Bacterial peptidoglycan (murein) hydrolases

Vollmer, Waldemar; Joris, Bernard; Charlier, Paulette; Foster, Simon J.

doi:10.1111/j.1574-6976.2007.00099.x

Cited by 761 publications

(892 citation statements)

References 286 publications

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“…In E. coli, amidases and/or their activators localize sharply to the septal ring (39)(40)(41). It is not known whether E. coli LTs also accumulate at the midcell, but most are anchored to the outer membrane, and this anchoring presumably causes them to lag behind the amidases during cell division (7,24). Whatever the underlying mechanism, sequential activity of amidases and enzymes that cleave the glycan backbone is likely to be an ancient and widespread feature of bacterial cell division because it pertains in both E. coli and B. subtilis, organisms that diverged at least 1 billion years ago.…”

Section: Discussionmentioning

confidence: 99%

“…In many bacteria, including E. coli, the glycan backbone of PG is degraded by LTs that cleave the β-1,4 glycosidic bond via a mechanism that creates a 1,6-anhydroMurNAc end (7,24,25). Thus, denuded glycans generated by cell-wall amidases are expected to persist longer and accumulate to higher than normal levels in an LT mutant.…”

Section: Spor Domains Bind Septal Regions Of Purifiedmentioning

confidence: 99%

“…The glycans are built from a repeating disaccharide of β-1,4-linked N-acetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc), from which branch the oligopeptides that mediate cross-linking. During cell division, a new PG wall is assembled between the incipient daughter cells (5,6), and subsequent cell separation depends on the activity of a collection of PG hydrolases that cleave various bonds in the PG mesh (7).…”

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Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Yahashiri

Jorgenson

Weiss

2015

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

142

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Bacterial SPOR domains bind peptidoglycan (PG) and are thought to target proteins to the cell division site by binding to "denuded" glycan strands that lack stem peptides, but uncertainties remain, in part because septal-specific binding has yet to be studied in a purified system. Here we show that fusions of GFP to SPOR domains from the Escherichia coli cell-division proteins DamX, DedD, FtsN, and RlpA all localize to septal regions of purified PG sacculi obtained from E. coli and Bacillus subtilis. Treatment of sacculi with an amidase that removes stem peptides enhanced SPOR domain binding, whereas treatment with a lytic transglycosylase that removes denuded glycans reduced SPOR domain binding. These findings demonstrate unequivocally that SPOR domains localize by binding to septal PG, that the physiologically relevant binding site is indeed a denuded glycan, and that denuded glycans are enriched in septal PG rather than distributed uniformly around the sacculus. Accumulation of denuded glycans in the septal PG of both E. coli and B. subtilis, organisms separated by 1 billion years of evolution, suggests that sequential removal of stem peptides followed by degradation of the glycan backbone is an ancient feature of PG turnover during bacterial cell division. Linking SPOR domain localization to the abundance of a structure (denuded glycans) present only transiently during biogenesis of septal PG provides a mechanism for coordinating the function of SPOR domain proteins with the progress of cell division.A defining feature of bacteria is the peptidoglycan (PG) cell wall or "sacculus" that confers cell shape, protects the cell against lysis caused by turgor pressure, and is the ultimate target of many clinically relevant antibiotics, including β-lactams and vancomycin (1-4). The structure of PG is characterized by a network of glycan strands connected at regular intervals by oligopeptide cross-links (Fig. 1). The glycans are built from a repeating disaccharide of β-1,4-linked N-acetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc), from which branch the oligopeptides that mediate cross-linking. During cell division, a new PG wall is assembled between the incipient daughter cells (5, 6), and subsequent cell separation depends on the activity of a collection of PG hydrolases that cleave various bonds in the PG mesh (7).In the model Gram-negative bacterium Escherichia coli, daughter-cell separation is driven primarily by three cell-wall amidases (8-10). These enzymes cleave the amide bond that joins the lactyl group of the MurNAc to the α-amino group of the first amino acid (L-Ala) of the stem peptide, releasing as products free oligopeptides and "denuded" glycan strands (Fig. 1). Lytic transglycosylases (LTs) that cleave the MurNAc-GlcNAc glycosidic bond and endopeptidases that cleave stem peptides make minor but still significant contributions to daughter-cell separation (9, 11). In Bacillus subtilis, a model Gram-positive species, the enzymology of daughter-cell separation is not as well characterized. The...

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Section: Discussionmentioning

confidence: 99%

Section: Spor Domains Bind Septal Regions Of Purifiedmentioning

confidence: 99%

mentioning

confidence: 99%

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Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Yahashiri

Jorgenson

Weiss

2015

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

142

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“…High‐molecular‐weight penicillin binding proteins (PBPs) are membrane‐embedded PG‐synthesizing enzymes that possess transglycosylase and/or transpeptidase activities. In B. subtilis , PG degradative enzymes, termed PG hydrolases, are numerous and highly redundant (Smith et al ., 2000; Vollmer et al ., 2008b). They possess a range of hydrolytic activities including recognizing and cutting the bonds between the sugar moieties in the glycan chain (glucosaminidases and muramidases/lytic transglycosylases), between N‐acetyl muramic acid and the peptide stem (amidases) and between specific amino acids in the peptide stems or in the peptide bridges (endopeptidases) (Smith et al ., 2000).…”

Section: Introductionmentioning

confidence: 99%

Hydrolysis of peptidoglycan is modulated by amidation of meso‐diaminopimelic acid and Mg²⁺ in Bacillus subtilis

