Fast Mechanically Driven Daughter Cell Separation Is Widespread in
            <i>Actinobacteria</i>

Zhou, Xiaoxue; Halladin, David K.; Theriot, Julie A.

doi:10.1128/mbio.00952-16

Cited by 26 publications

(25 citation statements)

References 22 publications

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“…In their pioneering study, Zhou et al 6 linked division of S. aureus to a fracture process and postulated that it might result from stress accumulation and mechanical failure of the cell wall, thereby laying the groundwork for viewing bacterial cell division from the perspective of physical forces 32 . Their observations are reminiscent of the "V-snapping" model of cell division in M. smegmatis 33 ; more recently, additional bacterial species have been identified that also undergo abrupt spatial reorientation during cell division 7 (see Figure 4a). This phenomenon (V-snapping) is consistent with a model in which rapid cleavage of sibling cells is due to progressive circumferential rupture of the connecting cell wall starting from the weakest section around the PCF.…”

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confidence: 89%

Overlapping and essential roles for molecular and mechanical mechanisms in mycobacterial cell division

et al. 2019

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Mechanisms to control cell division are essential for cell proliferation and survival 1. Bacterial cell growth and division require the coordinated activity of peptidoglycan synthases and hydrolytic enzymes 2-4 to maintain mechanical integrity of the cell wall 5. Recent studies suggest that cell separation is governed by mechanical forces 6,7. How mechanical forces interact with molecular mechanisms to control bacterial cell division in space and time is poorly understood. Here, we use a combination of atomic force microscope (AFM) imaging, nanomechanical mapping, and nanomanipulation to show that enzymatic activity and mechanical forces serve overlapping and essential roles in mycobacterial cell division. We find that mechanical stress gradually accumulates in the cell wall concentrated at the future division site, culminating in rapid (millisecond) cleavage of nascent sibling cells. Inhibiting cell wall hydrolysis delays cleavage; conversely, locally increasing cell wall stress causes instantaneous and premature cleavage. Cells deficient in peptidoglycan hydrolytic activity fail to locally decrease their cell wall strength and undergo natural cleavage, instead forming chains of non-growing cells. Cleavage of these cells can be mechanically induced by local application of stress with AFM. These findings establish a direct link between actively controlled molecular mechanisms and passively controlled mechanical forces in bacterial cell division. Marked morphological changes occur when a microbial cell divides to form two daughter cells 1. In Escherichia coli this process involves gradual constriction of the cell envelope and structural remodelling of the new cell poles 2-4. In contrast, other microbial species build a septum without gradual constriction of the cell envelope 8,9. Instead, the cell wall connecting Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

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confidence: 89%

Overlapping and essential roles for molecular and mechanical mechanisms in mycobacterial cell division

et al. 2019

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“…2C). Following septation, aerial hyphae divide into immature spores via a mechanism described as 'V snapping', which relies on turgor pressure and structural weakening of the PG to drive cell division in milliseconds (Zhou et al, 2016). In immature spore chains, the rodlet layer remained intact as a 20-nm thick sheath ( Fig.…”

Section: Streptomyces the Cell Envelope Undergoes Dramatic Remodelinmentioning

confidence: 99%

Ultrastructure of exospore formation inStreptomycesrevealed by cryo-electron tomography

Sexton

Tocheva

2020

Preprint

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AbstractMany bacteria form spores in response to adverse environmental conditions. Several sporulation pathways have evolved independently and occur through distinctive mechanisms. Here, using cryo-electron tomography (cryo-ET), we examine all stages of growth and exospore formation in the model organism Streptomyces albus. Our data reveal the native ultrastructure of vegetative hyphae, including the polarisome and filaments of ParA or FilP. In addition, we observed septal junctions in vegetative septa, likely involved in effector translocation between neighbouring cells. During sporulation, the cell envelope undergoes dramatic remodeling, including the formation of a spore cortex and two protective proteinaceous layers. Mature spores reveal the presence of a continuous spore coat and an irregular rodlet sheet. Together, these results provide an unprecedented examination of the ultrastructure in Streptomyces and further our understanding of the structural complexity of exospore formation.

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“…In addition to growing asymmetrically, mycobacteria also divide asymmetrically and undergo a fast, mechanical v-snapping process of daughter cell separation ( Aldridge et al, 2012 ; Richardson et al, 2016 ; Zhou et al, 2016 ). There is evidence to suggest that sites of asymmetric division are not just established at division, but are inherited from previous generations.…”

Section: The Basis Of Asymmetrymentioning

confidence: 99%

Stable Regulation of Cell Cycle Events in Mycobacteria: Insights From Inherently Heterogeneous Bacterial Populations

Logsdon

Aldridge

2018

Front. Microbiol.

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Model bacteria, such as E. coli and B. subtilis, tightly regulate cell cycle progression to achieve consistent cell size distributions and replication dynamics. Many of the hallmark features of these model bacteria, including lateral cell wall elongation and symmetric growth and division, do not occur in mycobacteria. Instead, mycobacterial growth is characterized by asymmetric polar growth and division. This innate asymmetry creates unequal birth sizes and growth rates for daughter cells with each division, generating a phenotypically heterogeneous population. Although the asymmetric growth patterns of mycobacteria lead to a larger variation in birth size than typically seen in model bacterial populations, the cell size distribution is stable over time. Here, we review the cellular mechanisms of growth, division, and cell cycle progression in mycobacteria in the face of asymmetry and inherent heterogeneity. These processes coalesce to control cell size. Although Mycobacterium smegmatis and Mycobacterium bovis Bacillus Calmette-Guérin (BCG) utilize a novel model of cell size control, they are similar to previously studied bacteria in that initiation of DNA replication is a key checkpoint for cell division. We compare the regulation of DNA replication initiation and strategies used for cell size homeostasis in mycobacteria and model bacteria. Finally, we review the importance of cellular organization and chromosome segregation relating to the physiology of mycobacteria and consider how new frameworks could be applied across the wide spectrum of bacterial diversity.

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Fast Mechanically Driven Daughter Cell Separation Is Widespread in Actinobacteria

Cited by 26 publications

References 22 publications

Overlapping and essential roles for molecular and mechanical mechanisms in mycobacterial cell division

Overlapping and essential roles for molecular and mechanical mechanisms in mycobacterial cell division

Ultrastructure of exospore formation inStreptomycesrevealed by cryo-electron tomography

Stable Regulation of Cell Cycle Events in Mycobacteria: Insights From Inherently Heterogeneous Bacterial Populations

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