groES

UniProt ID: Q88N56
Organism: Pseudomonas putida (strain ATCC 47054 / DSM 6125 / CFBP 8728 / NCIMB 11950 / KT2440)
Review Status: COMPLETE
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Gene Description

GroES (Cpn10/Hsp10, ~10 kDa) is the bacterial co-chaperonin partner of the GroEL chaperonin. It assembles as a heptameric, dome-shaped ring that binds in an ATP-dependent manner to the apical surface of a GroEL ring, capping the central cavity to form an enclosed nano-cage. Encapsulation of non-native substrate proteins in this chamber provides a folding-permissive environment that promotes productive folding and prevents aggregation, with cyclic GroES binding and release driven by the GroEL ATPase. GroES acts in the cytoplasm and is a constitutive component of the cellular proteostasis machinery; in Pseudomonas putida the groES-groEL operon is part of the sigma-32 (RpoH)-controlled heat-shock regulon and is induced under thermal, solvent, pressure and other proteotoxic stresses. The GroEL/GroES system is essential for viability in most bacteria.

Existing Annotations Review

GO Term Evidence Action Reason
GO:0005524 ATP binding
IEA
GO_REF:0000002
REMOVE
Summary: ATP binding within the GroEL/GroES chaperonin system is a property of GroEL, not of the GroES co-chaperonin. GroES itself has no nucleotide-binding site; its binding to GroEL is triggered by ATP binding to GroEL.
Reason: This InterPro-based IEA annotation conflates the ATP-dependent GroEL/GroES cycle with intrinsic ATP binding by GroES. GroES does not bind ATP; ATP binding is performed by the GroEL subunit. The annotation is an over-propagation from a family-level signature and is not appropriate for the co-chaperonin.
GO:0005737 cytoplasm
IEA
GO_REF:0000120
ACCEPT
Summary: GroES is a soluble cytoplasmic protein that binds cytoplasmic GroEL to form folding chambers. UniProt subcellular location and the conserved biology of the GroEL/GroES system support cytoplasmic localization.
GO:0006457 protein folding
IEA
GO_REF:0000120
ACCEPT
Summary: Assisting protein folding is the central biological role of GroES, which together with GroEL encapsulates non-native substrates in a folding chamber. This is the core process annotation for the gene. In P. putida KT2440 the groES (PP_1360)-groEL (PP_1361) operon is induced under heat, pressure and aromatic-solvent stress as part of the sigma-32/RpoH proteostasis regulon (see deep research).
Supporting Evidence:
file:PSEPK/groES/groES-deep-research-falcon.md
GroES participates in bacterial proteostasis and the heat-shock/stress response by assisting GroEL-mediated folding; in KT2440 groES/PP_1360 is induced together with groEL and rpoH under pressure and aromatic-solvent stress.
GO:0044183 protein folding chaperone
IEA
GO_REF:0000002
ACCEPT
Summary: GroES acts as a co-chaperonin that, in cooperation with GroEL, mediates protein folding. This molecular-function term captures the chaperone activity and is a core function annotation.
GO:0046872 metal ion binding
IEA
GO_REF:0000118
REMOVE
Summary: GroES has no established metal-ion-binding function. The co-chaperonin is a small beta-barrel protein whose function is to cap GroEL; metal binding is not part of its mechanism and is not described in UniProt or the structural literature for GroES.
Reason: This is a TreeGrafter/PANTHER tree-based over-annotation without support in the experimental or structural literature for GroES family proteins. Metal ion binding is not a known molecular function of the co-chaperonin.
GO:0051087 protein-folding chaperone binding
IEA
GO_REF:0000118
ACCEPT
Summary: GroES binds directly to the GroEL chaperonin, its obligate functional partner, capping the GroEL ring to form the folding chamber. Binding to the GroEL chaperonin is well supported and central to GroES function.

Core Functions

Co-chaperonin that binds GroEL to form an enclosed nano-cage promoting productive folding of non-native proteins in the cytoplasm

Molecular Function:
protein folding chaperone
Directly Involved In:
Cellular Locations:
Supporting Evidence:
  • PMID:39169181
    GroES binds GroEL to form closed folding chambers that allow non-native proteins to fold while protected from aggregation; in situ cryo-ET visualizes GroEL-GroES complexes operating intracellularly.

