Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates.
Small heat shock proteins (sHsps) are a conserved class of ATP-independent chaperones that bind to aggregation-prone polypeptides at stress conditions. sHsps encage these polypeptides in assemblies, shielding them from further aggregation. To facilitate their subsequent solubilization and refolding...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-10-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1008479 |
| _version_ | 1818581300177534976 |
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| author | Igor Obuchowski Artur Piróg Milena Stolarska Bartłomiej Tomiczek Krzysztof Liberek |
| author_facet | Igor Obuchowski Artur Piróg Milena Stolarska Bartłomiej Tomiczek Krzysztof Liberek |
| author_sort | Igor Obuchowski |
| collection | DOAJ |
| description | Small heat shock proteins (sHsps) are a conserved class of ATP-independent chaperones that bind to aggregation-prone polypeptides at stress conditions. sHsps encage these polypeptides in assemblies, shielding them from further aggregation. To facilitate their subsequent solubilization and refolding by Hsp70 (DnaK) and Hsp100 (ClpB) chaperones, first, sHsps need to dissociate from the assemblies. In most γ-proteobacteria, these functions are fulfilled by a single sHsp (IbpA), but in a subset of Enterobacterales, a two-protein sHsp (IbpA and IbpB) system has evolved. To gain insight into the emergence of complexity within this chaperone system, we reconstructed the phylogeny of γ-proteobacteria and their sHsps. We selected proteins representative of systems comprising either one or two sHsps and analysed their ability to form sHsps-substrate assemblies. All the tested IbpA proteins, but not IbpBs, stably interact with an aggregating substrate. Moreover, in Escherichia coli cells, ibpA but not ibpB suppress the growth defect associated with low DnaK level, which points to the major protective role of IbpA during the breakdown of protein quality control. We also examined how sHsps affect the association of Hsp70 with the assemblies at the initial phase of disaggregation and how they affect protein recovery after stress. Our results suggest that a single gene duplication event has given rise to the sHsp system consisting of a strong canonical binder, IbpA, and its non-canonical paralog IbpB that enhances sHsps dissociation from the assemblies. The cooperation between the sHsps reduces the demand for Hsp70 needed to outcompete them from the assemblies by promoting sHsps dissociation without compromising assembly formation at heat shock. This potentially increases the robustness and elasticity of sHsps protection against irreversible aggregation. |
| first_indexed | 2024-12-16T07:31:18Z |
| format | Article |
| id | doaj.art-e6bae949cadb421fa2da2f6e752e22fb |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-16T07:31:18Z |
| publishDate | 2019-10-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-e6bae949cadb421fa2da2f6e752e22fb2022-12-21T22:39:20ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-10-011510e100847910.1371/journal.pgen.1008479Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates.Igor ObuchowskiArtur PirógMilena StolarskaBartłomiej TomiczekKrzysztof LiberekSmall heat shock proteins (sHsps) are a conserved class of ATP-independent chaperones that bind to aggregation-prone polypeptides at stress conditions. sHsps encage these polypeptides in assemblies, shielding them from further aggregation. To facilitate their subsequent solubilization and refolding by Hsp70 (DnaK) and Hsp100 (ClpB) chaperones, first, sHsps need to dissociate from the assemblies. In most γ-proteobacteria, these functions are fulfilled by a single sHsp (IbpA), but in a subset of Enterobacterales, a two-protein sHsp (IbpA and IbpB) system has evolved. To gain insight into the emergence of complexity within this chaperone system, we reconstructed the phylogeny of γ-proteobacteria and their sHsps. We selected proteins representative of systems comprising either one or two sHsps and analysed their ability to form sHsps-substrate assemblies. All the tested IbpA proteins, but not IbpBs, stably interact with an aggregating substrate. Moreover, in Escherichia coli cells, ibpA but not ibpB suppress the growth defect associated with low DnaK level, which points to the major protective role of IbpA during the breakdown of protein quality control. We also examined how sHsps affect the association of Hsp70 with the assemblies at the initial phase of disaggregation and how they affect protein recovery after stress. Our results suggest that a single gene duplication event has given rise to the sHsp system consisting of a strong canonical binder, IbpA, and its non-canonical paralog IbpB that enhances sHsps dissociation from the assemblies. The cooperation between the sHsps reduces the demand for Hsp70 needed to outcompete them from the assemblies by promoting sHsps dissociation without compromising assembly formation at heat shock. This potentially increases the robustness and elasticity of sHsps protection against irreversible aggregation.https://doi.org/10.1371/journal.pgen.1008479 |
| spellingShingle | Igor Obuchowski Artur Piróg Milena Stolarska Bartłomiej Tomiczek Krzysztof Liberek Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. PLoS Genetics |
| title | Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. |
| title_full | Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. |
| title_fullStr | Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. |
| title_full_unstemmed | Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. |
| title_short | Duplicate divergence of two bacterial small heat shock proteins reduces the demand for Hsp70 in refolding of substrates. |
| title_sort | duplicate divergence of two bacterial small heat shock proteins reduces the demand for hsp70 in refolding of substrates |
| url | https://doi.org/10.1371/journal.pgen.1008479 |
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