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Cell-biological studies of osmotic shock response in Streptomyces spp

Fuchino, Katsuya LU ; Flärdh, Klas LU ; Dyson, Paul and Ausmees, Nora LU (2017) In Journal of Bacteriology 199(1).
Abstract

Most bacteria are likely to face osmotic challenges, but there is yet much to learn about how such environmental changes affect the architecture of bacterial cells. Here, we report a cell-biological study in model organisms of the genus Streptomyces, which are actinobacteria that grow in a highly polarized fashion to form branching hyphae. The characteristic apical growth of Streptomyces hyphae is orchestrated by protein assemblies, called polarisomes, which contain coiled-coil proteins DivIVA and Scy, and recruit cell wall synthesis complexes and the stressbearing cytoskeleton of FilP to the tip regions of the hyphae. We monitored cell growth and cell-architectural changes by time-lapse microscopy in osmotic upshift experiments.... (More)

Most bacteria are likely to face osmotic challenges, but there is yet much to learn about how such environmental changes affect the architecture of bacterial cells. Here, we report a cell-biological study in model organisms of the genus Streptomyces, which are actinobacteria that grow in a highly polarized fashion to form branching hyphae. The characteristic apical growth of Streptomyces hyphae is orchestrated by protein assemblies, called polarisomes, which contain coiled-coil proteins DivIVA and Scy, and recruit cell wall synthesis complexes and the stressbearing cytoskeleton of FilP to the tip regions of the hyphae. We monitored cell growth and cell-architectural changes by time-lapse microscopy in osmotic upshift experiments. Hyperosmotic shock caused arrest of growth, loss of turgor, and hypercondensation of chromosomes. The recovery period was protracted, presumably due to the dehydrated state of the cytoplasm, before hyphae could restore their turgor and start to grow again. In most hyphae, this regrowth did not take place at the original hyphal tips. Instead, cell polarity was reprogrammed, and polarisomes were redistributed to new sites, leading to the emergence of multiple lateral branches from which growth occurred. Factors known to regulate the branching pattern of Streptomyces hyphae, such as the serine/threonine kinase AfsK and Scy, were not involved in reprogramming of cell polarity, indicating that different mechanisms may act under different environmental conditions to control hyphal branching. Our observations of hyphal morphology during the stress response indicate that turgor and sufficient hydration of cytoplasm are required for Streptomyces tip growth.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Apical growth, Bacterial cytoskeleton, Osmotic stress response, Streptomyces, Turgor
in
Journal of Bacteriology
volume
199
issue
1
publisher
American Society for Microbiology
external identifiers
  • scopus:85008501950
  • wos:000391288200009
ISSN
0021-9193
DOI
10.1128/JB.00465-16
language
English
LU publication?
yes
id
ba3c3736-006b-4da0-82cd-ac260812cd84
date added to LUP
2017-03-16 14:01:14
date last changed
2018-01-07 11:56:03
@article{ba3c3736-006b-4da0-82cd-ac260812cd84,
  abstract     = {<p>Most bacteria are likely to face osmotic challenges, but there is yet much to learn about how such environmental changes affect the architecture of bacterial cells. Here, we report a cell-biological study in model organisms of the genus Streptomyces, which are actinobacteria that grow in a highly polarized fashion to form branching hyphae. The characteristic apical growth of Streptomyces hyphae is orchestrated by protein assemblies, called polarisomes, which contain coiled-coil proteins DivIVA and Scy, and recruit cell wall synthesis complexes and the stressbearing cytoskeleton of FilP to the tip regions of the hyphae. We monitored cell growth and cell-architectural changes by time-lapse microscopy in osmotic upshift experiments. Hyperosmotic shock caused arrest of growth, loss of turgor, and hypercondensation of chromosomes. The recovery period was protracted, presumably due to the dehydrated state of the cytoplasm, before hyphae could restore their turgor and start to grow again. In most hyphae, this regrowth did not take place at the original hyphal tips. Instead, cell polarity was reprogrammed, and polarisomes were redistributed to new sites, leading to the emergence of multiple lateral branches from which growth occurred. Factors known to regulate the branching pattern of Streptomyces hyphae, such as the serine/threonine kinase AfsK and Scy, were not involved in reprogramming of cell polarity, indicating that different mechanisms may act under different environmental conditions to control hyphal branching. Our observations of hyphal morphology during the stress response indicate that turgor and sufficient hydration of cytoplasm are required for Streptomyces tip growth.</p>},
  articleno    = {e00465-16},
  author       = {Fuchino, Katsuya and Flärdh, Klas and Dyson, Paul and Ausmees, Nora},
  issn         = {0021-9193},
  keyword      = {Apical growth,Bacterial cytoskeleton,Osmotic stress response,Streptomyces,Turgor},
  language     = {eng},
  number       = {1},
  publisher    = {American Society for Microbiology},
  series       = {Journal of Bacteriology},
  title        = {Cell-biological studies of osmotic shock response in Streptomyces spp},
  url          = {http://dx.doi.org/10.1128/JB.00465-16},
  volume       = {199},
  year         = {2017},
}