Binds the GroEL chaperonin in an ATP-dependent manner, capping the GroEL ring aperture

Supporting Evidence:
  • PMID:38064510
    GroES binding to GroEL is ATP-dependent and roughly doubles the chamber volume to create the encapsulated folding environment.

References

file:PSEPK/groES/groES-deep-research-falcon.md
Deep research report for groES (Q88N56 / PP_1360) in Pseudomonas putida KT2440
  • In KT2440, groES (PP_1360) lies immediately upstream of groEL (PP_1361) and both are induced together with rpoH under elevated pressure and aromatic-solvent stress, consistent with membership in the sigma-32/RpoH heat-shock regulon.
Gene Ontology annotation through association of InterPro records with GO terms
TreeGrafter-generated GO annotations
Combined Automated Annotation using Multiple IEA Methods
Visualizing chaperonin function in situ by cryo-electron tomography
  • GroEL/GroES forms folding chambers operating in the cytoplasm; both asymmetric (GroEL-GroES1) and symmetric (GroEL-GroES2) complexes are abundant and shift toward asymmetric under heat stress.
Structural basis of substrate progression through the bacterial chaperonin cycle
  • GroES binding to GroEL is ATP-dependent and approximately doubles chamber volume to create an encapsulated folding environment.

Deep Research

Falcon

(groES-deep-research-falcon.md)
Comprehensive Research Report: **groES** (UniProt Q88N56; locus **PP_1360**) in *Pseudomonas putida* KT2440 Falcon Edison Scientific Literature 34 citations 1 artifacts 2026-06-11T17:29:22.112575

The research report should be a detailed narrative explaining the function, biological processes, and localization of the gene product. Citations should be given for all claims.

You should prioritize authoritative reviews and primary scientific literature when conducting research. You can supplement
this with annotations you find in gene/protein databases, but these can be outdated or inaccurate.

We are specifically interested in the primary function of the gene - for enzymes, what reaction is catalyzed, and what is the substrate specificity? For transporters, what is the substrate? For structural proteins or adapters, what is the broader structural role? For signaling molecules, what is the role in the pathway.

We are interested in where in or outside the cell the gene product carries out its function.

We are also interested in the signaling or biochemical pathways in which the gene functions. We are less interested in broad pleiotropic effects, except where these elucidate the precise role.

Include evidence where possible. We are interested in both experimental evidence as well as inference from structure, evolution, or bioinformatic analysis. Precise studies should be prioritized over high-throughput, where available.

Comprehensive Research Report: groES (UniProt Q88N56; locus PP_1360) in Pseudomonas putida KT2440

1) Target verification (critical identity checks)

The target protein UniProt Q88N56 corresponds to GroES (Cpn10/Hsp10; ~10 kDa co-chaperonin) in Pseudomonas putida strain KT2440, encoded by groES with ordered locus name PP_1360. In KT2440 transcriptomic datasets, PP_1360 is explicitly annotated as “co-chaperonin GroES” and is adjacent to PP_1361 (groEL; “chaperonin 60 kDa”), consistent with the canonical bacterial groES–groEL locus organization and the GroES family assignment described in UniProt. (follonier2013newinsightson pages 5-6)

2) Key concepts and definitions (current understanding)

2.1 What GroES is

GroES is the lid-shaped co-chaperonin that binds the bacterial chaperonin GroEL, forming closed folding chambers that allow non-native proteins to fold while protected from aggregation. Structurally and functionally, GroES is typically a heptamer (7-mer) of ~10 kDa subunits that caps a GroEL ring aperture. (wagner2024visualizingchaperoninfunction pages 1-2, gardner2023structuralbasisof pages 1-2)

2.2 What GroES does (primary molecular function)

GroES does not catalyze a chemical reaction; rather, it is a protein-folding cofactor. In the GroEL/GroES cycle, ATP binding to GroEL promotes large conformational changes and GroES binding, which converts GroEL into an enclosed chamber (“cis” ring) where a substrate protein can fold. This encapsulation also remodels the internal environment (e.g., burying hydrophobic binding surfaces and creating a more folding-permissive cavity). (wagner2024visualizingchaperoninfunction pages 1-2, gardner2023structuralbasisof pages 1-2)

