Antimicrobial nodule-specific cysteine-rich peptides disturb the integrity of bacterial outer and inner membranes and cause loss of membrane potential

Mikuláss, Kata R.; Nagy, Krisztina; Bogos, Balázs; Szegletes, Zsolt; Kovács, Eszter; Farkas, Attila; Váró, György; Kondorosi, Éva; Kereszt, Attila

doi:10.1186/s12941-016-0159-8

Cited by 43 publications

(37 citation statements)

References 23 publications

(26 reference statements)

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“…Cationic NCRs Produce a Wide Range of Effects on Rhizobia. Earlier studies showed that cationic NCR247 and NCR335 provoked modifications in cell size and morphology and affected membrane permeability and cell viability in a concentration-dependent manner (9,10,17), general features that might correlate with the charge of the peptides. Similarly, the formation of networklike structures as well as outer membrane vesicles (OMVs) is a phenomenon often caused by the cationic peptides.…”

Section: Discussionmentioning

confidence: 99%

“…However, recent findings have revealed the existence of NCR peptides essential for symbiosis because the deletion of NCR169 or NCR211 impaired differentiation and survival of bacteroids in M. truncatula nodules (12,13). Cationic NCRs perform in vitro antimicrobial activities (15,16) partly by disturbing the integrity of the microbial membranes (17) or by interacting with a wide range of proteins involved in transcription, translation, and cell division in Sinorhizobium meliloti, the rhizobial partner of M. truncatula (9,10,18). Terminal differentiation of bacteroids is a complex process that occurs in coordination with host-cell development and requires various subsets and balanced production of cationic and noncationic NCRs.…”

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confidence: 99%

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Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides

Montiel

Downie

Farkas

et al. 2017

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

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In legume nodules, rhizobia differentiate into nitrogen-fixing forms called bacteroids, which are enclosed by a plant membrane in an organelle-like structure called the symbiosome. In the Inverted Repeat-Lacking Clade (IRLC) of legumes, this differentiation is terminal due to irreversible loss of cell division ability and is associated with genome amplification and different morphologies of the bacteroids that can be swollen, elongated, spherical, and elongated-branched, depending on the host plant. In , this process is orchestrated by nodule-specific cysteine-rich peptides (NCRs) delivered into developing bacteroids. Here, we identified the predicted NCR proteins in 10 legumes representing different subclades of the IRLC with distinct bacteroid morphotypes. Analysis of their expression and predicted sequences establishes correlations between the composition of the NCR family and the morphotypes of bacteroids. Although NCRs have a single origin, their evolution has followed different routes in individual lineages, and enrichment and diversification of cationic peptides has resulted in the ability to impose major morphological changes on the endosymbionts. The wide range of effects provoked by NCRs such as cell enlargement, membrane alterations and permeabilization, and biofilm and vesicle formation is dependent on the amino acid composition and charge of the peptides. These effects are strongly influenced by the rhizobial surface polysaccharides that affect NCR-induced differentiation and survival of rhizobia in nodule cells.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides

Montiel

Downie

Farkas

et al. 2017

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

Self Cite

136

183

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“…Based on the definitive loss of cell division ability of the nitrogen fixing bacteroids in M. truncatula root nodules, it is expected that at least a fraction of the ∼700 NCR peptides can inhibit bacterial cell division and act as antimicrobial agents in vitro. Indeed, in our previous studies we have shown the bactericidal action of several cationic NCR peptides (Van de Velde et al, 2010;Tiricz et al, 2013;Farkas et al, 2014;Mikuláss et al, 2016;Farkas et al, 2017;Farkas et al, 2018). Among them, the mode of action is the best known for NCR247 (Haag et al, 2012;Farkas et al, 2014;Penterman et al, 2014;Arnold et al, 2017).…”

