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...

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Autores principales:	Maarten G. K. Ghequire, Toon Swings, Jan Michiels, Susan K. Buchanan, René De Mot
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	BamA LlpA kin discrimination outer membrane proteins polymorphism target receptor Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/229b9fcf21094038bbc8a62a295cc881
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spelling	oai:doaj.org-article:229b9fcf21094038bbc8a62a295cc8812021-11-15T15:53:27ZHitting with a BAM: Selective Killing by Lectin-Like Bacteriocins10.1128/mBio.02138-172150-7511https://doaj.org/article/229b9fcf21094038bbc8a62a295cc8812018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02138-17https://doaj.org/toc/2150-7511ABSTRACT 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.Maarten G. K. GhequireToon SwingsJan MichielsSusan K. BuchananRené De MotAmerican Society for MicrobiologyarticleBamALlpAkin discriminationouter membrane proteinspolymorphismtarget receptorMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	BamA LlpA kin discrimination outer membrane proteins polymorphism target receptor Microbiology QR1-502
spellingShingle	BamA LlpA kin discrimination outer membrane proteins polymorphism target receptor Microbiology QR1-502 Maarten G. K. Ghequire Toon Swings Jan Michiels Susan K. Buchanan René De Mot Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins
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.
format	article
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
title	Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins
title_short	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_sort	hitting with a bam: selective killing by lectin-like bacteriocins
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/229b9fcf21094038bbc8a62a295cc881
work_keys_str_mv	AT maartengkghequire hittingwithabamselectivekillingbylectinlikebacteriocins AT toonswings hittingwithabamselectivekillingbylectinlikebacteriocins AT janmichiels hittingwithabamselectivekillingbylectinlikebacteriocins AT susankbuchanan hittingwithabamselectivekillingbylectinlikebacteriocins AT renedemot hittingwithabamselectivekillingbylectinlikebacteriocins
_version_	1718427261172973568

Hitting with a BAM: Selective Killing by Lectin-Like Bacteriocins

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