Dajkovic

Tesson

Chauhan

et al. 2017

Molecular Microbiology

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SummaryThe ability of excess Mg2+ to compensate the absence of cell wall related genes in Bacillus subtilis has been known for a long time, but the mechanism has remained obscure. Here, we show that the rigidity of wild‐type cells remains unaffected with excess Mg2+, but the proportion of amidated meso‐diaminopimelic (mDAP) acid in their peptidoglycan (PG) is significantly reduced. We identify the amidotransferase AsnB as responsible for mDAP amidation and show that the gene encoding it is essential without added Mg2+. Growth without excess Mg2+ causes ΔasnB mutant cells to deform and ultimately lyse. In cell regions with deformations, PG insertion is orderly and indistinguishable from the wild‐type. However, PG degradation is unevenly distributed along the sidewalls. Furthermore, ΔasnB mutant cells exhibit increased sensitivity to antibiotics targeting the cell wall. These results suggest that absence of amidated mDAP causes a lethal deregulation of PG hydrolysis that can be inhibited by increased levels of Mg2+. Consistently, we find that Mg2+ inhibits autolysis of wild‐type cells. We suggest that Mg2+ helps to maintain the balance between PG synthesis and hydrolysis in cell wall mutants where this balance is perturbed in favor of increased degradation.

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“…Bacterial peptidoglycan forms a network of linear polysaccharide strands of alternating Nacetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc) residues cross-linked by short polypeptides. As a giant bag-shaped sacculus, peptidoglycan expands via the action of endopeptidases, amidases, and lytic transglycosylases that cleave covalent bonds and allow insertion of new subunits (1). In contrast, the growing plant cell wall is formed from a scaffold of cellulose microfibrils tethered together by branched glycans such as xyloglucan or arabinoxylan that bind noncovalently to cellulose surfaces.…”

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confidence: 99%

Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization

Kerff

Amoroso

Herman

et al. 2008

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

Self Cite

183

291

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We solved the crystal structure of a secreted protein, EXLX1, encoded by the yoaJ gene of Bacillus subtilis. Its structure is remarkably similar to that of plant ␤-expansins (group 1 grass pollen allergens), consisting of 2 tightly packed domains (D1, D2) with a potential polysaccharide-binding surface spanning the 2 domains. Domain D1 has a double-␤-barrel fold with partial conservation of the catalytic site found in family 45 glycosyl hydrolases and in the MltA family of lytic transglycosylases. Domain D2 has an Ig-like fold similar to group 2/3 grass pollen allergens, with structural features similar to a type A carbohydratebinding domain. EXLX1 bound to plant cell walls, cellulose, and peptidoglycan, but it lacked lytic activity against a variety of plant cell wall polysaccharides and peptidoglycan. EXLX1 promoted plant cell wall extension similar to, but 10 times weaker than, plant ␤-expansins, which synergistically enhanced EXLX1 activity. Deletion of the gene encoding EXLX1 did not affect growth or peptidoglycan composition of B. subtilis in liquid medium, but slowed lysis upon osmotic shock and greatly reduced the ability of the bacterium to colonize maize roots. The presence of EXLX1 homologs in a small but diverse set of plant pathogens further supports a role in plant-bacterial interactions. Because plant expansins have proved difficult to express in active form in heterologous systems, the discovery of a bacterial homolog opens the door for detailed structural studies of expansin function.family 45 endoglucanase ͉ lytic transglycosylase ͉ peptidoglycan ͉ plant cell wall ͉ plant-microbe interactions B acterial and plant cell walls have similar functions but distinctive structures. Bacterial peptidoglycan forms a network of linear polysaccharide strands of alternating Nacetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc) residues cross-linked by short polypeptides. As a giant bag-shaped sacculus, peptidoglycan expands via the action of endopeptidases, amidases, and lytic transglycosylases that cleave covalent bonds and allow insertion of new subunits (1). In contrast, the growing plant cell wall is formed from a scaffold of cellulose microfibrils tethered together by branched glycans such as xyloglucan or arabinoxylan that bind noncovalently to cellulose surfaces. The cellulose-hemicellulose network enlarges via polymer slippage or ''creep,'' mechanically powered by turgorgenerated forces in the cell wall and catalyzed by expansins and other wall-loosening agents (2).Expansins are known principally from plants where they function in cell enlargement and other developmental events requiring cell wall loosening (3). Canonical expansins are small proteins (Ϸ26 kDa, Ϸ225 aa) consisting of 2 compact domains: D1 has a fold similar to that of family 45 glycosyl hydrolases (GH45), and D2 has a ␤-sandwich fold. Expansins facilitate cell wall creep without breakdown of wall polymers (3-5). Plant expansins consist of 2 major families: ␣-expansins, which preferentially loosen the cell walls of dicots compa...

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Bacterial peptidoglycan (murein) hydrolases

Cited by 761 publications

References 286 publications

Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Hydrolysis of peptidoglycan is modulated by amidation of meso‐diaminopimelic acid and Mg²⁺ in Bacillus subtilis

Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization

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Bacterial peptidoglycan (murein) hydrolases

Cited by 761 publications

References 286 publications

Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides

Hydrolysis of peptidoglycan is modulated by amidation of meso‐diaminopimelic acid and Mg2+ in Bacillus subtilis

Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization

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Hydrolysis of peptidoglycan is modulated by amidation of meso‐diaminopimelic acid and Mg²⁺ in Bacillus subtilis