Protection of Sinorhizobium against Host Cysteine-Rich Antimicrobial Peptides Is Critical for Symbiosis

Haag, Andreas F.; Baloban, Mikhail; Sani, Monica; Kerscher, Bernhard; Pierre, Olivier; Farkas, Attila; Longhi, Renato; Boncompagni, Éric; Hérouart, Didier; Dall’Angelo, Sergio; Kondorosi, Éva; Zanda, Matteo; Mergaert, Peter; Ferguson, Gail P.

doi:10.1371/journal.pbio.1001169

Cited by 169 publications

(271 citation statements)

References 34 publications

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“…This indicates an increased porosity of nitrogen-fixing vesicles relative to vegetative hyphae in host cells. This observation contrasts with those obtained from the Rhizobium-legume nodules, where the nitrogenfixing Rhizobium bacteria were not stained with PI (Haag et al, 2011). However, our observations confirm a previous hypothesis proposing that the permeability of vesicles in nodules is higher than that of in vitro vesicles (Tisa and Richards, 2004).…”

Section: Discussioncontrasting

confidence: 77%

Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia

et al. 2015

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Actinorhizal plant growth in pioneer ecosystems depends on the symbiosis with the nitrogen-fixing actinobacterium Frankia cells that are housed in special root organs called nodules. Nitrogen fixation occurs in differentiated Frankia cells known as vesicles. Vesicles lack a pathway for assimilating ammonia beyond the glutamine stage and are supposed to transfer reduced nitrogen to the plant host cells. However, a mechanism for the transfer of nitrogen-fixation products to the plant cells remains elusive. Here, new elements for this metabolic exchange are described. We show that Alnus glutinosa nodules express defensin-like peptides, and one of these, Ag5, was found to target Frankia vesicles. In vitro and in vivo analyses showed that Ag5 induces drastic physiological changes in Frankia, including an increased permeability of vesicle membranes. A significant release of nitrogen-containing metabolites, mainly glutamine and glutamate, was found in N 2 -fixing cultures treated with Ag5. This work demonstrates that the Ag5 peptide is central for Frankia physiology in nodules and uncovers a novel cellular function for this large and widespread defensin peptide family.

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Section: Discussioncontrasting

confidence: 77%

Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia

et al. 2015

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“…BacA is essential for bacteroid development (37), and it has been proposed to protect bacteria from host-derived NCR peptides during the instauration of symbiosis (38). BacA is thought to reduce the extent of cytoplasmic membrane damage due to nodule-specific cysteine-rich (NCR) peptides, possibly by mediating their uptake into the cytoplasm, thus reducing their local concentration at the membrane level.…”

Section: Mode Of Action Of Bac7(1-35) Against P Aeruginosamentioning

confidence: 99%

The Mechanism of Killing by the Proline-Rich Peptide Bac7(1–35) against Clinical Strains of Pseudomonas aeruginosa Differs from That against Other Gram-Negative Bacteria

Runti

Benincasa

Giuffrida

et al. 2017

Antimicrob Agents Chemother

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Pseudomonas aeruginosa infections represent a serious threat to worldwide health. Proline-rich antimicrobial peptides (PR-AMPs), a particular group of peptide antibiotics, have demonstrated in vitro activity against P. aeruginosa strains. Here we show that the mammalian PR-AMP Bac7(1-35) is active against some multidrug-resistant cystic fibrosis isolates of P. aeruginosa. By confocal microscopy and cytometric analyses, we investigated the mechanism of killing against P. aeruginosa strain PAO1 and three selected isolates, and we observed that the peptide inactivated the target cells by disrupting their cellular membranes. This effect is deeply different from that previously described for PR-AMPs in Escherichia coli and Salmonella enterica serovar Typhimurium, where these peptides act intracellularly after having been internalized by means of the transporter SbmA without membranolytic effects. The heterologous expression of SbmA in PAO1 cells enhanced the internalization of Bac7(1-35) into the cytoplasm, making the bacteria more susceptible to the peptide but at the same time more resistant to the membrane lysis, similarly to what occurs in E. coli. The results evidenced a new mechanism of action for PRAMPs and indicate that Bac7 has multiple and variable modes of action that depend on the characteristics of the different target species and the possibility to be internalized by bacterial transporters. This feature broadens the spectrum of activity of the peptide and makes the development of peptide-resistant bacteria a more difficult process.

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“…Recent research has established that NCR peptides are both required and sufficient to drive differentiation of intracellular S. meliloti bacteroids (3,4). Remarkably, in vitro treatment of S. meliloti with sublethal levels of individual cationic NCR peptides also increases bacterial size and ploidy, indicating that at least some of the symbiotically important effects of NCR peptides can be observed ex planta (4,9). NCR peptides have been postulated to mediate the increase in S. meliloti ploidy by altering its cell cycle (4), which is a highly regulated process involving sequential changes in gene expression (10).…”

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“…In addition to provoking bacteroid differentiation, NCR peptides exhibit antimicrobial activity (4,9,11). NCR peptides are similar to plant defensins, which are antimicrobial peptides (AMPs) that function in the innate immune response (4,12,13).…”

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confidence: 99%

“…NCR peptides are similar to plant defensins, which are antimicrobial peptides (AMPs) that function in the innate immune response (4,12,13). Investigations of a small number of synthesized NCR peptides have revealed that at high concentrations some of these peptides display potent antimicrobial activity against S. meliloti as well as other bacterial species (4,9,11). Work by Gail Ferguson and colleagues (9) provided strong evidence that NCR peptides are also antimicrobial in planta; mutation of the S. meliloti bacA gene, which codes for an inner membrane protein (14), increases the sensitivity of bacteria to the cytotoxic effects of NCR peptides Significance Sinorhizobium meliloti and its legume hosts establish a symbiosis in which bacterial fixed nitrogen is exchanged for plant carbon compounds.…”

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Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called "nodule-specific cysteine-rich" (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.rhizobia-legume | host-microbe interactions

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Protection of Sinorhizobium against Host Cysteine-Rich Antimicrobial Peptides Is Critical for Symbiosis

Abstract: A bacterial membrane protein, BacA, protects Sinorhizobium meliloti against the antimicrobial activity of host peptides, enabling the peptides to induce bacterial persistence rather than bacterial death.

Cited by 169 publications

References 34 publications

Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia

Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia

The Mechanism of Killing by the Proline-Rich Peptide Bac7(1–35) against Clinical Strains of Pseudomonas aeruginosa Differs from That against Other Gram-Negative Bacteria

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

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