avoid sudden culture crashes, they are also of potential significance for development of algae-based technologies for efficient bioremoval of P from P-rich waste streams.