Cargando…

The molecular architecture of engulfment during Bacillus subtilis sporulation

The study of bacterial cell biology is limited by difficulties in visualizing cellular structures at high spatial resolution within their native milieu. Here, we visualize Bacillus subtilis sporulation using cryo-electron tomography coupled with cryo-focused ion beam milling, allowing the reconstruc...

Descripción completa

Detalles Bibliográficos
Autores principales: Khanna, Kanika, Lopez-Garrido, Javier, Zhao, Ziyi, Watanabe, Reika, Yuan, Yuan, Sugie, Joseph, Pogliano, Kit, Villa, Elizabeth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6684271/
https://www.ncbi.nlm.nih.gov/pubmed/31282858
http://dx.doi.org/10.7554/eLife.45257
_version_ 1783442233349898240
author Khanna, Kanika
Lopez-Garrido, Javier
Zhao, Ziyi
Watanabe, Reika
Yuan, Yuan
Sugie, Joseph
Pogliano, Kit
Villa, Elizabeth
author_facet Khanna, Kanika
Lopez-Garrido, Javier
Zhao, Ziyi
Watanabe, Reika
Yuan, Yuan
Sugie, Joseph
Pogliano, Kit
Villa, Elizabeth
author_sort Khanna, Kanika
collection PubMed
description The study of bacterial cell biology is limited by difficulties in visualizing cellular structures at high spatial resolution within their native milieu. Here, we visualize Bacillus subtilis sporulation using cryo-electron tomography coupled with cryo-focused ion beam milling, allowing the reconstruction of native-state cellular sections at molecular resolution. During sporulation, an asymmetrically-positioned septum generates a larger mother cell and a smaller forespore. Subsequently, the mother cell engulfs the forespore. We show that the septal peptidoglycan is not completely degraded at the onset of engulfment. Instead, the septum is uniformly and only slightly thinned as it curves towards the mother cell. Then, the mother cell membrane migrates around the forespore in tiny finger-like projections, whose formation requires the mother cell SpoIIDMP protein complex. We propose that a limited number of SpoIIDMP complexes tether to and degrade the peptidoglycan ahead of the engulfing membrane, generating an irregular membrane front.
format Online
Article
Text
id pubmed-6684271
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-66842712019-08-09 The molecular architecture of engulfment during Bacillus subtilis sporulation Khanna, Kanika Lopez-Garrido, Javier Zhao, Ziyi Watanabe, Reika Yuan, Yuan Sugie, Joseph Pogliano, Kit Villa, Elizabeth eLife Microbiology and Infectious Disease The study of bacterial cell biology is limited by difficulties in visualizing cellular structures at high spatial resolution within their native milieu. Here, we visualize Bacillus subtilis sporulation using cryo-electron tomography coupled with cryo-focused ion beam milling, allowing the reconstruction of native-state cellular sections at molecular resolution. During sporulation, an asymmetrically-positioned septum generates a larger mother cell and a smaller forespore. Subsequently, the mother cell engulfs the forespore. We show that the septal peptidoglycan is not completely degraded at the onset of engulfment. Instead, the septum is uniformly and only slightly thinned as it curves towards the mother cell. Then, the mother cell membrane migrates around the forespore in tiny finger-like projections, whose formation requires the mother cell SpoIIDMP protein complex. We propose that a limited number of SpoIIDMP complexes tether to and degrade the peptidoglycan ahead of the engulfing membrane, generating an irregular membrane front. eLife Sciences Publications, Ltd 2019-07-08 /pmc/articles/PMC6684271/ /pubmed/31282858 http://dx.doi.org/10.7554/eLife.45257 Text en © 2019, Khanna et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
Khanna, Kanika
Lopez-Garrido, Javier
Zhao, Ziyi
Watanabe, Reika
Yuan, Yuan
Sugie, Joseph
Pogliano, Kit
Villa, Elizabeth
The molecular architecture of engulfment during Bacillus subtilis sporulation
title The molecular architecture of engulfment during Bacillus subtilis sporulation
title_full The molecular architecture of engulfment during Bacillus subtilis sporulation
title_fullStr The molecular architecture of engulfment during Bacillus subtilis sporulation
title_full_unstemmed The molecular architecture of engulfment during Bacillus subtilis sporulation
title_short The molecular architecture of engulfment during Bacillus subtilis sporulation
title_sort molecular architecture of engulfment during bacillus subtilis sporulation
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6684271/
https://www.ncbi.nlm.nih.gov/pubmed/31282858
http://dx.doi.org/10.7554/eLife.45257
work_keys_str_mv AT khannakanika themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT lopezgarridojavier themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT zhaoziyi themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT watanabereika themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT yuanyuan themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT sugiejoseph themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT poglianokit themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT villaelizabeth themoleculararchitectureofengulfmentduringbacillussubtilissporulation
AT khannakanika moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT lopezgarridojavier moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT zhaoziyi moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT watanabereika moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT yuanyuan moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT sugiejoseph moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT poglianokit moleculararchitectureofengulfmentduringbacillussubtilissporulation
AT villaelizabeth moleculararchitectureofengulfmentduringbacillussubtilissporulation