2.3 Client range and “substrate specificity”

GroES specificity is primarily physical/biophysical (non-native, aggregation-prone proteins) rather than sequence-specific. In E. coli (model evidence used for conserved inference), GroEL clients are often ~20–40 kDa, with fewer clients above ~50 kDa, and the chamber can accommodate up to roughly ~60 kDa (with some flexibility depending on conformational state). (gardner2023structuralbasisof pages 1-2, taguchi2023invivoclient pages 1-2)

2.4 Biological processes

In P. putida, GroEL/GroES is integrated into proteostasis and stress adaptation, including the heat-shock response (HSR) governed by the alternative sigma factor σ32/RpoH. GroEL/GroES are described as major chaperones involved in both normal growth proteome maintenance and stress recovery, and (together with DnaK/DnaJ/GrpE) provide negative-feedback control on σ32 activity through chaperone availability. (ito2014geneticandphenotypic pages 2-3)

3) Cellular localization and where GroES acts

GroES acts in the cytosol, where it binds cytosolic GroEL to form folding chambers and releases folded substrates back into the cytosol. Direct in-cell structural observations (in bacteria) show GroEL–GroES complexes operating intracellularly with substrates bound/encapsulated. No evidence in the retrieved sources suggests membrane insertion, secretion, or extracellular roles for GroES in P. putida. (wagner2024visualizingchaperoninfunction pages 1-2, wagner2024visualizingchaperoninfunction pages 3-4)

4) Pathways, operon context, and regulation in Pseudomonas putida KT2440

4.1 Operon/genomic context

Evidence from KT2440 transcriptomic annotation places groES at PP_1360 immediately upstream of groEL at PP_1361, consistent with the widely conserved groES–groEL arrangement. While adjacency is strongly supported, the retrieved excerpts do not directly map transcript boundaries (e.g., by Northern blot or transcript start/stop). (follonier2013newinsightson pages 5-6)

4.2 Regulation by RpoH (σ32) and heat-shock circuitry

Multiple lines of Pseudomonas evidence link groES/groEL to a σ32/RpoH-controlled heat-shock regulon. In KT2440, groES (PP_1360) and groEL (PP_1361) are explicitly listed among members of the RpoH (σ32) regulon induced under aromatic/solvent stress. (dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)

In KT strains, the heat-shock response includes rapid induction of hsp genes (including groEL), with induction occurring within ~10 minutes after temperature upshift and remaining elevated for at least ~30 minutes at higher temperatures (40–45°C conditions tested). Although this excerpt focuses on groEL rather than groES, it supports the operational linkage of the groE system to temperature stress response dynamics in P. putida. (ito2014geneticandphenotypic pages 6-8)

4.3 Stress-induced expression in KT2440 with quantitative data

Elevated pressure / industrially relevant bioreactor-like conditions (KT2440)

Under elevated pressure conditions, KT2440 shows a heat-shock-like transcriptional response including induction of groES/groEL and rpoH. Reported fold changes (microarray; adjusted P values):
- groES (PP_1360): +1.61 (Adj. P = 2.0E-02) under “Pressure”; +1.77 (Adj. P = 8.2E-02) under “Pressure Oxygen”.
- groEL (PP_1361): +1.78 (Adj. P = 1.0E-02) under “Pressure”; +2.19 (Adj. P = 6.0E-03) under “Pressure Oxygen”.
- rpoH (PP_5108): +1.49 (Adj. P = 3.6E-03) under “Pressure”; +1.57 (Adj. P = 8.7E-03) under “Pressure Oxygen”.
These coordinated inductions support that groES participates in a broader stress/proteostasis regulon in KT2440 relevant to industrial cultivation. (follonier2013newinsightson pages 5-6)

Aromatic solvent/toxicant exposure (KT2440; 15 min challenge)

After 15 minutes exposure to aromatics, groES/groEL are induced modestly but reproducibly as part of the σ32/RpoH program. Reported fold-changes (Table 5):
- groES (PP_1360): toluene 1.0; o-xylene 1.50; 3-methylbenzoate 1.45.
- groEL (PP_1361): toluene 1.1; o-xylene 1.83; 3-methylbenzoate 1.24.
The same study reports σ32 protein level measurements during these challenges and notes that some other RpoH genes show much larger induction (e.g., HslU up to ~12-fold), placing groES/groEL induction in context as part of a coordinated but gene-specific heat-shock regulon response. (dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)

Indole stress (P. putida; proteostasis disruption)

