Peptidoglycan reshaping by a noncanonical peptidase for helical cell shape in Campylobacter jejuni

Min, Kyoung‐Wook; An, Doo Ri; Yoon, Hye‐Jin; Rana, Neha; Park, Jisu; Kim, Jinshil; Lee, Mijoon; Hesek, Dušan; Ryu, Sangryeol; Kim, B. Moon; Mobashery, Shahriar; Suh, Se Won; Lee, Hyung Ho

doi:10.1038/s41467-019-13934-4

Cited by 15 publications

(14 citation statements)

References 43 publications

(63 reference statements)

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“…PG hydrolases have an additional role generally in the determination of cell shape 17 , which has been particularly studied in the non-predatory, -proteobacteria Helicobacter pylori 18,19,20 and Campylobacter jejuni 21,22,23 , in whom multiple PG hydrolases collectively generate helical morphology. In contrast, bacterial vibrioid morphology is generally determined by non-enzymatic cyto-or periskeletal proteins (well-studied in Caulobacter crescentus 24,25 and Vibrio cholerae 26 ).…”

Section: Introductionmentioning

confidence: 99%

Asymmetric peptidoglycan editing generates the curvature of predatory bacteria, optimizing invasion and replication within a spherical prey niche

Banks

Valdivia-Delgado

Biboy

et al. 2021

Preprint

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The vibrioid predatory bacterium Bdellovibrio bacteriovorus secretes prey wall-modifying enzymes to invade and replicate within the periplasm of Gram-negative prey bacteria. Studying self-modification of predator wall peptidoglycan during predation, we discover that Bd1075 generates self-wall curvature by exerting LD-carboxypeptidase activity in the vibrioid B. bacteriovorus strain HD100 as it grows inside spherical prey. Bd1075 localizes to the outer curved face of B. bacteriovorus, in contrast to most known shape-determinants. Asymmetric protein localization is determined by the novel function of a nuclear transport factor 2-like (NTF2) domain at the protein C-terminus. The solved structure of Bd1075 is monomeric, with key differences to other LD-carboxypeptidases. Rod-shaped Δbd1075 mutants invade prey more slowly than curved wild-type predators, and stretch and deform the invaded prey cell from within. Vibrioid morphology increases the evolutionary fitness of wild predatory bacteria, facilitating efficient prey invasion and intracellular growth of curved predators inside a spherical prey niche.

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Section: Introductionmentioning

confidence: 99%

Asymmetric peptidoglycan editing generates the curvature of predatory bacteria, optimizing invasion and replication within a spherical prey niche

Banks

Valdivia-Delgado

Biboy

et al. 2021

Preprint

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“…The LysA from these phages is noteworthy as the protein is nearly 1,100 amino acids making it twice as large as any LysA enzymes described in mycobacteriophages. These LysA proteins have four predicted domains including an N-acetylmuramoyl-L-alanine amidase (Ami-2A), a glycoside hydrolase (GH43 family) [ 62 ], a M23 peptidase (M23) [ 63 , 64 ], and an N-terminal region that may also have additional glycoside activity (GS25?) due to a hit to cd06418 (GS25 family) [ 65 ].…”

Section: Resultsmentioning

confidence: 99%

Bioinformatic characterization of endolysins and holin-like membrane proteins in the lysis cassette of phages that infect Gordonia rubripertincta

2022

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Holins are bacteriophage-encoded transmembrane proteins that function to control the timing of bacterial lysis event, assist with the destabilization of the membrane proton motive force and in some models, generate large “pores” in the cell membrane to allow the exit of the phage-encoded endolysin so they can access the peptidoglycan components of the cell wall. The lysis mechanism has been rigorously evaluated through biochemical and genetic studies in very few phages, and the results indicate that phages utilize endolysins, holins and accessory proteins to the outer membrane to achieve cell lysis through several distinct operational models. This observation suggests the possibility that phages may evolve novel variations of how the lysis proteins functionally interact in an effort to improve fitness or evade host defenses. To begin to address this hypothesis, the current study utilized a comprehensive bioinformatic approach to systematically identify the proteins encoded by the genes within the lysis cassettes in 16 genetically diverse phages that infect the Gram-positive Gordonia rubripertincta NRLL B-16540 strain. The results show that there is a high level of diversity of the various lysis genes and 16 different genome organizations of the putative lysis cassette, many which have never been described. Thirty-four different genes encoding holin-like proteins were identified as well as a potential holin-major capsid fusion protein. The holin-like proteins contained between 1–4 transmembrane helices, were not shared to a high degree amongst the different phages and are present in the lysis cassette in a wide range of combinations of up to 4 genes in which none are duplicated. Detailed evaluation of the transmembrane domains and predicted membrane topologies of the holin-like proteins show that many have novel structures that have not been previously characterized. These results provide compelling support that there are novel operational lysis models yet to be discovered.

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“…Lastly, Pgp3 of Campylobacter jejuni can adopt two conformations: open and closed. In the latter one, loop L1 from the flexible linker that joins its catalytic and binding modules enters the groove and, therefore, regulates the catalysis of Pgp3 ( Min et al, 2020 ). To summarize, the presence of pro-region is a common feature of the M23 peptidases.…”

Section: M23 Peptidasesmentioning

confidence: 99%

One fold, many functions—M23 family of peptidoglycan hydrolases

Razew¹,

Schwarz²,

Mitkowski³

et al. 2022

Front. Microbiol.

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Bacterial cell walls are the guards of cell integrity. They are composed of peptidoglycan that provides rigidity to sustain internal turgor and ensures isolation from the external environment. In addition, they harbor the enzymatic machinery to secure cell wall modulations needed throughout the bacterial lifespan. The main players in this process are peptidoglycan hydrolases, a large group of enzymes with diverse specificities and different mechanisms of action. They are commonly, but not exclusively, found in prokaryotes. Although in most cases, these enzymes share the same molecular function, namely peptidoglycan hydrolysis, they are leveraged to perform a variety of physiological roles. A well-investigated family of peptidoglycan hydrolases is M23 peptidases, which display a very conserved fold, but their spectrum of lytic action is broad and includes both Gram- positive and Gram- negative bacteria. In this review, we summarize the structural, biochemical, and functional studies concerning the M23 family of peptidases based on literature and complement this knowledge by performing large-scale analyses of available protein sequences. This review has led us to gain new insight into the role of surface charge in the activity of this group of enzymes. We present relevant conclusions drawn from the analysis of available structures and indicate the main structural features that play a crucial role in specificity determination and mechanisms of latency. Our work systematizes the knowledge of the M23 family enzymes in the context of their unique antimicrobial potential against drug-resistant pathogens and presents possibilities to modulate and engineer their features to develop perfect antibacterial weapons.

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Peptidoglycan reshaping by a noncanonical peptidase for helical cell shape in Campylobacter jejuni

Cited by 15 publications

References 43 publications

Asymmetric peptidoglycan editing generates the curvature of predatory bacteria, optimizing invasion and replication within a spherical prey niche

Asymmetric peptidoglycan editing generates the curvature of predatory bacteria, optimizing invasion and replication within a spherical prey niche

Bioinformatic characterization of endolysins and holin-like membrane proteins in the lysis cassette of phages that infect Gordonia rubripertincta

One fold, many functions—M23 family of peptidoglycan hydrolases

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