Section: Discussionmentioning

confidence: 96%

Potent Chimeric Antimicrobial Derivatives of the Medicago truncatula NCR247 Symbiotic Peptide

et al. 2020

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In Rhizobium-legume symbiosis, the bacteria are converted into nitrogen-fixing bacteroids. In many legume species, differentiation of the endosymbiotic bacteria is irreversible, culminating in definitive loss of their cell division ability. This terminal differentiation is mediated by plant peptides produced in the symbiotic cells. In Medicago truncatula more than ∼700 nodule-specific cysteine-rich (NCR) peptides are involved in this process. We have shown previously that NCR247 and NCR335 have strong antimicrobial activity on various pathogenic bacteria and identified interaction of NCR247 with many bacterial proteins, including FtsZ and several ribosomal proteins, which prevent bacterial cell division and protein synthesis. In this study we designed and synthetized various derivatives of NCR247, including shorter fragments and various chimeric derivatives. The antimicrobial activity of these peptides was tested on the ESKAPE bacteria; Enterococcus faecalis, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Escherichia coli as a member of Enterobacteriaceae and in addition Listeria monocytogenes and Salmonella enterica. The 12 amino acid long C-terminal half of NCR247, NCR247C partially retained the antimicrobial activity and preserved the multitarget interactions with partners of NCR247. Nevertheless NCR247C became ineffective on S. aureus, P. aeruginosa, and L. monocytogenes. The chimeric derivatives obtained by fusion of NCR247C with other peptide fragments and particularly with a truncated mastoparan sequence significantly increased bactericidal activity and altered the antimicrobial spectrum. The minimal bactericidal concentration of the most potent derivatives was 1.6 µM, which is remarkably lower than that of most classical antibiotics. The killing activity of the NCR247-based chimeric peptides was practically instant. Importantly, these peptides had no hemolytic activity or cytotoxicity on human cells. The properties of these NCR derivatives make them promising antimicrobials for clinical use.

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“…RSS are known to be involved in post-translational modification of proteins [71], and excess RSS in infected cells might cause abnormal modification of symbiosis-related proteins. We do not exclude the possibility that RSS affect the biological activity of bacteroids in infected cells because bacteroids have highly permeable cell membranes [72,73] and are susceptible to their external environment.…”

Section: Discussionmentioning

confidence: 99%

Reactive Sulfur Species Interact with Other Signal Molecules in Root Nodule Symbiosis in Lotus japonicus

et al. 2020

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Reactive sulfur species (RSS) function as strong antioxidants and are involved in various biological responses in animals and bacteria. Few studies; however, have examined RSS in plants. In the present study, we clarified that RSS are involved in root nodule symbiosis in the model legume Lotus japonicus. Polysulfides, a type of RSS, were detected in the roots by using a sulfane sulfur-specific fluorescent probe, SSP4. Supplying the sulfane sulfur donor Na2S3 to the roots increased the amounts of both polysulfides and hydrogen sulfide (H2S) in the roots and simultaneously decreased the amounts of nitric oxide (NO) and reactive oxygen species (ROS). RSS were also detected in infection threads in the root hairs and in infected cells of nodules. Supplying the sulfane sulfur donor significantly increased the numbers of infection threads and nodules. When nodules were immersed in the sulfane sulfur donor, their nitrogenase activity was significantly reduced, without significant changes in the amounts of NO, ROS, and H2S. These results suggest that polysulfides interact with signal molecules such as NO, ROS, and H2S in root nodule symbiosis in L. japonicus. SSP4 and Na2S3 are useful tools for study of RSS in plants.

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Antimicrobial nodule-specific cysteine-rich peptides disturb the integrity of bacterial outer and inner membranes and cause loss of membrane potential

Cited by 43 publications

References 23 publications

Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides

Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides

Potent Chimeric Antimicrobial Derivatives of the Medicago truncatula NCR247 Symbiotic Peptide

Reactive Sulfur Species Interact with Other Signal Molecules in Root Nodule Symbiosis in Lotus japonicus

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