Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation

Quentin Nicoud (1) , Quentin Barrière (1) , Nicolas Busset (1) , Sara Dendene (1) , Dmitrii Travin , Mickaël Bourge (1) , Romain Le Bars (1) , Claire Boulogne (1) , Marie Lecroël (1) , Sándor Jenei , Atilla Kereszt , Eva Kondorosi , Emanuele G Biondi (1) , Tatiana Timchenko (1) , Benoît Alunni (1) , Peter Mergaert (2, 1)

1 I2BC - Institut de Biologie Intégrative de la Cellule
2 CNRS - Centre National de la Recherche Scientifique

Legumes of the Medicago genus have a symbiotic relationship with the bacterium Sinorhizobium meliloti and develop root nodules housing large numbers of intracellular symbionts. Members of the nodule-specific cysteine-rich peptide (NCR) family induce the endosymbionts into a terminal differentiated state. Individual cationic NCRs are antimicrobial peptides that have the capacity to kill the symbiont, but the nodule cell environment prevents killing. Moreover, the bacterial broad-specificity peptide uptake transporter BacA and exopolysaccharides contribute to protect the endosymbionts against the toxic activity of NCRs. Here, we show that other S. meliloti functions participate in the protection of the endosymbionts; these include an additional broad-specificity peptide uptake transporter encoded by the yejABEF genes and lipopolysaccharide modifications mediated by lpsB and lpxXL, as well as rpoH1, encoding a stress sigma factor. Strains with mutations in these genes show a strain-specific increased sensitivity profile against a panel of NCRs and form nodules in which bacteroid differentiation is affected. The lpsB mutant nodule bacteria do not differentiate, the lpxXL and rpoH1 mutants form some seemingly fully differentiated bacteroids, although most of the nodule bacteria are undifferentiated, while the yejABEF mutants form hypertrophied but nitrogen-fixing bacteroids. The nodule bacteria of all the mutants have a strongly enhanced membrane permeability, which is dependent on the transport of NCRs to the endosymbionts. Our results suggest that S. meliloti relies on a suite of functions, including peptide transporters, the bacterial envelope structures, and stress response regulators, to resist the aggressive assault of NCR peptides in the nodule cells.

Domaines: Sciences du Vivant [q-bio]

Quentin Nicoud, Quentin Barrière, Nicolas Busset, Sara Dendene, Dmitrii Travin, et al.. Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation. mBio, 2021, ⟨10.1128/mbio.00895-21⟩. ⟨hal-03302731⟩