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Unstructured hydrophilic sequences in prokaryotic proteomes correlate with dehydration tolerance and host association

Unstructured hydrophilic sequences in prokaryotic proteomes correlate with dehydration tolerance and host association
Unstructured hydrophilic sequences in prokaryotic proteomes correlate with dehydration tolerance and host association

Water loss or desiccation is among the most life-threatening stresses. It leads to DNA double-strand breakage, protein aggregation, cell shrinkage, and low water activity precluding all biological functions. Yet, in all kingdoms of life, rare organisms are resistant to desiccation through prevention or reversibility of such damage. Here, we explore possible hallmarks of prokaryotic desiccation tolerance in their proteomes. The content of unstructured, low complexity (LC) regions was analyzed in a total of 460 bacterial and archaeal proteomes. It appears that species endowed with proteomes abundant in unstructured hydrophilic LC regions are desiccation-tolerant or sporulating bacteria, halophilic archaea and bacteria, or host-associated species. In the desiccation- and radiation-resistant bacterium Deinococcus radiodurans, most proteins that contain large hydrophilic LC regions have unassigned function, but those with known function are mostly involved in diverse cellular recovery processes. Such LC regions are typically absent in orthologous proteins in desiccation-sensitive species. D. radiodurans encodes also special LC proteins, akin to those associated with desiccation resistance of plant seeds and some plants and animals. Therefore, we postulate that large unstructured hydrophilic LC regions and proteins provide for cellular resistance to dehydration and we discuss mechanisms of their protective activity.

Archaea/chemistry, Archaeal Proteins/chemistry, Bacteria/chemistry, Bacterial Proteins/chemistry, Desiccation, Protein Structure, Tertiary, Proteome/analysis
0022-2836
775-82
Kriško, Anita
cad25bd5-1011-4c0e-951d-daa0d970201d
Smole, Zlatko
09775a99-3e77-4b71-ac58-0404c1c2f842
Debret, Gaelle
6a6c058c-99cb-43d6-9e9e-a4dc0844af3c
Nikolić, Nela
88a8f576-d9e2-4eb6-9219-39b7065963d3
Radman, Miroslav
7a0fdecd-b28b-42f7-8d43-0ee415bd3ae2
Kriško, Anita
cad25bd5-1011-4c0e-951d-daa0d970201d
Smole, Zlatko
09775a99-3e77-4b71-ac58-0404c1c2f842
Debret, Gaelle
6a6c058c-99cb-43d6-9e9e-a4dc0844af3c
Nikolić, Nela
88a8f576-d9e2-4eb6-9219-39b7065963d3
Radman, Miroslav
7a0fdecd-b28b-42f7-8d43-0ee415bd3ae2

Kriško, Anita, Smole, Zlatko, Debret, Gaelle, Nikolić, Nela and Radman, Miroslav (2010) Unstructured hydrophilic sequences in prokaryotic proteomes correlate with dehydration tolerance and host association. Journal of Molecular Biology, 402 (5), 775-82. (doi:10.1016/j.jmb.2010.08.012).

Record type: Article

Abstract

Water loss or desiccation is among the most life-threatening stresses. It leads to DNA double-strand breakage, protein aggregation, cell shrinkage, and low water activity precluding all biological functions. Yet, in all kingdoms of life, rare organisms are resistant to desiccation through prevention or reversibility of such damage. Here, we explore possible hallmarks of prokaryotic desiccation tolerance in their proteomes. The content of unstructured, low complexity (LC) regions was analyzed in a total of 460 bacterial and archaeal proteomes. It appears that species endowed with proteomes abundant in unstructured hydrophilic LC regions are desiccation-tolerant or sporulating bacteria, halophilic archaea and bacteria, or host-associated species. In the desiccation- and radiation-resistant bacterium Deinococcus radiodurans, most proteins that contain large hydrophilic LC regions have unassigned function, but those with known function are mostly involved in diverse cellular recovery processes. Such LC regions are typically absent in orthologous proteins in desiccation-sensitive species. D. radiodurans encodes also special LC proteins, akin to those associated with desiccation resistance of plant seeds and some plants and animals. Therefore, we postulate that large unstructured hydrophilic LC regions and proteins provide for cellular resistance to dehydration and we discuss mechanisms of their protective activity.

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More information

Published date: 8 October 2010
Additional Information: Copyright © 2010 Elsevier Ltd. All rights reserved.
Keywords: Archaea/chemistry, Archaeal Proteins/chemistry, Bacteria/chemistry, Bacterial Proteins/chemistry, Desiccation, Protein Structure, Tertiary, Proteome/analysis

Identifiers

Local EPrints ID: 488030
URI: http://eprints.soton.ac.uk/id/eprint/488030
ISSN: 0022-2836
PURE UUID: 5f65a0ca-560f-40fe-bec3-7d575a4cd736
ORCID for Nela Nikolić: ORCID iD orcid.org/0000-0001-9068-6090

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Date deposited: 12 Mar 2024 18:21
Last modified: 18 Mar 2024 04:18

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Contributors

Author: Anita Kriško
Author: Zlatko Smole
Author: Gaelle Debret
Author: Nela Nikolić ORCID iD
Author: Miroslav Radman

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