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Abstract Tardigrades are a group of microscopic animals renowned for their ability to survive near complete desiccation. A family of proteins, unique to tardigrades, called Cytoplasmic Abundant Heat Soluble (CAHS) proteins are necessary to mediate robust desiccation tolerance in these animals. However, the mechanism(s) by which CAHS proteins help to protect tardigrades during water-loss have not been fully elucidated. Here we use thermogravimetric analysis to empirically test the proposed hypothesis that tardigrade CAHS proteins, due to their propensity to form hydrogels, help to retain water during desiccation. We find that regardless of its gelled state, both in vitro and in vivo, a model CAHS protein (CAHS D) retains no more water than common proteins and control cells in the dry state. However, we find that while CAHS D proteins do not increase the total amount of water retained in a dry system, they interact with the small amount of water that does remain. Our study indicates that desiccation tolerance mediated by CAHS D cannot be simply ascribed to water retention and instead implicates its ability to interact more tightly with residual water as a possible mechanism underlying its protective capacity. These results advance our fundamental understanding of tardigrade desiccation tolerance which could provide potential avenues for new technologies to aid in the storage of dry shelf-stable pharmaceuticals and the generation of stress tolerant crops to ensure food security in the face of global climate change.
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Tardigrade small heat shock proteins can limit desiccation-induced protein aggregation
Abstract Small heat shock proteins (sHSPs) are chaperones with well-characterized roles in heat stress, but potential roles for sHSPs in desiccation tolerance have not been as thoroughly explored. We identified nine sHSPs from the tardigradeHypsibius exemplaris, each containing a conserved alpha-crystallin domain flanked by disordered regions. Many of these sHSPs are highly expressed. Multiple tardigrade and human sHSPs could improve desiccation tolerance ofE. coli, suggesting that the capacity to contribute to desicco-protection is a conserved property of some sHSPs. Purification and subsequent analysis of two tardigrade sHSPs, HSP21 and HSP24.6, revealed that these proteins can oligomerize in vitro. These proteins limited heat-induced aggregation of the model enzyme citrate synthase. Heterologous expression of HSP24.6 improved bacterial heat shock survival, and the protein significantly reduced heat-induced aggregation of soluble bacterial protein. Thus, HSP24.6 likely chaperones against protein aggregation to promote heat tolerance. Furthermore, HSP21 and HSP24.6 limited desiccation-induced aggregation and loss of function of citrate synthase. This suggests a mechanism by which tardigrade sHSPs promote desiccation tolerance, by limiting desiccation-induced protein aggregation, thereby maintaining proteostasis and supporting survival. These results suggest that sHSPs provide a mechanism of general stress resistance that can also be deployed to support survival during anhydrobiosis.
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- Award ID(s):
- 2028860
- PAR ID:
- 10393994
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 6
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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