Bacillus subtilis spoIIIE protein required for DNA segregation during asymmetric cell division

ABSTRACT The switch from symmetric to asymmetric cell division is a key feature of development in many organisms, including Bacillus subtilis sporulation. Here we demonstrate that, prior to the onset of asymmetric cell division, the B. subtilis chromosome is partitioned into two unequally sized domains, with the origin-proximal one-third of the future forespore chromosome condensed near one pole of the cell. Asymmetric chromosome partitioning is independent of polar division, as it occurs in cells depleted of FtsZ but depends on two transcription factors that govern the initiation of sporulation, σH and Spo0A-P. It is also independent of chromosome partitioning proteins Spo0J and Soj, suggesting the existence of a novel mechanism controlling chromosome structure. Thus, our results demonstrate that, during sporulation, two separable events prepare B. subtilis for asymmetric cell division: the relocation of cell division sites to the cell poles and the asymmetric partitioning of the future forespore chromosome.

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Linking the Peptidoglycan Synthesis Protein Complex with Asymmetric Cell Division during Bacillus subtilis Sporulation

International Journal of Molecular Sciences ◽

10.3390/ijms21124513 ◽

2020 ◽

Vol 21 (12) ◽

pp. 4513 ◽

Cited By ~ 1

Author(s):

Katarína Muchová ◽

Zuzana Chromiková ◽

Imrich Barák

Keyword(s):

Bacillus Subtilis ◽

Cell Division ◽

Protein Complex ◽

Asymmetric Cell Division ◽

Morphological Changes ◽

Direct Interaction ◽

Specific Protein ◽

Peptidoglycan Biosynthesis ◽

Peptidoglycan Synthesis ◽

Septum Formation

Peptidoglycan is generally considered one of the main determinants of cell shape in bacteria. In rod-shaped bacteria, cell elongation requires peptidoglycan synthesis to lengthen the cell wall. In addition, peptidoglycan is synthesized at the division septum during cell division. Sporulation of Bacillus subtilis begins with an asymmetric cell division. Formation of the sporulation septum requires almost the same set of proteins as the vegetative septum; however, these two septa are significantly different. In addition to their differences in localization, the sporulation septum is thinner and it contains SpoIIE, a crucial sporulation specific protein. Here we show that peptidoglycan biosynthesis is linked to the cell division machinery during sporulation septum formation. We detected a direct interaction between SpoIIE and GpsB and found that both proteins co-localize during the early stages of asymmetric septum formation. We propose that SpoIIE is part of a multi-protein complex which includes GpsB, other division proteins and peptidoglycan synthesis proteins, and could provide a link between the peptidoglycan synthesis machinery and the complex morphological changes required for forespore formation during B. subtilis sporulation.

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Postdivisional Synthesis of the Sporosarcina ureae DNA Translocase SpoIIIE either in the Mother Cell or in the Prespore Enables Bacillus subtilis To Translocate DNA from the Mother Cell to the Prespore

Journal of Bacteriology ◽

10.1128/jb.185.3.879-886.2003 ◽

2003 ◽

Vol 185 (3) ◽

pp. 879-886 ◽

Cited By ~ 11

Author(s):

Vasant K. Chary ◽

Patrick J. Piggot

Keyword(s):

Bacillus Subtilis ◽

Cell Division ◽

Mother Cell ◽

Asymmetric Cell Division ◽

Dna Translocation ◽

Sporosarcina Ureae ◽

Correct Orientation ◽

Chromosome Partitioning ◽

Specific Synthesis ◽

Dna Translocase

ABSTRACT The differentiation of vegetative cells of Bacillus subtilis into spores involves asymmetric cell division, which precedes complete chromosome partitioning. The DNA translocase SpoIIIE is required to translocate the origin distal 70% of the chromosome from the larger mother cell into the smaller prespore, the two cells that result from the division. We have tested the effect of altering the time and location of SpoIIIE synthesis on spore formation. We have expressed the spoIIIE homologue from Sporosarcina ureae in B. subtilis under the control of different promoters. Expression from either a weak mother cell-specific (σE) promoter or a weak prespore-specific (σF) promoter partly complemented the sporulation defect of a spoIIIE36 mutant; however, expression from a strong prespore-specific (σF) promoter did not. DNA translocation from the mother cell to the prespore was assayed using spoIIQ-lacZ inserted at thrC; transcription of spoIIQ occurs only in the prespore. Translocation of thrC::spoIIQ-lacZ into the prespore occurred efficiently when spoIIIE Su was expressed from the weak σE- or σF-controlled promoters but not when it was expressed from the strong σF-controlled promoter. It is speculated that the mechanism directing SpoIIIE insertion into the septum in the correct orientation may accommodate slow postseptational, prespore-specific SpoIIIE synthesis but may be swamped by strong prespore-specific synthesis.

