Bradyrhizobium diazoefficiens USDA110 Nodulation of Aeschynomene afraspera Is Associated with Atypical Terminal Bacteroid Differentiation and Suboptimal Symbiotic Efficiency

Nicoud, Quentin and Lamouche, Florian and Chaumeret, Anais and Balliau, Thierry and Le Bars, Romain and Nagy, István and Kereszt, Attila (2021) Bradyrhizobium diazoefficiens USDA110 Nodulation of Aeschynomene afraspera Is Associated with Atypical Terminal Bacteroid Differentiation and Suboptimal Symbiotic Efficiency. MSYSTEMS, 6 (3). ISSN 2379-5077

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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.

Item Type: Article
Additional Information: Funding Agency and Grant Number: Universite Paris-Sud; France-BioImagingFrench National Research Agency (ANR) [ANR-10-INBS-04-01]; Labex Saclay Plant Sciences [ANR-11-IDEX-0003-02]; Agence Nationale de la RechercheFrench National Research Agency (ANR)European Commission [ANR-13-BSV7-0013, ANR-17-CE20-0011]; National Office for Research, Development and Innovation of Hungary [120120] Funding text: Quentin Nicoud and Florian Lamouche were supported by a Ph.D. fellowship from the Universite Paris-Sud. The present work has benefited from the core facilities of Imagerie-Gif (, a member of IBiSA (, supported by France-BioImaging (ANR-10-INBS-04-01), and the Labex Saclay Plant Sciences (ANR-11-IDEX-0003-02). This work was funded by the Agence Nationale de la Recherche, grant no. ANR-13-BSV7-0013 and ANR-17-CE20-0011, and used resources from the National Office for Research, Development and Innovation of Hungary, grant no. 120120 to Attila Kereszt.
Uncontrolled Keywords: PEPTIDES; PROTEIN; GENES; PLANT; Cell Differentiation; ROOT; proteomics; metabolomics; MEDICAGO-TRUNCATULA; nitrogen fixation; legume-rhizobium symbiosis; STRAIN ORS285;
Subjects: Q Science / természettudomány > QH Natural history / természetrajz > QH301 Biology / biológia > QH3011 Biochemistry / biokémia
Q Science / természettudomány > QK Botany / növénytan > QK10 Plant physiology / növényélettan
Q Science / természettudomány > QR Microbiology / mikrobiológia
Depositing User: MTMT SWORD
Date Deposited: 07 Feb 2022 10:33
Last Modified: 07 Feb 2022 10:33

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