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Cell water dynamics on multiple time scales

Persson Sunde, Erik LU and Halle, Bertil LU (2008) In Proceedings of the National Academy of Sciences 105(17). p.6266-6271
Abstract
Water–biomolecule interactions have been extensively studied in dilute solutions, crystals, and rehydrated powders, but none of these model systems may capture the behavior of water in the highly organized intracellular milieu. Because of the experimental difficulty of selectively probing the structure and dynamics of water in intact cells, radically different views about the properties of cell water have proliferated. To resolve this long-standing controversy, we have measured the 2H spin relaxation rate in living bacteria cultured in D2O. The relaxation data, acquired in a wide magnetic field range (0.2 mT–12 T) and analyzed in a model-independent way, reveal water dynamics on a wide range of time scales. Contradicting the view that a... (More)
Water–biomolecule interactions have been extensively studied in dilute solutions, crystals, and rehydrated powders, but none of these model systems may capture the behavior of water in the highly organized intracellular milieu. Because of the experimental difficulty of selectively probing the structure and dynamics of water in intact cells, radically different views about the properties of cell water have proliferated. To resolve this long-standing controversy, we have measured the 2H spin relaxation rate in living bacteria cultured in D2O. The relaxation data, acquired in a wide magnetic field range (0.2 mT–12 T) and analyzed in a model-independent way, reveal water dynamics on a wide range of time scales. Contradicting the view that a substantial fraction of cell water is strongly perturbed, we find that ≈85% of cell water in Escherichia coli and in the extreme halophile Haloarcula marismortui has bulk-like dynamics. The remaining ≈15% of cell water interacts directly with biomolecular surfaces and is motionally retarded by a factor 15 ± 3 on average, corresponding to a rotational correlation time of 27 ps. This dynamic perturbation is three times larger than for small monomeric proteins in solution, a difference we attribute to secluded surface hydration sites in supramolecular assemblies. The relaxation data also show that a small fraction (≈0.1%) of cell water exchanges from buried hydration sites on the microsecond time scale, consistent with the current understanding of protein hydration in solutions and crystals. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Haloarcula marismortui, in vivo NMR, buried water molecules, Escherichia coli, biomolecular hydration
in
Proceedings of the National Academy of Sciences
volume
105
issue
17
pages
6266 - 6271
publisher
National Acad Sciences
external identifiers
  • wos:000255534100012
  • scopus:44049105071
ISSN
1091-6490
DOI
10.1073/pnas.0709585105
language
English
LU publication?
yes
id
26098097-d856-4b65-a12d-417f398f242b (old id 1227838)
date added to LUP
2008-09-05 11:14:49
date last changed
2017-09-03 03:46:16
@article{26098097-d856-4b65-a12d-417f398f242b,
  abstract     = {Water–biomolecule interactions have been extensively studied in dilute solutions, crystals, and rehydrated powders, but none of these model systems may capture the behavior of water in the highly organized intracellular milieu. Because of the experimental difficulty of selectively probing the structure and dynamics of water in intact cells, radically different views about the properties of cell water have proliferated. To resolve this long-standing controversy, we have measured the 2H spin relaxation rate in living bacteria cultured in D2O. The relaxation data, acquired in a wide magnetic field range (0.2 mT–12 T) and analyzed in a model-independent way, reveal water dynamics on a wide range of time scales. Contradicting the view that a substantial fraction of cell water is strongly perturbed, we find that ≈85% of cell water in Escherichia coli and in the extreme halophile Haloarcula marismortui has bulk-like dynamics. The remaining ≈15% of cell water interacts directly with biomolecular surfaces and is motionally retarded by a factor 15 ± 3 on average, corresponding to a rotational correlation time of 27 ps. This dynamic perturbation is three times larger than for small monomeric proteins in solution, a difference we attribute to secluded surface hydration sites in supramolecular assemblies. The relaxation data also show that a small fraction (≈0.1%) of cell water exchanges from buried hydration sites on the microsecond time scale, consistent with the current understanding of protein hydration in solutions and crystals.},
  author       = {Persson Sunde, Erik and Halle, Bertil},
  issn         = {1091-6490},
  keyword      = {Haloarcula marismortui,in vivo NMR,buried water molecules,Escherichia coli,biomolecular hydration},
  language     = {eng},
  number       = {17},
  pages        = {6266--6271},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences},
  title        = {Cell water dynamics on multiple time scales},
  url          = {http://dx.doi.org/10.1073/pnas.0709585105},
  volume       = {105},
  year         = {2008},
}