A new factor controlling cell envelope integrity in <i>Alphaproteobacteria</i> in the context of cell cycle, stress response and infection

Beroual, Wanassa; Biondi, Emanuele G.

doi:10.1111/mmi.14201

Cited by 2 publications

(3 citation statements)

References 19 publications

(19 reference statements)

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“…Detection of NifH by Western blotting was performed using a commercial polyclonal antibody against a NifH peptide (Agrisera). Western blotting was carried out as previously described ( 62 ), using bacterial exponential (OD 600 = 0.5)- and stationary (OD 600 > 2.5)-phase cultures as well as 14-dpi nodule-extracted bacteroids.…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2021

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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.

show abstract

Section: Methodsmentioning

confidence: 99%

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

et al. 2021

View full text Add to dashboard Cite

show abstract

“…Detection of NifH by western blotting was performed using a commercial polyclonal antibody against a NifH peptide (Agrisera) respectively. The western blotting was carried out as previously described 61 using bacterial exponential (OD 600nm = 0.5) and stationary (OD 600nm > 2.5) phase cultures as well as 14 dpi nodule-extracted bacteroids.…”

Section: Methodsmentioning

confidence: 99%

Section: Western Blot Analysismentioning

confidence: 99%

Bradyrhizobium diazoefficiensUSDA110 nodulation ofAeschynomene afrasperais associated with atypical terminal bacteroid differentiation and suboptimal symbiotic efficiency

Nicoud

Lamouche

Chaumeret

et al. 2020

Preprint

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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 is varying from non-fixing 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 membrane permeability leading to loss of bacterial viability while plants increase their symbiotic benefit. A combination of plant metabolomics, bacterial proteomics and transcriptomics along with cytological analyses was used to study the physiology of USDA110 bacteroids in these two host plants. We show that USDA110 establish a poorly efficient symbiosis with A. afraspera, despite the full activation of the bacterial symbiotic program. We found molecular signatures of high level 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 an 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 co-evolve with such a host.ImportanceLegume-rhizobium symbiosis is a major ecological process in the nitrogen cycle, responsible for the main input of fixed nitrogen in the biosphere. The efficiency of this symbiosis relies on the coevolution of the partners. Some legume plants, but not all, 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 reduce their viability. We combined multi-omics with physiological analyses to show that the non-natural symbiotic couple formed by Bradyrhizobium diazoefficiens USDA110 and Aeschynomene afraspera is functional but displays a low symbiotic efficiency associated to a disconnection of terminal bacteroid differentiation features.

show abstract

A new factor controlling cell envelope integrity in Alphaproteobacteria in the context of cell cycle, stress response and infection

Cited by 2 publications

References 19 publications

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

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

Bradyrhizobium diazoefficiensUSDA110 nodulation ofAeschynomene afrasperais associated with atypical terminal bacteroid differentiation and suboptimal symbiotic efficiency

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