Warming and polymetallic stress induce proteomic and physiological shifts in the neurotoxic Alexandrium pacificum as possible response to global changes

Harmful Algal Blooms involving the dinoflagellate Alexandrium pacificum continue to increase in ecosystems suffering the climate warming and anthropogenic pressure. Changes in the total proteome and physiological traits of the Mediterranean A. pacificum SG C10–3 strain were measured in response to increasing temperature (24 °C, 27 °C, 30 °C) and trace metal contamination (Cu2+, Pb2+, Zn2+, Cd2+). Warming reduced the cell densities and maximal growth rate (μmax), but the strain persisted at 30 °C with more large cells. The polymetallic stress increased cell sizes, reduced cell growth at 24 °C–27 °C and it increased this at 30 °C. Toxin profiles showed a predominance of GTX4 (32–38 %), then C2 (11–34 %) or GTX6 (18–24 %) among the total Paralytic Shellfish Toxins, however these were modified under warming, showing increased contents in GTX1 (among the most toxic), GTX5, C1 and NeoSTX, while dc-NeoSTX and STX (among the most toxic) only appeared at 30 °C. Under polymetallic contamination, warming also increased contents in GTX5 and NeoSTX. In contrast, polymetallic stress, or warming had harmful effects on C2 contents. Proteins were more quantitatively produced by A. pacificum SG C10–3 under warming in accordance with the high levels of up-regulated proteins found in the total proteome in this condition. Polymetallic stress, only or combined with warming, led to low proteomic modifications (1 % or 4 %), whereas warming induced strong 52 % modified proteomic response, mainly based on up-regulated proteins involved in photosynthesis (light harvesting complex protein), carbohydrate metabolism (arylsulfatase) and translation (ribosomal proteins), and with the lesser down-regulated proteins principally associated with the lipid metabolism (type I polyketide synthase). Our results show that warming triggers a strong up-regulated A. pacificum SG C10–3 proteomic response, which, coupled to modified cell sizes and toxin profiles, could help it to withstand stress conditions. This could presage the success of A. pacificum in anthropized ecosystems submitted to global warming in which this dinoflagellate also might be more toxic.