Generating specialized cell types by asymmetric division in Bacillus subtilis

Biofilm formation by the Gram-positive bacterium Bacillus subtilis is tightly controlled at the level of transcription. The biofilm contains specialized cell types that arise from controlled differentiation of the resident isogenic bacteria. DegU is a response regulator that controls several social behaviours exhibited by B. subtilis including swarming motility, biofilm formation and extracellular protease (exoprotease) production. Here, for the first time, we examine the prevalence and origin of exoprotease-producing cells within the biofilm. This was accomplished using single-cell analysis techniques including flow cytometry and fluorescence microscopy. We established that the number of exoprotease-producing cells increases as the biofilm matures. This is reflected by both an increase at the level of transcription and an increase in exoprotease activity over time. We go on to demonstrate that exoprotease-producing cells arise from more than one cell type, namely matrix-producing and non-matrix-producing cells. In toto these findings allow us to add exoprotease-producing cells to the list of specialized cell types that are derived during B. subtilis biofilm formation and furthermore the data highlight the plasticity in the origin of differentiated cells.

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Metal-dependent SpoIIE oligomerization stabilizes FtsZ during asymmetric division in Bacillus subtilis

PLoS ONE ◽

10.1371/journal.pone.0174713 ◽

2017 ◽

Vol 12 (3) ◽

pp. e0174713 ◽

Cited By ~ 4

Author(s):

Ewa Król ◽

Anabela de Sousa Borges ◽

Malgorzata Kopacz ◽

Dirk-Jan Scheffers

Keyword(s):

Bacillus Subtilis ◽

Asymmetric Division

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Phage-encoded sigma factors alter bacterial dormancy

10.1101/2021.11.12.468384 ◽

2021 ◽

Author(s):

Daniel A Schwartz ◽

Brent K Lehmkuhl ◽

Jay T Lennon

Keyword(s):

Bacillus Subtilis ◽

Metabolic Activity ◽

Gene Network ◽

Transcriptional Regulators ◽

Cell Types ◽

Sigma Factors ◽

Lytic Infection ◽

Parasitic Infections ◽

Spore Yield

By entering a reversible state of reduced metabolic activity, dormant microorganisms are able to tolerate suboptimal conditions that would otherwise reduce their fitness. Dormancy may also benefit bacteria by serving as a refuge from parasitic infections. Here we focus on dormancy in the Firmicutes, where endospore development is transcriptionally regulated by the expression of sigma factors. A disruption of this process could influence the survivorship and reproduction of phages that infect spore-forming hosts with implications for coevolutionary dynamics. Here, we characterized the distribution and diversity of sigma factors in nearly 3,500 phage genomes. Homologs of sporulation-specific sigma factors were identified in phages that infect spore-forming hosts. Unlike sigma factors required for phage reproduction, the sporulation-like sigma factors were non-essential for lytic infection. However, when expressed in the spore-forming Bacillus subtilis, sigma factors from phages activated the bacterial sporulation gene network and reduced spore yield. Our findings suggest that the acquisition of host-like transcriptional regulators may allow phages to manipulate a complex and ancient trait in one of the most abundant cell types on Earth.

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The secretory pathway at 50: a golden anniversary for some momentous grains of silver

Molecular Biology of the Cell ◽

10.1091/mbc.e16-07-0508 ◽

2017 ◽

Vol 28 (2) ◽

pp. 229-232 ◽

Cited By ~ 1

Author(s):

Karl S. Matlin ◽

Michael J. Caplan

Keyword(s):

Membrane Proteins ◽

Cell Biology ◽

Secretory Pathway ◽

Cell Types ◽

Dynamic Nature ◽

Specialized Cell ◽

Central Paradigm ◽

Biosynthetic Machinery

The secretory pathway along which newly synthesized secretory and membrane proteins traffic through the cell was revealed in two articles published 50 years ago. This discovery was the culmination of decades of effort to unite the power of biochemical and morphological methodologies in order to elucidate the dynamic nature of the cell’s biosynthetic machinery. The secretory pathway remains a central paradigm of modern cell biology. Its elucidation 50 years ago inspired tremendous multidisciplinary and on-going efforts to understand the machinery that makes it run, the adaptations that permit it to serve the needs of specialized cell types, and the pathological consequences that arise when it is perturbed.

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Expression of spoIIIJ in the Prespore Is Sufficient for Activation of σG and for Sporulation in Bacillus subtilis

Journal of Bacteriology ◽

10.1128/jb.185.13.3905-3917.2003 ◽

2003 ◽

Vol 185 (13) ◽

pp. 3905-3917 ◽

Cited By ~ 27

Author(s):

Mónica Serrano ◽

Luísa Côrte ◽

Jason Opdyke ◽

Charles P. Moran, ◽

Adriano O. Henriques

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Rna Polymerase ◽

Sigma Factor ◽

Vegetative Growth ◽

Mother Cell ◽

Asymmetric Division ◽

Developmental Program ◽

Inactive Form

ABSTRACT During sporulation in Bacillus subtilis, the prespore-specific developmental program is initiated soon after asymmetric division of the sporangium by the compartment-specific activation of RNA polymerase sigma factor σF. σF directs transcription of spoIIIG, encoding the late forespore-specific regulator σG. Following synthesis, σG is initially kept in an inactive form, presumably because it is bound to the SpoIIAB anti-sigma factor. Activation of σG occurs only after the complete engulfment of the prespore by the mother cell. Mutations in spoIIIJ arrest sporulation soon after conclusion of the engulfment process and prevent activation of σG. Here we show that σG accumulates but is mostly inactive in a spoIIIJ mutant. We also show that expression of the spoIIIGE155K allele, encoding a form of σG that is not efficiently bound by SpoIIAB in vitro, restores σG-directed gene expression to a spoIIIJ mutant. Expression of spoIIIJ occurs during vegetative growth. However, we show that expression of spoIIIJ in the prespore is sufficient for σG activation and for sporulation. Mutations in the mother cell-specific spoIIIA locus are known to arrest sporulation just after completion of the engulfment process. Previous work has also shown that σG accumulates in an inactive form in spoIIIA mutants and that the need for spoIIIA expression for σG activation can be circumvented by the spoIIIGE155K allele. However, in contrast to the case for spoIIIJ, we show that expression of spoIIIA in the prespore does not support efficient sporulation. The results suggest that the activation of σG at the end of the engulfment process involves the action of spoIIIA from the mother cell and of spoIIIJ from the prespore.

