Abstract
Legume plants can form root organs called nodules where they house intracellular symbiotic rhizobium bacteria. Within nodule cells, rhizobia differentiate into bacteroids, which fix nitrogen for the benefit of the plant. Depending on the combination of host plants and rhizobial strains, the output of rhizobium-legume interactions varies from nonfixing associations to symbioses that are highly beneficial for the plant. Bradyrhizobium diazoefficiens USDA110 was isolated as a soybean symbiont, but it can also establish a functional symbiotic interaction with Aeschynomene afraspera In contrast to soybean, A. afraspera triggers terminal bacteroid differentiation, a process involving bacterial cell elongation, polyploidy, and increased membrane permeability, leading to a loss of bacterial viability while plants increase their symbiotic benefit. A combination of plant metabolomics, bacterial proteomics, and transcriptomics along with cytological analyses were used to study the physiology of USDA110 bacteroids in these two host plants. We show that USDA110 establishes a poorly efficient symbiosis with A. afraspera despite the full activation of the bacterial symbiotic program. We found molecular signatures of high levels of stress in A. afraspera bacteroids, whereas those of terminal bacteroid differentiation were only partially activated. Finally, we show that in A. afraspera, USDA110 bacteroids undergo atypical terminal differentiation hallmarked by the disconnection of the canonical features of this process. This study pinpoints how a rhizobium strain can adapt its physiology to a new host and cope with terminal differentiation when it did not coevolve with such a host.IMPORTANCE Legume-rhizobium symbiosis is a major ecological process in the nitrogen cycle, responsible for the main input of fixed nitrogen into the biosphere. The efficiency of this symbiosis relies on the coevolution of the partners. Some, but not all, legume plants optimize their return on investment in the symbiosis by imposing on their microsymbionts a terminal differentiation program that increases their symbiotic efficiency but imposes a high level of stress and drastically reduces their viability. We combined multi-omics with physiological analyses to show that the symbiotic couple formed by Bradyrhizobium diazoefficiens USDA110 and Aeschynomene afraspera, in which the host and symbiont did not evolve together, is functional but displays a low symbiotic efficiency associated with a disconnection of terminal bacteroid differentiation features.
Highlights
IMPORTANCE Legume-rhizobium symbiosis is a major ecological process in the nitrogen cycle, responsible for the main input of fixed nitrogen into the biosphere
Bradyrhizobium Differentiation in Aeschynomene msystems.asm.org 3 a phylogenetically distant host belonging to the dalbergioid clade that naturally interacts with photosynthetic rhizobia such as Bradyrhizobium sp. strain ORS285 (Fig. 1A to C) [14,15,16,17,18]
The plants inoculated with ORS285 are clearly much larger than the ones inoculated with USDA110 at later time points (21 days postinoculation [dpi]) (Fig. 1C), validating our conclusions drawn from the physiological analysis at 14 dpi that USDA110 is a poor symbiotic partner for A. afraspera, the symbiosis is functional
Summary
IMPORTANCE Legume-rhizobium symbiosis is a major ecological process in the nitrogen cycle, responsible for the main input of fixed nitrogen into the biosphere. Plants of the legume family acquired the capacity to form symbiotic associations with soil bacteria, the rhizobia, which fix atmospheric nitrogen for the plants’ benefit. These symbiotic associations lead to the development of rhizobium-housing root organs called nodules. Increased permeability of the bacteroid envelope occurs during TBD, most probably due to the interaction of NCR peptides with bacterial membranes [6, 7, 10, 12] Together, these alterations of bacteroid physiology are associated with a strongly decreased viability of the differentiated bacteria, which fail to recover growth when extracted from nodules [6]. We find that USDA110 undergoes terminal but atypical bacteroid differentiation in A. afraspera with reduced cell viability and increased membrane permeability, while cell size and ploidy levels remain unchanged
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