In the symbiosome: Cross-kingdom dating under the moonlight

Abstract

Throughout legume–rhizobium symbiosis, nitrogen fixation occurs within the symbiosome, a membrane-bound organelle-like structure found in nodule cells. The symbiosome represents a temporary organelle in which rhizobia-encoded nitrogenase catalyzes dinitrogen conversion to ammonia in an oxygen-regulated microenvironment. Investigating symbiosome biology will undoubtedly improve our understanding of nitrogen fixation mechanisms and highlight novel targets for improving nitrogen fixation efficiency. Recent research advancements have taken place on regulatory aspects of symbiosome generation and functions, but obtaining spatiotemporally resolved symbiosome proteome and metabolomes, as well as tracking and deciphering its intracellular communication, is challenging. As a symbiotic interface, the symbiosome membrane proteome is largely composed of plant-derived proteins, while the symbiosome space between the symbiosome membrane and bacteria consists of proteins and metabolites from the rhizobium and plant. In the unique microenvironment, symbiosome proteins likely perform multiple tasks via their moonlighting functions, accounting for the many unsolved questions associated with symbiotic nitrogen fixation. In this review, we outline the current knowledge regarding the composition and potential moonlighting functions of symbiosome proteins. We highlight our current understanding of emergent symbiosome properties closely tied to nitrogen fixation activity. Ultimately, we discuss the challenges and opportunities for discovering new paradigms in symbiosome biology using recently developed technologies.