SecA defects are accompanied by dysregulation of MukB, DNA gyrase, chromosome partitioning and DNA superhelicity in Escherichia coli

Adachi, Shun; Murakawa, Yuji; Hiraga, Sota

doi:10.1099/mic.0.077685-0

Cited by 6 publications

(21 citation statements)

References 43 publications

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“…We revealed that the ATPase activity of SecA was essential for dynamic localization of these proteins. Integrating the present results with our previous work that SecA/SecY/AcpP genetically interact with MukB and DNA topoisomerases (Adachi et al, 2014 ), we hypothesize that SecA/SecY/AcpP is the core component of the dynamic property of the chromosome segregation proteins in E. coli .…”

Section: Introductionsupporting

confidence: 88%

“…Finally, ADP is converted to ATP and the cycle is repeated again and again (Bauer et al, 2014 ). Previously we have described that SecA, SecY, and A cyl c arrier p rotein P (AcpP) are involved in chromosome partition and that inactivation of SecA causes disorder in decatenation and maintenance of superhelicity on plasmid DNA (Adachi et al, 2014 ). AcpP, which is an acyl carrier protein of ACP complex, acts as a source of acyl groups inside the cell of E. coli .…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, AcpP is copurified with MukB (Niki et al, 1992 ), suggesting the role of AcpP on chromosome segregation. It is notable that AcpP binds to both SecA and MukB, In addition, we have described that a network involving the interaction of SecA/SecY-AcpP-MukB-Topo IV (DNA topoisomerase IV, ParC/ParE complex)/SeqA-DNA gyrase (GyrA/GyrB complex) may be important for chromosome positioning and partitioning (separation of chromosomes) (Adachi et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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Dynamic nature of SecA and its associated proteins in Escherichia coli

2015

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Mechanical properties such as physical constraint and pushing of chromosomes are thought to be important for chromosome segregation in Escherichia coli and it could be mediated by a hypothetical molecular “tether.” However, the actual tether that mediates these features is not known. We previously described that SecA (Secretory A) and Secretory Y (SecY), components of the membrane protein translocation machinery, and AcpP (Acyl carrier protein P) were involved in chromosome segregation and homeostasis of DNA topology. In the present work, we performed three-dimensional deconvolution of microscopic images and time-lapse experiments of these proteins together with MukB and DNA topoisomerases, and found that these proteins embraced the structures of tortuous nucleoids with condensed regions. Notably, SecA, SecY, and AcpP dynamically localized in cells, which was interdependent on each other requiring the ATPase activity of SecA. Our findings imply that the membrane protein translocation machinery plays a role in the maintenance of proper chromosome partitioning, possibly through “tethering” of MukB [a functional homolog of structural maintenance of chromosomes (SMC) proteins], DNA gyrase, DNA topoisomerase IV, and SeqA (Sequestration A).

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Section: Introductionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Dynamic nature of SecA and its associated proteins in Escherichia coli

2015

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“…52 Other studies reported an attachment at 20-30 membrane sites in addition to oriC. 54,55 Alternately, this linkage might result from an interaction with DNA coupling transcription, translation and insertion of membrane proteins 56,57 i.e. 54,55 Alternately, this linkage might result from an interaction with DNA coupling transcription, translation and insertion of membrane proteins 56,57 i.e.…”

Section: Chromosomal Linkages To the Inner Membranementioning

confidence: 99%

Single cell super-resolution imaging ofE. coliOmpR during environmental stress

Foo

Spahn

Zhang

et al. 2015

Integrative Biology

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Two-component signaling systems are a major strategy employed by bacteria, and to some extent, yeast and plants, to respond to environmental stress. The EnvZ/OmpR system in E. coli responds to osmotic and acid stress and is responsible for regulating the protein composition of the outer membrane. EnvZ is a histidine kinase located in the inner membrane. Upon activation, it is autophosphorylated by ATP and subsequently, it activates OmpR. Phosphorylated OmpR binds with high affinity to the regulatory regions of the ompF and ompC porin genes to regulate their transcription. We set out to visualize these two-components in single bacterial cells during different environmental stress conditions and to examine the subsequent modifications to the bacterial nucleoid as a result. We created a chromosomally-encoded, active, fluorescent OmpR-PAmCherry fusion protein and compared its expression levels with RNA polymerase. Quantitative western blotting had indicated that these two proteins were expressed at similar levels. From our images, it is evident that OmpR is significantly less abundant compared to RNA polymerase. In cross-sectional axial images, we observed OmpR molecules closely juxtaposed near the inner membrane during acidic and hyposomotic growth. In acidic conditions, the chromosome was compacted. Surprisingly, under acidic conditions, we also observed evidence of a spatial correlation between the DNA and the inner membrane, suggesting a mechanical link through an active DNA-OmpR-EnvZ complex. This work represents the first direct visualization of a response regulator with respect to the bacterial chromosome.

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“…Although in addition to the latter also other proteins with more specific functions are involved in the organisation of the nucleoid structure [see e.g. Adachi et al, 2014;Edwards et al, 2013; for a review, see Dame et al, 2011], we primarily consider the effects of the NAPs, which not only regulate the chromosomal dynamics but also act as global regulators of gene expression [Browning et al, 2010;Dillon and Dorman, 2010;Dorman, 2013;Rimsky and Travers, 2011;Travers and Muskhelishvili, 2005a]. Indeed, the comparisons of the genomic NAP binding patterns with spatial transcript profiles revealed remarkable correlations [Scolari et al, 2011].…”

Section: Structural Organisation Of the Bacterial Chromosome: A Briefmentioning

confidence: 99%

Order from the Order: How a Spatiotemporal Genetic Program Is Encoded in a 2-D Genetic Map of the Bacterial Chromosome

Muskhelishvili

Travers²

2014

Microb Physiol

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In this article, we sketch out a holistic methodology used for exploring how the genetic program is encoded in a 2-D genetic map of a bacterial chromosome. We argue that the major problem resides in the conceptual integration of the two logically distinct types of information encoded in the chiral double-helical DNA polymer. This integration is accomplished by mapping the genetic function on the genomic sequence organisation and therefore is potentially applicable to any chromosome. The vast generalisation achieved by this approach necessarily ignores exquisite details, yet it is fundamental in providing comprehensive methodology for exploring the role of the DNA sequence organisation in harnessing genetic information and sustaining biological order.

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SecA defects are accompanied by dysregulation of MukB, DNA gyrase, chromosome partitioning and DNA superhelicity in Escherichia coli

Cited by 6 publications

References 43 publications

Dynamic nature of SecA and its associated proteins in Escherichia coli

Dynamic nature of SecA and its associated proteins in Escherichia coli

Single cell super-resolution imaging ofE. coliOmpR during environmental stress

Order from the Order: How a Spatiotemporal Genetic Program Is Encoded in a 2-D Genetic Map of the Bacterial Chromosome

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