Heat shock effects and population survival in the polar dinoflagellate Polarella glacialis

The rare bipolar dinoflagellate Polarella glacialis forms blooms in the Antarctic sea ice and the Arctic water column every year. Recently, P. glacialis-like genotypes were found in temperate waters. Here, we investigated how P. glacialis would respond if it were transported from polar to temperate waters by shifting cultures of P. glacialis (strain CCMP2088) from 4 °C to 10° and 15 °C. After a 4-day lag phase, the cultures remaining at 4 °C grew exponentially at 0.10 ± 0.17 d− 1 for 22 days before entering early stationary phase. Consistent to this growth pattern, flow cytometric analysis on samples collected at the same time showed higher percentages of S-cells on day 9 and day 12 than day 33 and day 37. Western blot analysis of the CO2-fixing enzyme Rubisco1 (typically 55 kDa) and the cell cycle-related protein PCNA2 (typically 36 kDa) revealed active expression of both proteins, and higher expression in exponential growth than in early stationary phase. In comparison, cultures shifted to 10° and 15 °C first experienced a 4-day lag phase plus a 13–15 day declining phase (growth rates were − 0.21 ± 0.10 d− 1 and − 0.23 ± 0.08 d− 1 respectively), then a steady cell density period (growth rates were 0.05 ± 0.12 d− 1 and 0.01 ± 0.15 d− 1 respectively). Strikingly, the percentages of the G2/M phase (%G2M) in the 10 °C-cultures remained at high levels and G1 population at a low level, suggesting that a subpopulation of the cells might still be actively dividing. %G2M of the 15 °C-culture remained to be the lowest among the three temperature treatments (P < 0.05), indicative of least active cell division. Molecular apparatus of photosynthesis and cell division cycle appeared to be substantially damaged as the culture stayed longer at the elevated temperatures, as evidenced by the progressive degradation of Rubisco and aggregation of PCNA. Our results show that although extreme heat shock as exerted by the temperature rise from 4 °C to 10° or 15 °C caused impairment of molecular engines of photosynthesis and cell division cycle and extensive population decline in P. glacialis, this polar dinoflagellate seems to be able to survive the extreme temperature insults and potentially can be spread by humans to temperate regions.

► We studied Polarella glacialis's response to temperature rises from 4 °C up to 15 °C.
► The cultures experienced a 13–15 day decline then a steady cell density period.
► We observed progressive degradation of Rubisco and aggregation of PCNA.
► The alga survived the heat shock, showing the potential to spread to warm waters.