Indole exposure was reported to upregulate a set of heat-shock/protease genes including groEL and groES. Beyond transcriptional response, indole also directly impaired GroEL/GroES-mediated refolding of malate dehydrogenase (MDH) in vitro/assay conditions: with 1 mM indole present during GroEL/GroES-mediated MDH refolding, refolding rates decreased; after 60 min, up to ~70% native MDH activity could be regained but at reduced rates relative to chaperones alone. This supports a mechanistic link between indole toxicity and inhibition of ATP generation/protein folding capacity. (kim2013indoletoxicityinvolves pages 8-9)

5) Recent developments and latest research (prioritizing 2023–2024)

Because GroES is highly conserved, recent mechanistic work—although often performed in E. coli—is directly informative for functional annotation in P. putida.

5.1 2023: Structural basis for substrate progression through the GroEL/GroES cycle

A 2023 cryo-EM study resolved multiple nucleotide/complex states (including GroEL–GroES in a transition-state analog condition) and provided detailed snapshots for how a substrate progresses toward encapsulation. Key quantitative/mechanistic points include:
- GroEL is a tetradecameric double ring; GroES binding is ATP-dependent and approximately doubles chamber volume to create an encapsulated folding environment.
- Substrates are captured by hydrophobic apical helices and C-terminal tails, and conformational changes can exert a stretching/forced-unfolding effect.
- An asymmetric substrate-bound ring was described where 4 GroEL subunits contacted a 50.5 kDa Rubisco client, while 3 subunits adopted a GroES-accepting conformation, illuminating how GroES recruitment and substrate retention can be coordinated. (gardner2023structuralbasisof pages 1-2)

5.2 2024: In situ quantification of GroEL–GroES states and stoichiometry in living cells

A 2024 Nature cryo-electron tomography study measured GroEL/GroES complexes in situ and provided quantitative evidence for how GroES-capped complexes populate the cell:
- Under typical growth conditions, ~55–60% of GroEL is in asymmetric GroEL–GroES1 complexes, while ~40–45% is in symmetric GroEL–GroES2 complexes.
- Under heat stress, the asymmetric fraction increases to ~70%, and GroEL/GroES levels rise ~threefold, shifting the GroEL:ribosome ratio from ~1:23 (37°C) to ~1:10 (heat stress).
- Two trans-ring conformations of asymmetric complexes were resolved: a narrow opening (~45 Å) associated with substrate density and a wide opening (~65 Å) associated with substrate release; this connects GroES cycling to substrate acceptor/release states.
These findings refine and partially reconcile long-standing debates about whether GroEL/GroES cycles are primarily asymmetric or symmetric in vivo by showing both states are abundant and condition-dependent. (wagner2024visualizingchaperoninfunction pages 2-3, wagner2024visualizingchaperoninfunction pages 1-2, wagner2024visualizingchaperoninfunction pages 3-4)

5.3 2023: Expanding and interpreting “in vivo client” repertoires

A 2023 review synthesized progress in identifying GroEL/GroES “client proteins,” including obligate clients and broader interactor sets (primarily in E. coli). It emphasizes that GroEL/GroES is generally indispensable for bacterial viability and that modern proteomics-based methods reveal hundreds of GroE interactors and a subset of obligate folding clients. It further connects GroE client misfolding to degradation pathways (e.g., Lon), reinforcing GroES/GroEL’s role in protein quality control beyond folding alone. (taguchi2023invivoclient pages 1-2, taguchi2023invivoclient pages 6-6)

6) Current applications and real-world implementations (2023–2024 emphasized)

Although these applications are not specific to P. putida PP_1360, they are direct real-world uses of GroES/GroEL function as a folding module in engineered microbes.

6.1 Biomanufacturing and recombinant protein production

A 2024 study on PET plastic-degrading enzymes reported that co-expression of bacterial chaperones can greatly improve soluble expression and secretion. Specifically, co-expression of cognate DnaK/DnaJ increased soluble FastPETase up to 2.56-fold, and combining chaperone co-expression with a secretion strategy produced >2 g/L extracellular target protein in a 5-L bioreactor. The paper also cites prior GroEL/ES co-expression improving solubility for a related PETase with ~75 mg/L purified soluble protein. (wu2024boostingextracellularfastpetase pages 1-5)

