Oxygen and derived reactive species in legume-rhizobia interactions: paradoxes and dual roles.

Abstract

Biological nitrogen (N2) fixation between legumes and rhizobia is the result of a symbiosis characterized by the formation of a new organ, the nodule, in which the plants house and feed the bacteria. Oxygen (O2) concentration inside the nodule is very low (of the order of a few tens of nanomolar). The nitrogenase responsible for the reduction of atmospheric N2 to ammonia is irreversibly inhibited by traces of O2, while O2 is required for the overall process of N2 fixation which consumes high amounts of energy and reducing power. How is this paradox solved? The setting up of a physical and chemical O2 diffusion barrier, including the synthesis of numerous leghemoglobins, a class of hemoproteins with a very high O2 absorption capacity, was evidenced. However, why are so many leghemoglobin genes present when they appear to be mainly expressed in the same nodule zone? Furthermore, why do the bacterial symbionts contain multiple O2 sensors despite the existence of a very low O2 tension inside the nodule? On the other hand, reactive oxygen species (ROS), which play important metabolic and signaling roles in symbiosis, appear to act as Janus molecules, exhibiting opposite effects throughout symbiosis establishment and nodule life. We aim to provide possible answers to the questions asked and to highlight the dual roles of ROS in nodule development, functioning, and senescence.