Extracellular Vesicle-Driven Crosstalk between Legume Plants and Rhizobia: The Peribacteroid Space of Symbiosomes as a Protein Trafficking Interface

Prokaryotes and eukaryotes secrete extracellular vesicles
(EVs)
into the surrounding milieu to preserve and transport elevated concentrations
of biomolecules across long distances. EVs encapsulate metabolites,
DNA, RNA, and proteins, whose abundance and composition fluctuate
depending on environmental cues. EVs are involved in eukaryote-to-prokaryote
communication owing to their ability to navigate different ecological
niches and exchange molecular cargo between the two domains. Among
the different bacterium–host relationships, rhizobium–legume
symbiosis is one of the closest known to nature. A crucial developmental
stage of symbiosis is the formation of N2-fixing root nodules
by the plant. These nodules contain endocytosed rhizobiacalled
bacteroidsconfined by plant-derived peribacteroid membranes.
The unrestricted interface between the bacterial external membrane
and the peribacteroid membrane is the peribacteroid space. Many molecular
aspects of symbiosis have been studied, but the interbacterial and
interdomain molecule trafficking by EVs in the peribacteroid space
has not been questioned yet. Here, we unveil intensive EV trafficking
within the symbiosome interface of several rhizobium–legume
dual systems by developing a robust EV isolation procedure. We analyze
the EV-encased proteomes from the peribacteroid space of each bacterium–host
partnership, uncovering both conserved and differential traits of
every symbiotic system. This study opens the gates for designing EV-based
biotechnological tools for sustainable agriculture.