6.2 Co-expression of GroEL/ES with Trigger Factor for difficult proteins

A 2024 study reported that GroEL/ES + Trigger Factor co-expression in E. coli supported production of a difficult viral protein (GST-F13), giving approximately 50–80 mg/L product in shake flasks (though much was recovered from insoluble fractions with refolding). This illustrates how GroES/GroEL is deployed even when proteins still require downstream refolding, to raise overall recoverable yield. (merkuleva2024theeffectsof pages 8-11)

7) Expert opinion and analysis (authoritative synthesis)

Across organism-specific stress transcriptomics (KT2440) and conserved mechanistic work, GroES is best annotated as a core cytosolic co-chaperonin required for GroEL-dependent protein folding under both basal and stress conditions. In P. putida KT2440, groES behaves like a stress-responsive σ32/RpoH-associated gene that is induced (often modestly) under multiple industrially relevant perturbations (pressure, aromatic solvents, toxic metabolites). (follonier2013newinsightson pages 5-6, dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8, kim2013indoletoxicityinvolves pages 8-9)

The 2023–2024 structural literature strengthens the mechanistic interpretation of these transcriptional responses: increased groES expression plausibly supports increased demand for GroEL chamber closure and cycling between asymmetric and symmetric complexes to maintain folding throughput and prevent aggregation during stress. (wagner2024visualizingchaperoninfunction pages 2-3, gardner2023structuralbasisof pages 1-2)

8) Key data summary (statistics from recent and strain-specific studies)

  • KT2440 elevated pressure induction: groES +1.61 (Adj. P=2.0E-02); groEL +1.78 (Adj. P=1.0E-02); rpoH +1.49 (Adj. P=3.6E-03). (follonier2013newinsightson pages 5-6)
  • KT2440 aromatic exposure (15 min): groES 1.50 (o-xylene), 1.45 (3-methylbenzoate); groEL 1.83 (o-xylene). (dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)
  • 2024 in situ chaperonin cycle: ~55–60% EL–ES1 vs ~40–45% EL–ES2 in growth; EL–ES1 rises to ~70% in heat stress; GroEL/GroES levels rise ~3×; GroEL:ribosome ratio shifts ~1:23 → ~1:10; trans-ring opening ~45 Å (narrow) vs ~65 Å (wide). (wagner2024visualizingchaperoninfunction pages 2-3, wagner2024visualizingchaperoninfunction pages 3-4)
  • 2024 biotechnology: >2 g/L extracellular FastPETase (5-L bioreactor) with chaperone + secretion strategy; soluble expression up to 2.56× with DnaK/DnaJ; cited GroEL/ES improving ThermoPETase solubility to ~75 mg/L purified soluble protein. (wu2024boostingextracellularfastpetase pages 1-5)

Gene: groES (PP_1360) in P. putida KT2440

Protein product: GroES (Cpn10/Hsp10), cytosolic co-chaperonin.

Primary function: Forms a heptameric lid that binds GroEL in an ATP-dependent manner to create an enclosed folding chamber for non-native proteins, thereby promoting correct folding and limiting aggregation; participates in σ32/RpoH-associated stress responses. (wagner2024visualizingchaperoninfunction pages 1-2, gardner2023structuralbasisof pages 1-2, dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)

Localization: Cytosol (functions as part of cytosolic GroEL–GroES folding complexes). (wagner2024visualizingchaperoninfunction pages 1-2)

Pathway/regulation: Part of the heat-shock/proteostasis network; in KT2440, groES is induced by multiple stresses (elevated pressure; aromatic solvent exposure) consistent with RpoH regulon membership. (follonier2013newinsightson pages 5-6, dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)

Phenotype/essentiality: Direct essentiality or knockout phenotype for P. putida KT2440 groES was not found in the retrieved excerpts; however, GroEL/GroES is widely described as indispensable for bacterial viability in model organisms, supporting strong functional importance by conserved biology. (taguchi2023invivoclient pages 1-2)

10) Consolidated table (evidence map)