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Bifunctional protein required for asymmetric cell division and cell-specific transcription in Bacillus subtilis.

Genes & Development ◽

10.1101/gad.10.7.794 ◽

1996 ◽

Vol 10 (7) ◽

pp. 794-803 ◽

Cited By ~ 81

Author(s):

A Feucht ◽

T Magnin ◽

M D Yudkin ◽

J Errington

Keyword(s):

Bacillus Subtilis ◽

Cell Division ◽

Asymmetric Cell Division ◽

Bifunctional Protein

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PAR-4 and anillin regulate myosin to coordinate spindle and furrow position during asymmetric division

The Journal of Cell Biology ◽

10.1083/jcb.201503006 ◽

2015 ◽

Vol 210 (7) ◽

pp. 1085-1099 ◽

Cited By ~ 28

Author(s):

Anne Pacquelet ◽

Perrine Uhart ◽

Jean-Pierre Tassan ◽

Grégoire Michaux

Keyword(s):

Cell Division ◽

Caenorhabditis Elegans ◽

Mitotic Spindle ◽

Asymmetric Cell Division ◽

Asymmetric Division ◽

Anterior Cortex ◽

Dna Segregation ◽

Spindle Midzone ◽

Dependent Pathway

During asymmetric cell division, the mitotic spindle and polarized myosin can both determine the position of the cytokinetic furrow. However, how cells coordinate signals from the spindle and myosin to ensure that cleavage occurs through the spindle midzone is unknown. Here, we identify a novel pathway that is essential to inhibit myosin and coordinate furrow and spindle positions during asymmetric division. In Caenorhabditis elegans one-cell embryos, myosin localizes at the anterior cortex whereas the mitotic spindle localizes toward the posterior. We find that PAR-4/LKB1 impinges on myosin via two pathways, an anillin-dependent pathway that also responds to the cullin CUL-5 and an anillin-independent pathway involving the kinase PIG-1/MELK. In the absence of both PIG-1/MELK and the anillin ANI-1, myosin accumulates at the anterior cortex and induces a strong displacement of the furrow toward the anterior, which can lead to DNA segregation defects. Regulation of asymmetrically localized myosin is thus critical to ensure that furrow and spindle midzone positions coincide throughout cytokinesis.

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Centromere assembly and non-random sister chromatid segregation in stem cells

Essays in Biochemistry ◽

10.1042/ebc20190066 ◽

2020 ◽

Vol 64 (2) ◽

pp. 223-232 ◽

Cited By ~ 1

Author(s):

Ben L. Carty ◽

Elaine M. Dunleavy

Keyword(s):

Stem Cells ◽

Cell Division ◽

Cell Fate ◽

Sister Chromatid ◽

Asymmetric Cell Division ◽

Protein A ◽

Germline Stem Cells ◽

Sister Chromatids ◽

Centromere Protein A ◽

Oocyte Meiosis

Abstract Asymmetric cell division (ACD) produces daughter cells with separate distinct cell fates and is critical for the development and regulation of multicellular organisms. Epigenetic mechanisms are key players in cell fate determination. Centromeres, epigenetically specified loci defined by the presence of the histone H3-variant, centromere protein A (CENP-A), are essential for chromosome segregation at cell division. ACDs in stem cells and in oocyte meiosis have been proposed to be reliant on centromere integrity for the regulation of the non-random segregation of chromosomes. It has recently been shown that CENP-A is asymmetrically distributed between the centromeres of sister chromatids in male and female Drosophila germline stem cells (GSCs), with more CENP-A on sister chromatids to be segregated to the GSC. This imbalance in centromere strength correlates with the temporal and asymmetric assembly of the mitotic spindle and potentially orientates the cell to allow for biased sister chromatid retention in stem cells. In this essay, we discuss the recent evidence for asymmetric sister centromeres in stem cells. Thereafter, we discuss mechanistic avenues to establish this sister centromere asymmetry and how it ultimately might influence cell fate.

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