Chromosome Segregation and Peptidoglycan Remodeling Are Coordinated at a Highly Stabilized Septal Pore to Maintain Bacterial Spore Development.
Bacillus subtilis
/ genetics
Bacterial Proteins
/ genetics
Cell Wall
/ enzymology
Chromosome Segregation
Chromosomes
/ genetics
Microscopy, Electron, Transmission
Penicillin-Binding Proteins
/ genetics
Peptidoglycan
/ biosynthesis
Periplasmic Proteins
/ genetics
Protein Binding
Spores, Bacterial
/ genetics
SpoIIIE
cell wall
chromosome segregation
chromosome translocation
development
endospores
peptidoglycan
spores
sporulation
Journal
Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028
Informations de publication
Date de publication:
11 01 2021
11 01 2021
Historique:
received:
30
09
2020
revised:
21
11
2020
accepted:
07
12
2020
pubmed:
1
1
2021
medline:
17
4
2021
entrez:
31
12
2020
Statut:
ppublish
Résumé
Asymmetric division, a hallmark of endospore development, generates two cells, a larger mother cell and a smaller forespore. Approximately 75% of the forespore chromosome must be translocated across the division septum into the forespore by the DNA translocase SpoIIIE. Asymmetric division also triggers cell-specific transcription, which initiates septal peptidoglycan remodeling involving synthetic and hydrolytic enzymes. How these processes are coordinated has remained a mystery. Using Bacillus subtilis, we identified factors that revealed the link between chromosome translocation and peptidoglycan remodeling. In cells lacking these factors, the asymmetric septum retracts, resulting in forespore cytoplasmic leakage and loss of DNA translocation. Importantly, these phenotypes depend on septal peptidoglycan hydrolysis. Our data support a model in which SpoIIIE is anchored at the edge of a septal pore, stabilized by newly synthesized peptidoglycan and protein-protein interactions across the septum. Together, these factors ensure coordination between chromosome translocation and septal peptidoglycan remodeling to maintain spore development.
Identifiants
pubmed: 33383000
pii: S1534-5807(20)30981-3
doi: 10.1016/j.devcel.2020.12.006
pmc: PMC8048138
mid: NIHMS1686958
pii:
doi:
Substances chimiques
Bacterial Proteins
0
PbpG protein, Bacillus subtilis
0
Penicillin-Binding Proteins
0
Peptidoglycan
0
Periplasmic Proteins
0
spore-specific proteins, Bacillus
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
36-51.e5Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM086466
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM127399
Pays : United States
Informations de copyright
Copyright © 2020 Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of Interests The authors declare no competing interests.
Références
J Bacteriol. 2001 Oct;183(20):6046-53
pubmed: 11567005
Genes Dev. 2010 Feb 15;24(4):411-22
pubmed: 20159959
Mol Microbiol. 2013 May;88(4):673-86
pubmed: 23531131
J Bacteriol. 2014 Jul;196(13):2481-90
pubmed: 24769697
Mol Microbiol. 1998 Feb;27(4):777-86
pubmed: 9515703
Mol Microbiol. 2013 Sep;89(6):1039-52
pubmed: 23834622
Elife. 2015 May 07;4:e06474
pubmed: 25950186
Cells. 2020 Jan 22;9(2):
pubmed: 31979090
Cell. 2007 Dec 28;131(7):1301-12
pubmed: 18160039
Genes Dev. 2010 Jun 1;24(11):1160-72
pubmed: 20516200
Mol Microbiol. 2007 Apr;64(1):139-52
pubmed: 17376078
Elife. 2019 Jul 08;8:
pubmed: 31282858
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):11585-11590
pubmed: 27681621
Mol Microbiol. 2008 May;68(4):838-47
pubmed: 18430080
J Mol Biol. 2003 Apr 11;327(5):945-72
pubmed: 12662922
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14553-8
pubmed: 10588743
EMBO J. 1997 Apr 15;16(8):2161-9
pubmed: 9155041
Mol Microbiol. 2006 Feb;59(4):1097-113
pubmed: 16430687
Genes Dev. 2004 Dec 1;18(23):2916-28
pubmed: 15574594
Nucleic Acids Res. 2018 Mar 16;46(5):2699
pubmed: 29425356
Curr Opin Microbiol. 2004 Dec;7(6):579-86
pubmed: 15556029
Mol Microbiol. 2010 Dec;78(5):1055-7
pubmed: 21155139
Nat Struct Mol Biol. 2008 May;15(5):485-93
pubmed: 18391964
Proc Natl Acad Sci U S A. 1998 May 12;95(10):5752-6
pubmed: 9576956
Proc Natl Acad Sci U S A. 2011 Mar 1;108(9):3773-8
pubmed: 21321206
EMBO Rep. 2013 May;14(5):473-9
pubmed: 23559069
Microbiol Mol Biol Rev. 2006 Jun;70(2):317-43
pubmed: 16760306
PLoS Biol. 2016 Jan 06;14(1):e1002341
pubmed: 26735940
Biochem Soc Trans. 2010 Apr;38(2):395-8
pubmed: 20298190
Mol Microbiol. 2010 Dec;78(5):1058-76
pubmed: 21091496
Annu Rev Genet. 1996;30:297-41
pubmed: 8982457
Cell. 2009 May 15;137(4):697-707
pubmed: 19450517
Mol Microbiol. 2019 Sep;112(3):766-784
pubmed: 31152469
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Bacteriol. 2000 Feb;182(4):1096-108
pubmed: 10648537
Cell. 2006 Sep 8;126(5):917-28
pubmed: 16959571
Nat Microbiol. 2016 Jun 20;1(7):16077
pubmed: 27572972
J Bacteriol. 2004 Apr;186(7):1983-90
pubmed: 15028681
Annu Rev Microbiol. 2020 Sep 8;74:361-386
pubmed: 32660383
Elife. 2016 Nov 17;5:
pubmed: 27852437
PLoS Biol. 2013;11(5):e1001557
pubmed: 23667326
Cell. 2018 Feb 8;172(4):758-770.e14
pubmed: 29425492
Genes Dev. 2013 Feb 1;27(3):322-34
pubmed: 23388828
Cell Syst. 2017 Mar 22;4(3):291-305.e7
pubmed: 28189581
J Bacteriol. 2008 Nov;190(21):6983-95
pubmed: 18723616
Curr Biol. 2003 Dec 16;13(24):2196-200
pubmed: 14680637
J Biol Chem. 2013 Oct 4;288(40):28962-74
pubmed: 23974211
Genes Dev. 2008 Jul 1;22(13):1786-95
pubmed: 18593879
Proc Natl Acad Sci U S A. 2014 Sep 2;111(35):12877-82
pubmed: 25071173
Science. 2002 Jan 4;295(5552):137-9
pubmed: 11778051
PLoS Genet. 2009 Jul;5(7):e1000566
pubmed: 19609349
PLoS Comput Biol. 2014 Oct 30;10(10):e1003912
pubmed: 25356555
Mol Microbiol. 2007 Dec;66(5):1051-5
pubmed: 17973909
Cold Spring Harb Perspect Biol. 2010 Jul;2(7):a000406
pubmed: 20573715
Nucleic Acids Res. 2014 Feb;42(4):2624-36
pubmed: 24297254