Category Summary (1-2 sentences) Key evidence & quantitative data Key sources (include DOI URL and year)
Protein identity/family & domains Q88N56 in Pseudomonas putida KT2440 corresponds to GroES (Hsp10/Cpn10), the small co-chaperonin partner of GroEL in the conserved bacterial GroEL/GroES chaperonin system. The literature for Pseudomonas heat-shock/chaperonin biology is fully consistent with the UniProt annotation for locus PP_1360 as GroES adjacent to groEL/PP_1361. In KT2440 transcriptomics, PP_1360 is explicitly annotated as “co-chaperonin GroES,” with neighboring PP_1361 annotated as “chaperonin 60 kDa” (GroEL), matching the expected GroES/GroEL pair (follonier2013newinsightson pages 5-6). GroES is defined mechanistically as a heptameric ~10 kDa lid-shaped cofactor that caps GroEL rings (wagner2024visualizingchaperoninfunction pages 1-2, gardner2023structuralbasisof pages 1-2). Follonier et al., 2013, https://doi.org/10.1186/1475-2859-12-30 (2013) (follonier2013newinsightson pages 5-6); Wagner et al., 2024, https://doi.org/10.1038/s41586-024-07843-w (2024) (wagner2024visualizingchaperoninfunction pages 1-2); Gardner et al., 2023, https://doi.org/10.1073/pnas.2308933120 (2023) (gardner2023structuralbasisof pages 1-2)
Molecular function GroES acts as the co-chaperonin “lid” for GroEL, enabling ATP-dependent encapsulation of non-native proteins in a folding chamber rather than catalyzing a chemical reaction. Its primary role is to bind GroEL and help convert the chaperonin into a protected environment that promotes productive folding and limits aggregation. GroES binding to GroEL is ATP-dependent and creates the cis folding chamber; encapsulation buries hydrophobic surfaces and allows substrate folding before release (wagner2024visualizingchaperoninfunction pages 1-2, gardner2023structuralbasisof pages 1-2). The GroEL/GroES cavity can accommodate many proteins up to ~60 kDa, with most E. coli GroEL substrates concentrated around 20-40 kDa and sharply declining above ~50 kDa (gardner2023structuralbasisof pages 1-2, taguchi2023invivoclient pages 1-2). Wagner et al., 2024, https://doi.org/10.1038/s41586-024-07843-w (2024) (wagner2024visualizingchaperoninfunction pages 1-2); Gardner et al., 2023, https://doi.org/10.1073/pnas.2308933120 (2023) (gardner2023structuralbasisof pages 1-2); Taguchi & Koike-Takeshita, 2023, https://doi.org/10.3389/fmolb.2023.1091677 (2023) (taguchi2023invivoclient pages 1-2)
Biological process GroES participates in bacterial proteostasis and the heat-shock/stress response by assisting GroEL-mediated folding of proteins produced during normal growth and under stress. In P. putida, the groE system is part of the σ32/RpoH-linked heat-shock network. In P. putida KT strains, GroEL and associated heat-shock proteins are rapidly induced after temperature upshift, and σ32/RpoH governs the heat-shock response with induction peaking within ~5-15 min in proteobacteria (ito2014geneticandphenotypic pages 2-3, ito2014geneticandphenotypic pages 6-8). Under elevated-pressure stress in KT2440, groES and groEL are upregulated together with rpoH and other heat-shock genes, consistent with a proteostasis response (follonier2013newinsightson pages 5-6). Ito et al., 2014, https://doi.org/10.1002/mbo3.217 (2014) (ito2014geneticandphenotypic pages 2-3, ito2014geneticandphenotypic pages 6-8); Follonier et al., 2013, https://doi.org/10.1186/1475-2859-12-30 (2013) (follonier2013newinsightson pages 5-6)
Cellular localization GroES functions in the cytosol, where it transiently binds the cytosolic GroEL double-ring complex to form enclosed folding chambers for soluble protein substrates. No evidence in the provided context suggests secretion, membrane localization, or extracellular activity. GroEL/GroES is described as a cytosolic folding machine that encloses substrate proteins in central chambers; in situ cryo-ET visualized these assemblies directly inside bacterial cells (wagner2024visualizingchaperoninfunction pages 1-2). The functional readout is folding and release of encapsulated substrate back into the cytosol (wagner2024visualizingchaperoninfunction pages 1-2, wagner2024visualizingchaperoninfunction pages 3-4). Wagner et al., 2024, https://doi.org/10.1038/s41586-024-07843-w (2024) (wagner2024visualizingchaperoninfunction pages 1-2, wagner2024visualizingchaperoninfunction pages 3-4)
Operon/genomic context In KT2440, groES is located at PP_1360 adjacent to groEL/PP_1361, strongly supporting a canonical groES-groEL locus. The retrieved evidence supports adjacency, but the precise transcript boundaries of a bicistronic operon were not directly mapped in the provided context. The KT2440 stress-transcriptome table lists consecutive loci PP_1360 (groES) and PP_1361 (groEL), both induced under the same stress conditions (follonier2013newinsightson pages 5-6). Broader Pseudomonas heat-shock literature treats GroEL/GroES as part of the heat-shock regulon (craig2021leveragingpseudomonasstress pages 6-7). Follonier et al., 2013, https://doi.org/10.1186/1475-2859-12-30 (2013) (follonier2013newinsightson pages 5-6); Craig et al., 2021, https://doi.org/10.3389/fmicb.2021.660134 (2021) (craig2021leveragingpseudomonasstress pages 6-7)
