How Rhizobia Adapt to the Nodule Environment

Abstract

Rhizobia are a phylogenetically diverse group of soil bacteria that engage in mutualistic interactions with legume plants. Although specifics of the symbioses differ between strains and plants, all symbioses ultimately result in the formation of specialized root nodule organs which host the nitrogen-fixing microsymbionts called bacteroids. Inside nodules, bacteroids encounter unique conditions that necessitate global reprogramming of physiological processes and rerouting of their metabolism. Decades of research have addressed these questions using genetics, omics approaches, and more recently computational modelling. Here we discuss the common adaptations of rhizobia to the nodule environment that define the core principles of bacteroid functioning. All bacteroids are growth-arrested and perform energy-intensive nitrogen fixation fueled by plant-provided C4-dicarboxylates at nanomolar oxygen levels. At the same time, bacteroids are subject to host control and sanctioning that ultimately determine their fitness and have fundamental importance for the evolution of a stable mutualistic relationship.

Differential Expression of Paraburkholderia phymatum Type VI Secretion Systems (T6SS) Suggests a Role of T6SS-b in Early Symbiotic Interaction

“…The rhizobia are then surrounded by a plant membrane forming an organelle like structure called a symbiosome. Within these symbiosomes, the bacteria differentiate into nitrogen-fixing bacteroids ( Udvardi and Poole, 2013 ; Clarke et al, 2014 ; Ledermann et al, 2021 ). The rhizobial enzyme nitrogenase, a complex two-component metalloenzyme that consists of a homodimeric reductase (the Fe protein, encoded by nifH ) and of a heterotetrameric dinitrogenase (the MoFe protein, encoded by nifD and nifK ), reduces N 2 into a plant usable nitrogen form ( Halbleib and Ludden, 2000 ; Dixon and Kahn, 2004 ).…”

Metabolomics and Dual RNA-Sequencing on Root Nodules Revealed New Cellular Functions Controlled by Paraburkholderia phymatum NifA

“…Commonly through infection threads, rhizobia penetrate the deeper plant tissue and are released intracellularly and surrounded by a symbiosome membrane. Inside plant cells, they differentiate into nitrogen-fixing bacteroids [ 13 , 14 ]. The oxygen concentration inside nodules is roughly 11 nM, which corresponds to a 10,000-fold lower concentration compared to aerobic conditions [ 14 , 15 ].…”

“…Inside plant cells, they differentiate into nitrogen-fixing bacteroids [ 13 , 14 ]. The oxygen concentration inside nodules is roughly 11 nM, which corresponds to a 10,000-fold lower concentration compared to aerobic conditions [ 14 , 15 ]. This oxygen-limited environment is important to protect nitrogenase activity and thereby initiate the expression of nitrogen fixation ( nif ) genes [ 14 , 16 ].…”

“…The oxygen concentration inside nodules is roughly 11 nM, which corresponds to a 10,000-fold lower concentration compared to aerobic conditions [ 14 , 15 ]. This oxygen-limited environment is important to protect nitrogenase activity and thereby initiate the expression of nitrogen fixation ( nif ) genes [ 14 , 16 ]. In diazotrophic bacteria and in P. phymatum , the sigma factor RpoN (or sigma-54) and its enhancer binding protein NifA have been shown to be essential for activation of nif gene expression and nitrogenase activity [ 17 , 18 , 19 ].…”

Genome-scale metabolic modelling of lifestyle changes in Rhizobium leguminosarum

“…As a result of this signal exchange, rhizobia are typically entrapped by root hairs and grow down so-called infection threads until they are endocytosed by plant cells in the developing nodule. The bacteria then undergo further cell division and eventually differentiate into bacteroids converting atmospheric N2 into ammonia, which is secreted to the plant host in exchange for carbon sources, mainly dicarboxylates (2)(3)(4).…”