What limits photosynthesis? Identifying the thermodynamic constraints of the terrestrial biosphere within the Earth system.

Photosynthesis converts sunlight into the chemical free energy that feeds the Earth's biosphere, yet at levels much lower than what thermodynamics would allow for. I propose here that photosynthesis is nevertheless thermodynamically limited, but this limit acts indirectly on the material exchange. I substantiate this proposition for the photosynthetic activity of terrestrial ecosystems, which are notably more productive than the marine biosphere. The material exchange for terrestrial photosynthesis involves water and carbon dioxide, which I evaluate using global observation-based datasets of radiation, photosynthesis, precipitation and evaporation. I first calculate the conversion efficiency of photosynthesis in terrestrial ecosystems and its climatological variation, with a median efficiency of 0.77% (n = 13,274). The rates tightly correlate with evaporation on land (r2 = 0.87), which demonstrates the importance of the coupling of photosynthesis to material exchange. I then infer evaporation from the maximum material exchange between the surface and the atmosphere that is thermodynamically possible using datasets of solar radiation and precipitation. This inferred rate closely correlates with the observation-based land evaporation dataset (r2 = 0.84). When this rate is converted back into photosynthetic activity, the resulting patterns correlate highly with the observation-based dataset (r2 = 0.66). This supports the interpretation that it is not energy directly that limits terrestrial photosynthesis, but rather the material exchange that is driven by sunlight. This interpretation can explain the very low, observed conversion efficiency of photosynthesis in terrestrial ecosystems as well as its spatial variations. More generally, this implies that one needs to take the necessary material flows and exchanges associated with life into account to understand the thermodynamics of life. This, ultimately, requires a perspective that links the activity of the biosphere to the thermodynamic constraints of transport processes in the Earth system.