The stoichiometry of nutrient and energy transfer: from organelles to organisms

Abstract

All life requires the acquisition and transformation of nutrients and energy, driving processes from cellular nutrient flow to planetary biogeochemical cycling. However, the organisms and communities responsible for these processes are often uncultivable and too complex to observe directly and understand. Stoichiometric modeling, a systems biology approach, analyzes the reactions in an organism and incorporates data from multiple sources to extract biologically meaningful parameters, such as theoretical limits of conversion and yields of a metabolism. These limits and yields quantify relationships between organisms to establish governing principles, from resource requirements to community productivity as a function of population composition. The presented work expanded the stoichiometric modeling algorithm and identified fundamental principles that govern nutrient and energy transfer associated with heterotrophy, community composition, and intracellular compartmentalization. A scalable routine capable of analyzing complex metabolic networks by dividing them into tractable subnetworks was demonstrated for a eukaryotic diatom. The metabolic model contained approximately two billion routes through the network and established an international benchmark for elementary flux mode analysis. Additionally, a heterotrophic archaeon was examined for the resource requirements while consuming 29 different forms of biomass derived dissolved organic carbon. These resource requirements and limitations establish a basis to analyze heterotrophy with regard to the limiting nutrient in a variety of systems. The resulting resource requirements of heterotrophy were incorporated into a community where an iron oxidizing autotroph was hypothesized to be the primary source of carbon and energy. Analysis of the community model and in situ measurements of iron and oxygen utilization indicated additional electron donors were required to account for the observed acquisition of nutrients in some communities. Finally, limits and resource requirements for fungal production of hydrocarbons were identified as a function of carbon and energy partitioning using simulated genetic modifications, providing context regarding endophytic production of bioactive molecules for host resistance as well as endophyte capacity as a petroleum producing alternative.