Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins
ABSTRACT Lectin-like bacteriocins (LlpAs) are secreted by proteobacteria and selectively kill strains of their own or related species, and they are composed of two B-lectin domains with divergent sequences. In Pseudomonas spp., initial binding of these antibacterial proteins to cells is mediated by...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-05-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02138-17 |
| _version_ | 1818740145977819136 |
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| author | Maarten G. K. Ghequire Toon Swings Jan Michiels Susan K. Buchanan René De Mot |
| author_facet | Maarten G. K. Ghequire Toon Swings Jan Michiels Susan K. Buchanan René De Mot |
| author_sort | Maarten G. K. Ghequire |
| collection | DOAJ |
| description | ABSTRACT Lectin-like bacteriocins (LlpAs) are secreted by proteobacteria and selectively kill strains of their own or related species, and they are composed of two B-lectin domains with divergent sequences. In Pseudomonas spp., initial binding of these antibacterial proteins to cells is mediated by the carboxy-terminal domain through d-rhamnose residues present in the common polysaccharide antigen of their lipopolysaccharide, whereas the amino-terminal domain accounts for strain selectivity of killing. Here, we show that spontaneous LlpA-resistant mutants carry mutations in one of three surface-exposed moieties of the essential β-barrel outer membrane protein insertase BamA, the core component of the BAM complex. Polymorphism of this loop in different Pseudomonas groups is linked to LlpA susceptibility, and targeted cells all share the same signature motif in this loop. Since heterologous expression of such a bamA gene confers LlpA susceptibility upon a resistant strain, BamA represents the primary bacteriocin selectivity determinant in pseudomonads. Contrary to modular bacteriocins that require uptake via the Tol or Ton system, parasitism of BamA as an LlpA receptor advocates a novel bacteriocin killing mechanism initiated by impairment of the BAM machinery. IMPORTANCE Bacteria secrete a variety of molecules to eliminate microbial rivals. Bacteriocins are a pivotal group of peptides and proteins that assist in this fight, specifically killing related bacteria. In Gram-negative bacteria, these antibacterial proteins often comprise distinct domains for initial binding to a target cell’s surface and subsequent killing via enzymatic or pore-forming activity. Here, we show that lectin-like bacteriocins, a family of bacteriocins that lack the prototypical modular toxin architecture, also stand out by parasitizing BamA, the core component of the outer membrane protein assembly machinery. A particular surface-exposed loop of BamA, critical for its function, serves as a key discriminant for cellular recognition, and polymorphisms in this loop determine whether a strain is susceptible or immune to a particular bacteriocin. These findings suggest a novel mechanism of contact-dependent killing that does not require cellular uptake. The evolutionary advantage of piracy of an essential cellular compound is highlighted by the observation that contact-dependent growth inhibition, a distinct antagonistic system, can equally take advantage of this receptor. |
| first_indexed | 2024-12-18T01:36:05Z |
| format | Article |
| id | doaj.art-229b9fcf21094038bbc8a62a295cc881 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T01:36:05Z |
| publishDate | 2018-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-229b9fcf21094038bbc8a62a295cc8812022-12-21T21:25:26ZengAmerican Society for MicrobiologymBio2150-75112018-05-019210.1128/mBio.02138-17Hitting with a BAM: Selective Killing by Lectin-Like BacteriocinsMaarten G. K. Ghequire0Toon Swings1Jan Michiels2Susan K. Buchanan3René De Mot4Centre of Microbial and Plant Genetics, KU Leuven, Heverlee, BelgiumCentre of Microbial and Plant Genetics, KU Leuven, Heverlee, BelgiumCentre of Microbial and Plant Genetics, KU Leuven, Heverlee, BelgiumLaboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, USACentre of Microbial and Plant Genetics, KU Leuven, Heverlee, BelgiumABSTRACT Lectin-like bacteriocins (LlpAs) are secreted by proteobacteria and selectively kill strains of their own or related species, and they are composed of two B-lectin domains with divergent sequences. In Pseudomonas spp., initial binding of these antibacterial proteins to cells is mediated by the carboxy-terminal domain through d-rhamnose residues present in the common polysaccharide antigen of their lipopolysaccharide, whereas the amino-terminal domain accounts for strain selectivity of killing. Here, we show that spontaneous LlpA-resistant mutants carry mutations in one of three surface-exposed moieties of the essential β-barrel outer membrane protein insertase BamA, the core component of the BAM complex. Polymorphism of this loop in different Pseudomonas groups is linked to LlpA susceptibility, and targeted cells all share the same signature motif in this loop. Since heterologous expression of such a bamA gene confers LlpA susceptibility upon a resistant strain, BamA represents the primary bacteriocin selectivity determinant in pseudomonads. Contrary to modular bacteriocins that require uptake via the Tol or Ton system, parasitism of BamA as an LlpA receptor advocates a novel bacteriocin killing mechanism initiated by impairment of the BAM machinery. IMPORTANCE Bacteria secrete a variety of molecules to eliminate microbial rivals. Bacteriocins are a pivotal group of peptides and proteins that assist in this fight, specifically killing related bacteria. In Gram-negative bacteria, these antibacterial proteins often comprise distinct domains for initial binding to a target cell’s surface and subsequent killing via enzymatic or pore-forming activity. Here, we show that lectin-like bacteriocins, a family of bacteriocins that lack the prototypical modular toxin architecture, also stand out by parasitizing BamA, the core component of the outer membrane protein assembly machinery. A particular surface-exposed loop of BamA, critical for its function, serves as a key discriminant for cellular recognition, and polymorphisms in this loop determine whether a strain is susceptible or immune to a particular bacteriocin. These findings suggest a novel mechanism of contact-dependent killing that does not require cellular uptake. The evolutionary advantage of piracy of an essential cellular compound is highlighted by the observation that contact-dependent growth inhibition, a distinct antagonistic system, can equally take advantage of this receptor.https://journals.asm.org/doi/10.1128/mBio.02138-17BamALlpAkin discriminationouter membrane proteinspolymorphismtarget receptor |
| spellingShingle | Maarten G. K. Ghequire Toon Swings Jan Michiels Susan K. Buchanan René De Mot Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins mBio BamA LlpA kin discrimination outer membrane proteins polymorphism target receptor |
| title | Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins |
| title_full | Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins |
| title_fullStr | Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins |
| title_full_unstemmed | Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins |
| title_short | Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins |
| title_sort | hitting with a bam selective killing by lectin like bacteriocins |
| topic | BamA LlpA kin discrimination outer membrane proteins polymorphism target receptor |
| url | https://journals.asm.org/doi/10.1128/mBio.02138-17 |
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