Regulation/induction conditions The best organism-specific evidence indicates that groES/groEL is stress inducible in P. putida KT2440 and linked to the heat-shock regulatory network involving σ32/RpoH. Expression rises under elevated pressure and likely also under heat-shock-like conditions, although the supplied KT2442 data quantify groEL rather than groES directly. Under elevated pressure in KT2440, groES/PP_1360 increased +1.61-fold (adjusted P = 2.0E-02), and under pressure + elevated dissolved oxygen it increased +1.77-fold (adjusted P = 8.2E-02); groEL/PP_1361 increased +1.78-fold (adjusted P = 1.0E-02) and +2.19-fold (adjusted P = 6.0E-03), while rpoH/PP_5108 increased +1.49-fold and +1.57-fold, respectively (follonier2013newinsightson pages 5-6). In KT strains, groEL is significantly induced within 10 min after transfer to higher temperatures, even at 33°C, with sustained induction up to 30 min at 40-45°C (ito2014geneticandphenotypic pages 6-8). Follonier et al., 2013, https://doi.org/10.1186/1475-2859-12-30 (2013) (follonier2013newinsightson pages 5-6); Ito et al., 2014, https://doi.org/10.1002/mbo3.217 (2014) (ito2014geneticandphenotypic pages 6-8)
Phenotypes/essentiality (note if not found) Direct P. putida KT2440/KT2442 groES knockout or essentiality data were not found in the provided context, so strain-specific essentiality should be treated as not directly demonstrated here. However, GroEL/GroES is broadly described as an indispensable bacterial chaperone system in many bacteria, supporting strong functional importance by conservation. The supplied P. putida studies did not report a groES null mutant phenotype or direct essentiality test (ito2014geneticandphenotypic pages 2-3, ito2014geneticandphenotypic pages 6-8). More generally, GroEL/GroES is described as the only indispensable chaperone system for bacterial viability in most bacteria, based largely on model-organism evidence (taguchi2023invivoclient pages 1-2). Ito et al., 2014, https://doi.org/10.1002/mbo3.217 (2014) (ito2014geneticandphenotypic pages 2-3, ito2014geneticandphenotypic pages 6-8); Taguchi & Koike-Takeshita, 2023, https://doi.org/10.3389/fmolb.2023.1091677 (2023) (taguchi2023invivoclient pages 1-2)
Recent (2023-2024) advances relevant to GroES/GroEL Recent structural work substantially refined the current model of GroES/GroEL action and is directly relevant to functional annotation of P. putida groES because GroES function is highly conserved. These studies support a dynamic cycle involving asymmetric and symmetric GroEL-GroES complexes, substrate capture on the trans ring, and substrate encapsulation/release through distinct conformational states. A 2023 cryo-EM study showed GroEL-ADP·AlF3-GroES and related states with asymmetric substrate engagement, where 4 GroEL subunits contact a 50.5 kDa Rubisco client while 3 adopt a GroES-accepting conformation; GroES binding roughly doubles chamber volume (gardner2023structuralbasisof pages 1-2). A 2024 in situ cryo-ET study found ~55-60% asymmetric EL-ES1 and ~40-45% symmetric EL-ES2 complexes during typical growth, shifting to ~70% EL-ES1 under heat stress; GroEL/GroES abundance rose ~3-fold, the GroEL:ribosome ratio changed from ~1:23 to ~1:10, and EL-ES1 narrow vs wide trans-ring openings were ~45 Å vs ~65 Å (wagner2024visualizingchaperoninfunction pages 2-3, wagner2024visualizingchaperoninfunction pages 3-4). Gardner et al., 2023, https://doi.org/10.1073/pnas.2308933120 (2023) (gardner2023structuralbasisof pages 1-2); Wagner et al., 2024, https://doi.org/10.1038/s41586-024-07843-w (2024) (wagner2024visualizingchaperoninfunction pages 2-3, wagner2024visualizingchaperoninfunction pages 3-4)
Applications/biotech implementations Although not specific to P. putida PP_1360, GroEL/ES has active biotechnology use as a folding aid for difficult recombinant proteins, which is relevant because it operationalizes the core function of GroES as a co-chaperonin. Current implementations mainly use GroEL/ES co-expression to reduce aggregation and increase soluble product yield in microbial cell factories. Recent examples include improved soluble expression of problematic recombinant proteins by GroEL/ES co-expression, including difficult enzymes and viral proteins (craig2021leveragingpseudomonasstress pages 6-7). More broadly, Pseudomonas stress-response knowledge, including chaperone systems such as GroEL/GroES, is being leveraged for industrial strain robustness and process optimization (craig2021leveragingpseudomonasstress pages 6-7). Craig et al., 2021, https://doi.org/10.3389/fmicb.2021.660134 (2021) (craig2021leveragingpseudomonasstress pages 6-7)

