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PreprintCited by 16Protein Structure and DynamicsTardigrade Biology and EcologyHeat shock proteins research

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Disordered proteins interact with the chemical environment to tune their protective function during drying

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KC, Shraddha, Nguyen, Kenny, Nicholson, Vincent, Walgren, Annie, Trent, Tony, Gollub, Edith, Romero, Sofia, Holehouse, Alex S., Sukenik, Shahar, Boothby, Thomas C.·2024·eLife
DOI 10.1101/2024.02.28.582506PMC PMC10925285

Preprint — published as 10.7554/elife.97231 · Paper page

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Abstract

The conformational ensemble and function of intrinsically disordered proteins (IDPs) are sensitive to their solution environment. The inherent malleability of disordered proteins combined with the exposure of their residues accounts for this sensitivity. One context in which IDPs play important roles that is concomitant with massive changes to the intracellular environment is during desiccation (extreme drying). The ability of organisms to survive desiccation has long been linked to the accumulation of high levels of cosolutes such as trehalose or sucrose as well as the enrichment of IDPs, such as late embryogenesis abundant (LEA) proteins or cytoplasmic abundant heat soluble (CAHS) proteins. Despite knowing that IDPs play important roles and are co-enriched alongside endogenous, species-specific cosolutes during desiccation, little is known mechanistically about how IDP-cosolute interactions influence desiccation tolerance. Here, we test the notion that the protective function of desiccation-related IDPs is enhanced through conformational changes induced by endogenous cosolutes. We find that desiccation-related IDPs derived from four different organisms spanning two LEA protein families and the CAHS protein family, synergize best with endogenous cosolutes during drying to promote desiccation protection. Yet the structural parameters of protective IDPs do not correlate with synergy for either CAHS or LEA proteins. We further demonstrate that for CAHS, but not LEA proteins, synergy is related to self-assembly and the formation of a gel. Our results suggest that functional synergy between IDPs and endogenous cosolutes is a convergent desiccation protection strategy seen among different IDP families and organisms, yet, the mechanisms underlying this synergy differ between IDP families.

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Metadata

Authors
KC, S., Nguyen, K., Nicholson, V., Walgren, A., Trent, T., Gollub, E., Romero, S., Holehouse, A. S., Sukenik, S., & Boothby, T. C.
Affiliations
  • University of Wyoming (US)
  • University of California, Merced (US)
  • Washington University in St. Louis (US)
Corresponding author
  • Sukenik, Shahar
  • Boothby, Thomas C.
ORCID
Venue
eLife
Publisher
openRxiv
Published
2024-03-02
Volume
13
ISSN
2050-084X (ISSN-L)
DOI
10.1101/2024.02.28.582506
PMC
PMC10925285
OpenAlex
W4404527234
Cited by
16
References
1
Citations by year
2026: 4 · 2025: 11 · 2024: 1
FWCI
2.18
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
Funders
  • National Science Foundation (2213983, 2128067, 2128068, 2128069)
  • U.S. Department of Energy
  • U.S. Department of Agriculture (1012152)
  • National Institutes of Health (5p20gm103432-23, 2P20GM103432)
  • National Institute of Food and Agriculture (#1012152)
  • National Institute of General Medical Sciences (2 P20 GM103432)
  • Division of Biological Infrastructure (2213983)
  • Basic Energy Sciences
  • Biological and Environmental Research
  • Lawrence Berkeley National Laboratory
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Tardigrade Biology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
Keywords
intrinsically disordered proteins, desiccation tolerance, late embryogenesis abundant proteins, protein self-assembly, protein conformational change, protein-protein interaction

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