Energy strategies sustaining the legume-rhizobia symbiotic nitrogen fixation system

Abstract

Symbiotic nitrogen fixation (SNF) by legumes and rhizobia is a highly energy demanding mode of biological nitrogen fixation. Although the nitrogenase reaction defines the theoretical minimum energy requirement, how energy is supplied, consumed, and regulated across symbiotic stages remains incompletely understood. In this review, we use energy economics as an interpretive framework to examine how legumes and rhizobia coordinate energy supply and demand, how multilevel regulatory networks shape carbon–nitrogen exchange and nitrogen conversion efficiency, and how energy sourcing and allocation vary across symbiotic stages, organs, nodule zones, and cell types. Furthermore, we briefly consider whether lipid derived metabolites contribute to nodule carbon metabolism under specific conditions, noting that direct evidence that lipid derived carbon enters bacteroid central metabolism, fuels respiration, or supports nitrogenase activity remains lacking. We also discuss stress induced reprogramming of symbiotic energy allocation in horticultural legumes. We further highlight the limitations of bulk omics and the potential of high resolution spatiotemporal multi omics to resolve metabolic heterogeneity among nodule zones and cell types. Finally, we propose a framework for systematic research encompassing “spatiotemporal atlas resolution—validation of coupling driving forces—predictive model construction”. In summary, this review conceptualizes energy intensive SNF as a multilevel supply demand system and shifts the analysis of SNF from macroscopic description to identifiable, quantitative, and predictable control nodes. This perspective provides a fresh analytical basis for optimizing energy allocation strategies during SNF and lays a theoretical foundation for designing low energy, high efficiency symbiotic systems through synthetic biology.