Universal metabolic constraints on the thermal tolerance of marine phytoplankton

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 specific 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 both photosynthesis and growth. Consequently, the respiratory cost of growth increased exponentially with rising temperatures eventually exceeding the supply of reduced carbon from photosynthesis, causing performance to decline rapidly past an optimum temperature. Our findings suggest that declines in performance at temperatures exceeding the optimum reflect diversion of metabolic energy away from growth to accommodate exponentially increasing costs of repair and maintenance likely driven by heat-induced cellular damage. 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.