TY - JOUR
T1 - Intermembrane crosstalk drives inner-membrane protein organization in Escherichia coli
AU - Rassam, Patrice
AU - Long, Kathleen R.
AU - Kaminska, Renata
AU - Williams, David J.
AU - Papadakos, Grigorios
AU - Baumann, Christoph G.
AU - Kleanthous, Colin
N1 - This work was funded by the Biotechnology and Biological Sciences Research Council UK (BB/G020671/2) to C.K. and C.G.B. and by a European Research Council Advanced grant (742555 - OMPorg) to C.K.
PY - 2018/3/14
Y1 - 2018/3/14
N2 - Gram-negative bacteria depend on energised protein complexes that connect the two membranes of the cell envelope. However, β-barrel outer-membrane proteins (OMPs) and α-helical inner-membrane proteins (IMPs) display quite different organisation. OMPs cluster into islands that restrict their lateral mobility, while IMPs generally diffuse throughout the cell. Here, using live cell imaging of Escherichia coli, we demonstrate that when transient, energy-dependent transmembrane connections are formed, IMPs become subjugated by the inherent organisation of OMPs and that such connections impact IMP function. We show that while establishing a translocon for import, the colicin ColE9 sequesters the IMPs of the proton motive force (PMF)-linked Tol-Pal complex into islands mirroring those of colicin-bound OMPs. Through this imposed organisation, the bacteriocin subverts the outer-membrane stabilising role of Tol-Pal, blocking its recruitment to cell division sites and slowing membrane constriction. The ordering of IMPs by OMPs via an energised inter-membrane bridge represents an emerging functional paradigm in cell envelope biology.
AB - Gram-negative bacteria depend on energised protein complexes that connect the two membranes of the cell envelope. However, β-barrel outer-membrane proteins (OMPs) and α-helical inner-membrane proteins (IMPs) display quite different organisation. OMPs cluster into islands that restrict their lateral mobility, while IMPs generally diffuse throughout the cell. Here, using live cell imaging of Escherichia coli, we demonstrate that when transient, energy-dependent transmembrane connections are formed, IMPs become subjugated by the inherent organisation of OMPs and that such connections impact IMP function. We show that while establishing a translocon for import, the colicin ColE9 sequesters the IMPs of the proton motive force (PMF)-linked Tol-Pal complex into islands mirroring those of colicin-bound OMPs. Through this imposed organisation, the bacteriocin subverts the outer-membrane stabilising role of Tol-Pal, blocking its recruitment to cell division sites and slowing membrane constriction. The ordering of IMPs by OMPs via an energised inter-membrane bridge represents an emerging functional paradigm in cell envelope biology.
KW - Journal article
KW - Biological fluorescence
KW - Cellular microbiology
KW - Membrane structure and assembly
UR - http://www.scopus.com/inward/record.url?scp=85044237782&partnerID=8YFLogxK
U2 - 10.1038/s41467-018-03521-4
DO - 10.1038/s41467-018-03521-4
M3 - Article
C2 - 29540681
SN - 2041-1723
VL - 9
SP - 1
EP - 8
JO - Nature Communications
JF - Nature Communications
M1 - 1082
ER -