DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter

Erin D Goley, Luis R. Comolli, Katherine E. Fero, Kenneth H. Downing, Lucy Shapiro

Research output: Contribution to journalArticle

Abstract

Cell division in Gram-negative organisms requires coordinated invagination of the multilayered cell envelope such that each daughter receives an intact inner membrane, peptidoglycan (PG) layer and outer membrane (OM). Here, we identify DipM, a putative LytM endopeptidase in Caulobacter crescentus, and show that it plays a critical role in maintaining cell envelope architecture during growth and division. DipM localized to the division site in an FtsZ-dependent manner via its PG-binding LysM domains. Although not essential for viability, ΔdipM cells exhibited gross morphological defects, including cell widening and filamentation, indicating a role in cell shape maintenance and division that we show requires its LytM domain. Strikingly, cells lacking DipM also showed OM blebbing at the division site, at cell poles and along the cell body. Cryo electron tomography of sacculi isolated from cells depleted of DipM revealed marked thickening of the PG as compared to wild type, which we hypothesize leads to loss of trans-envelope contacts between components of the Tol-Pal complex. We conclude that DipM is required for normal envelope invagination during division and to maintain a sacculus of constant thickness that allows for maintenance of OM connections throughout the cell envelope.

Original languageEnglish (US)
Pages (from-to)56-73
Number of pages18
JournalMolecular Microbiology
Volume77
Issue number1
DOIs
StatePublished - 2010
Externally publishedYes

Fingerprint

Caulobacter
Peptidoglycan
Membranes
Cell Division
Caulobacter crescentus
Maintenance
Electron Microscope Tomography
Endopeptidases
Cell Shape
Blister
Cell Survival

ASJC Scopus subject areas

  • Molecular Biology
  • Microbiology
  • Medicine(all)

Cite this

DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter. / Goley, Erin D; Comolli, Luis R.; Fero, Katherine E.; Downing, Kenneth H.; Shapiro, Lucy.

In: Molecular Microbiology, Vol. 77, No. 1, 2010, p. 56-73.

Research output: Contribution to journalArticle

Goley, Erin D ; Comolli, Luis R. ; Fero, Katherine E. ; Downing, Kenneth H. ; Shapiro, Lucy. / DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter. In: Molecular Microbiology. 2010 ; Vol. 77, No. 1. pp. 56-73.
@article{4b4a11229ab94b94be5a87a0ce148552,
title = "DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter",
abstract = "Cell division in Gram-negative organisms requires coordinated invagination of the multilayered cell envelope such that each daughter receives an intact inner membrane, peptidoglycan (PG) layer and outer membrane (OM). Here, we identify DipM, a putative LytM endopeptidase in Caulobacter crescentus, and show that it plays a critical role in maintaining cell envelope architecture during growth and division. DipM localized to the division site in an FtsZ-dependent manner via its PG-binding LysM domains. Although not essential for viability, ΔdipM cells exhibited gross morphological defects, including cell widening and filamentation, indicating a role in cell shape maintenance and division that we show requires its LytM domain. Strikingly, cells lacking DipM also showed OM blebbing at the division site, at cell poles and along the cell body. Cryo electron tomography of sacculi isolated from cells depleted of DipM revealed marked thickening of the PG as compared to wild type, which we hypothesize leads to loss of trans-envelope contacts between components of the Tol-Pal complex. We conclude that DipM is required for normal envelope invagination during division and to maintain a sacculus of constant thickness that allows for maintenance of OM connections throughout the cell envelope.",
author = "Goley, {Erin D} and Comolli, {Luis R.} and Fero, {Katherine E.} and Downing, {Kenneth H.} and Lucy Shapiro",
year = "2010",
doi = "10.1111/j.1365-2958.2010.07222.x",
language = "English (US)",
volume = "77",
pages = "56--73",
journal = "Molecular Microbiology",
issn = "0950-382X",
publisher = "Wiley-Blackwell",
number = "1",

}

TY - JOUR

T1 - DipM links peptidoglycan remodelling to outer membrane organization in Caulobacter

AU - Goley, Erin D

AU - Comolli, Luis R.

AU - Fero, Katherine E.

AU - Downing, Kenneth H.

AU - Shapiro, Lucy

PY - 2010

Y1 - 2010

N2 - Cell division in Gram-negative organisms requires coordinated invagination of the multilayered cell envelope such that each daughter receives an intact inner membrane, peptidoglycan (PG) layer and outer membrane (OM). Here, we identify DipM, a putative LytM endopeptidase in Caulobacter crescentus, and show that it plays a critical role in maintaining cell envelope architecture during growth and division. DipM localized to the division site in an FtsZ-dependent manner via its PG-binding LysM domains. Although not essential for viability, ΔdipM cells exhibited gross morphological defects, including cell widening and filamentation, indicating a role in cell shape maintenance and division that we show requires its LytM domain. Strikingly, cells lacking DipM also showed OM blebbing at the division site, at cell poles and along the cell body. Cryo electron tomography of sacculi isolated from cells depleted of DipM revealed marked thickening of the PG as compared to wild type, which we hypothesize leads to loss of trans-envelope contacts between components of the Tol-Pal complex. We conclude that DipM is required for normal envelope invagination during division and to maintain a sacculus of constant thickness that allows for maintenance of OM connections throughout the cell envelope.

AB - Cell division in Gram-negative organisms requires coordinated invagination of the multilayered cell envelope such that each daughter receives an intact inner membrane, peptidoglycan (PG) layer and outer membrane (OM). Here, we identify DipM, a putative LytM endopeptidase in Caulobacter crescentus, and show that it plays a critical role in maintaining cell envelope architecture during growth and division. DipM localized to the division site in an FtsZ-dependent manner via its PG-binding LysM domains. Although not essential for viability, ΔdipM cells exhibited gross morphological defects, including cell widening and filamentation, indicating a role in cell shape maintenance and division that we show requires its LytM domain. Strikingly, cells lacking DipM also showed OM blebbing at the division site, at cell poles and along the cell body. Cryo electron tomography of sacculi isolated from cells depleted of DipM revealed marked thickening of the PG as compared to wild type, which we hypothesize leads to loss of trans-envelope contacts between components of the Tol-Pal complex. We conclude that DipM is required for normal envelope invagination during division and to maintain a sacculus of constant thickness that allows for maintenance of OM connections throughout the cell envelope.

UR - http://www.scopus.com/inward/record.url?scp=77953995341&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77953995341&partnerID=8YFLogxK

U2 - 10.1111/j.1365-2958.2010.07222.x

DO - 10.1111/j.1365-2958.2010.07222.x

M3 - Article

C2 - 20497504

AN - SCOPUS:77953995341

VL - 77

SP - 56

EP - 73

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 1

ER -