Universal metabolic constraints on the thermal tolerance of marine phytoplankton

Abstract

Marine phytoplankton are responsible for over 45% of annual global net primary production. Ocean warming is expected to drive massive reorganisation of phytoplankton communities, resulting in pole-ward range shifts and sharp declines in species diversity, particularly in the tropics. The impacts of warming on phytoplankton species depend critically on their physiological sensitivity to temperature change, characterised by thermal tolerance curves. Local extinctions arise when temperatures exceed species thermal tolerance limits. The mechanisms that determine the characteristics of thermal tolerance curves (e.g. optimal and maximal temperatures) and their variability among the broad physiological diversity of marine phytoplankton are however poorly understood. Here we show that differences in the temperature responses of photosynthesis and respiration establish physiological trade-offs that constrain the thermal tolerance of 18 species of marine phytoplankton, spanning cyanobacteria as well as the red and green super-families. Across all species we found that rates of respiration were more sensitive to increasing temperature and typically had higher optimal temperatures than photosynthesis. Consequently, the fraction of photosynthetic energy available for allocation to growth (carbon-use efficiency) declined exponentially with rising temperatures with a sensitivity that was invariant among the 18 species. Furthermore, the optimal temperature of growth was generally lower than that of photosynthesis and as a result, supra-optimal declines in growth rate were associated with temperature ranges where the carbon-use efficiency exhibited accelerated declines. These highly conserved patterns demonstrate that the limits of thermal tolerance in marine phytoplankton are underpinned by common metabolic constraints linked to the differential temperature responses of photosynthesis and respiration.\n\nSignificance StatementThe impacts of warming on marine phytoplankton depend on their sensitivity to rising temperatures, yet there is currently limited understanding of the mechanisms that limit thermal tolerance among the diversity of marine phytoplankton. Using a comparative study on the dominant, ecologically important lineages of marine phytoplankton - Bacillariophyceae, Dinophyceae, Cyanophyceae, Prasinophyceae, Prymnesiophyceae - we show that rates of respiration are consistently more sensitive to increasing temperature than photosynthesis. Consequently, the fraction of photosynthetic energy available for growth declines with rising temperatures with a sensitivity that is invariant among species. Our results suggest that declines in phytoplankton performance at high temperatures are driven by universal metabolic constrains linked to rising respiratory costs eventually exceeding the supply of reduced carbon from photosynthesis.