A Phytoplankton Model for the Allocation of Gross Photosynthetic Energy Including the Trade-Offs of Diazotrophy

Abstract

Gross photosynthetic activity by phytoplankton is directed to linear and alternative electron pathways that generate ATP, reductant, and fix carbon. Ultimately less than half is directed to net growth. Here we present a phytoplankton cell allocation model that explicitly represents a number of cell metabolic processes and functional pools with the goal of evaluating ATP and reductant demands as a function of light, nitrate, iron, oxygen, and temperature for diazotrophic versus nondiazotrophic growth. We employ model analogues of Synechoccocus and Crocosphaera watsonii, to explore the trade-offs of diazotrophy over a range of environmental conditions. Model analogues are identical in construction, except for an iron quota associated with nitrogenase, an additional respiratory demand to remove oxygen in order to protect nitrogenase and an additional ATP demand to split dinitrogen. We find that these changes explain observed differences in growth rate and iron limitation between diazotrophs and nondiazotrophs. Oxygen removal imparted a significantly larger metabolic cost to diazotrophs than ATP demand for fixing nitrogen. Results suggest that diazotrophs devote a much smaller fraction of gross photosynthetic energy to growth than nondiazotrophs. The phytoplankton cell allocation model model provides a predictive framework for how photosynthate allocation varies with environmental conditions in order to balance cellular demands for ATP and reductant across phytoplankton functional groups.