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A Zenopus multifinger protein, Xfin, is expressed in specialized cell types and is localized in the cytoplasm

Mechanisms of Development ◽

10.1016/0925-4773(91)90069-i ◽

1991 ◽

Vol 36 (1-2) ◽

pp. 31-40 ◽

Cited By ~ 4

Author(s):

Stefania De Lucchini ◽

Filippo M. Rijli ◽

Gennaro Ciliberto ◽

Giuseppina Barsacchi

Keyword(s):

Cell Types ◽

Specialized Cell

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CELLS, FOSSILS, AND EMBRYOS: USING PHYLOGENETIC COMPARATIVE METHODS TO UNDERSTAND HOW SPECIALIZED CELL TYPES HAVE CHANGED IN DEEP TIME

10.1130/abs/2018am-324530 ◽

2018 ◽

Author(s):

Eric M. Erkenbrack ◽

◽

Jeffrey R. Thompson

Keyword(s):

Cell Types ◽

Comparative Methods ◽

Phylogenetic Comparative Methods ◽

Deep Time ◽

Specialized Cell

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Role of the σD-Dependent Autolysins in Bacillus subtilis Population Heterogeneity

Journal of Bacteriology ◽

10.1128/jb.00521-09 ◽

2008 ◽

Vol 191 (18) ◽

pp. 5775-5784 ◽

Cited By ~ 72

Author(s):

Rui Chen ◽

Sarah B. Guttenplan ◽

Kris M. Blair ◽

Daniel B. Kearns

Keyword(s):

Bacillus Subtilis ◽

Cell Separation ◽

Cell Types ◽

Population Heterogeneity ◽

Gene Encoding ◽

Swarming Motility ◽

Morphological Heterogeneity ◽

Distinct Cell ◽

Flagellum Biosynthesis ◽

Necessary And Sufficient

ABSTRACT Exponentially growing populations of Bacillus subtilis contain two morphologically and functionally distinct cell types: motile individuals and nonmotile multicellular chains. Motility differentiation arises because RNA polymerase and the alternative sigma factor σD activate expression of flagellin in a subpopulation of cells. Here we demonstrate that the peptidoglycan-remodeling autolysins under σD control, LytC, LytD, and LytF, are expressed in the same subpopulation of cells that complete flagellar synthesis. Morphological heterogeneity is explained by the expression of LytF that is necessary and sufficient for cell separation. Moreover, LytC is required for motility but not at the level of cell separation or flagellum biosynthesis. Rather, LytC appears to be important for flagellar function, and motility was restored to a LytC mutant by mutation of either lonA, encoding the LonA protease, or a gene encoding a previously unannotated swarming motility inhibitor, SmiA. We conclude that heterogeneous activation of σD-dependent gene expression is sufficient to explain both the morphological heterogeneity and functional heterogeneity present in vegetative B. subtilis populations.

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Genetic Dissection of the Sporulation Protein SpoIIE and Its Role in Asymmetric Division in Bacillus subtilis

Journal of Bacteriology ◽

10.1128/jb.187.10.3511-3520.2005 ◽

2005 ◽

Vol 187 (10) ◽

pp. 3511-3520 ◽

Cited By ~ 18

Author(s):

Karen Carniol ◽

Sigal Ben-Yehuda ◽

Nicole King ◽

Richard Losick

Keyword(s):

Bacillus Subtilis ◽

Critical Role ◽

Asymmetric Division ◽

Dual Function ◽

Genetic Dissection ◽

Dependent Manner ◽

Phosphatase Domain ◽

Polar Cell ◽

Membrane Spanning ◽

Polar Division

ABSTRACT SpoIIE is a dual-function protein in Bacillus subtilis that contributes to the switch from medial to polar cell division during sporulation and is responsible for activating the cell-specific transcription factor σF. SpoIIE consists of an N-terminal domain with 10 membrane-spanning segments (region I), a C-terminal phosphatase domain (region III), and a central domain (region II) of uncertain function. To investigate the role of SpoIIE in polar division, we took advantage of a system for efficiently producing polar septa during growth in a SpoIIE-dependent manner using cells engineered to produce the sporulation protein in response to an inducer. The results show that regions II and III play a critical role in polar septum formation and that specific amino acid substitutions in those regions affect the abilities of SpoIIE both to promote polar division and to localize to the division machinery. Additionally, we show that neither the phosphatase function of SpoIIE nor the N-terminal, membrane-spanning region is needed for the switch to asymmetric division.

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Specialized cell types in the human fetal small intestine

The Anatomical Record ◽

10.1002/ar.1091910302 ◽

1978 ◽

Vol 191 (3) ◽

pp. 269-285 ◽

Cited By ~ 83

Author(s):

Pamela Colony Moxey ◽

Jerry S. Trier

Keyword(s):

Small Intestine ◽

Cell Types ◽

Specialized Cell

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