Asymmetric peptidoglycan editing generates cell curvature in Bdellovibrio predatory bacteria

Emma J. Banks; Mauricio Valdivia-Delgado; Jacob Biboy; Amber Wilson; Ian T. Cadby; Waldemar Vollmer; Carey Lambert; Andrew L. Lovering; R. Elizabeth Sockett

doi:10.1038/s41467-022-29007-y

Asymmetric peptidoglycan editing generates cell curvature in Bdellovibrio predatory bacteria

Emma J. Banks, Mauricio Valdivia-Delgado, Jacob Biboy, Amber Wilson, Ian T. Cadby, Waldemar Vollmer, Carey Lambert, Andrew L. Lovering, R. Elizabeth Sockett

Biosciences

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Abstract

Peptidoglycan hydrolases contribute to the generation of helical cell shape in Campylobacter and Helicobacter bacteria, while cytoskeletal or periskeletal proteins determine the curved, vibrioid cell shape of Caulobacter and Vibrio. Here, we identify a peptidoglycan hydrolase in the vibrioid-shaped predatory bacterium Bdellovibrio bacteriovorus which invades and replicates within the periplasm of Gram-negative prey bacteria. The protein, Bd1075, generates cell curvature in B. bacteriovorus by exerting LD-carboxypeptidase activity upon the predator cell wall as it grows inside spherical prey. Bd1075 localizes to the outer convex face of B. bacteriovorus; this asymmetric localization requires a nuclear transport factor 2-like (NTF2) domain at the protein C-terminus. We solve the crystal structure of Bd1075, which is monomeric with key differences to other LD-carboxypeptidases. Rod-shaped Δbd1075 mutants invade prey more slowly than curved wild-type predators and stretch invaded prey from within. We therefore propose that the vibrioid shape of B. bacteriovorus contributes to predatory fitness.

Original language	English
Article number	1509
Number of pages	15
Journal	Nature Communications
Volume	13
Issue number	1
Early online date	21 Mar 2022
DOIs	https://doi.org/10.1038/s41467-022-29007-y
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
This work was funded by a Wellcome Trust PhD studentship (215025/Z/18/Z) to E.J.B., a Becas Chile studentship (72180329) to M.V-D., a BBSRC studentship to A.W., and the UKRI Strategic Priorities Fund (https://www.ukri.org) EP/T002778/1 to W.V. R.E.S., C.L., and A.L.L. are currently funded by a Wellcome Trust Investigator Award in Science (209437/Z/17/Z). We thank Chloe Hudson for trials of Bd1075 purification, Daniela Vollmer for purification of PG, Joe Gray for mass spectrometry analysis of muropeptides, Rob Till for general laboratory support, and Block Allocation Group mx19880 for access to Diamond Synchrotron. Genome sequencing was provided by MicrobesNG (http://www.microbesng.uk), which is supported by the BBSRC (grant number BB/L024209/1). Electron microscopy was carried out at the Nanoscale and Microscale Research Centre at the University of Nottingham.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Bdellovibrio bacteriovorus/genetics
Bdellovibrio/genetics
Cell Wall/metabolism
Peptidoglycan/metabolism
Periplasm/metabolism

ASJC Scopus subject areas

General Physics and Astronomy
General Chemistry
General Biochemistry,Genetics and Molecular Biology

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10.1038/s41467-022-29007-y

BanksE2022AsymmetricFinal published version, 3.55 MBLicence: Creative Commons: Attribution (CC BY)

Cite this

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title = "Asymmetric peptidoglycan editing generates cell curvature in Bdellovibrio predatory bacteria",

abstract = "Peptidoglycan hydrolases contribute to the generation of helical cell shape in Campylobacter and Helicobacter bacteria, while cytoskeletal or periskeletal proteins determine the curved, vibrioid cell shape of Caulobacter and Vibrio. Here, we identify a peptidoglycan hydrolase in the vibrioid-shaped predatory bacterium Bdellovibrio bacteriovorus which invades and replicates within the periplasm of Gram-negative prey bacteria. The protein, Bd1075, generates cell curvature in B. bacteriovorus by exerting LD-carboxypeptidase activity upon the predator cell wall as it grows inside spherical prey. Bd1075 localizes to the outer convex face of B. bacteriovorus; this asymmetric localization requires a nuclear transport factor 2-like (NTF2) domain at the protein C-terminus. We solve the crystal structure of Bd1075, which is monomeric with key differences to other LD-carboxypeptidases. Rod-shaped Δbd1075 mutants invade prey more slowly than curved wild-type predators and stretch invaded prey from within. We therefore propose that the vibrioid shape of B. bacteriovorus contributes to predatory fitness.",

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note = "Funding Information: This work was funded by a Wellcome Trust PhD studentship (215025/Z/18/Z) to E.J.B., a Becas Chile studentship (72180329) to M.V-D., a BBSRC studentship to A.W., and the UKRI Strategic Priorities Fund (https://www.ukri.org) EP/T002778/1 to W.V. R.E.S., C.L., and A.L.L. are currently funded by a Wellcome Trust Investigator Award in Science (209437/Z/17/Z). We thank Chloe Hudson for trials of Bd1075 purification, Daniela Vollmer for purification of PG, Joe Gray for mass spectrometry analysis of muropeptides, Rob Till for general laboratory support, and Block Allocation Group mx19880 for access to Diamond Synchrotron. Genome sequencing was provided by MicrobesNG (http://www.microbesng.uk), which is supported by the BBSRC (grant number BB/L024209/1). Electron microscopy was carried out at the Nanoscale and Microscale Research Centre at the University of Nottingham. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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AU - Vollmer, Waldemar

AU - Lambert, Carey

AU - Lovering, Andrew L.

AU - Sockett, R. Elizabeth

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Asymmetric peptidoglycan editing generates cell curvature in Bdellovibrio predatory bacteria

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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