Table: This table summarizes the most relevant functional annotation evidence for Pseudomonas putida KT2440 groES (Q88N56/PP_1360), integrating strain-specific data with recent conserved mechanistic insights on the GroES/GroEL chaperonin system. It is useful for distinguishing direct organism-specific evidence from broader, well-supported inference based on the highly conserved GroES family.

References (URLs and publication dates)

  • Domínguez-Cuevas P, et al. J Biol Chem. 2006-04. “Transcriptional Tradeoff between Metabolic and Stress-response Programs in Pseudomonas putida KT2440 Cells Exposed to Toluene.” https://doi.org/10.1074/jbc.m509848200 (dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8)
  • Follonier S, et al. Microbial Cell Factories. 2013-03. “Reorganization of gene transcription in P. putida KT2440 at elevated pressure.” https://doi.org/10.1186/1475-2859-12-30 (follonier2013newinsightson pages 5-6)
  • Ito F, et al. MicrobiologyOpen. 2014-10. “Genetic and phenotypic characterization of the heat shock response in Pseudomonas putida.” https://doi.org/10.1002/mbo3.217 (ito2014geneticandphenotypic pages 2-3, ito2014geneticandphenotypic pages 6-8)
  • Taguchi H, Koike-Takeshita A. Frontiers in Molecular Biosciences. 2023-02. “In vivo client proteins of the chaperonin GroEL–GroES …” https://doi.org/10.3389/fmolb.2023.1091677 (taguchi2023invivoclient pages 1-2)
  • Gardner S, et al. PNAS. 2023-12. “Structural basis of substrate progression through the bacterial chaperonin cycle.” https://doi.org/10.1073/pnas.2308933120 (gardner2023structuralbasisof pages 1-2)
  • Wagner J, et al. Nature. 2024-08. “Visualizing chaperonin function in situ by cryo-electron tomography.” https://doi.org/10.1038/s41586-024-07843-w (wagner2024visualizingchaperoninfunction pages 2-3, wagner2024visualizingchaperoninfunction pages 1-2)
  • Kim J, et al. FEMS Microbiology Letters. 2013-06. “Indole toxicity involves the inhibition of ATP production and protein folding in Pseudomonas putida.” https://doi.org/10.1111/1574-6968.12135 (kim2013indoletoxicityinvolves pages 8-9)
  • Wu T, et al. Int J Biol Macromol. 2024-11. “Boosting extracellular FastPETase production in E. coli …” https://doi.org/10.1016/j.ijbiomac.2024.137857 (wu2024boostingextracellularfastpetase pages 1-5)
  • Merkuleva IA, et al. BioTech. 2024-12. “Combined co-expression of GroEL/ES and Trigger Factor …” https://doi.org/10.3390/biotech13040057 (merkuleva2024theeffectsof pages 8-11)

References

  1. (follonier2013newinsightson pages 5-6): Stéphanie Follonier, Isabel F Escapa, Pilar M Fonseca, Bernhard Henes, Sven Panke, Manfred Zinn, and María Auxiliadora Prieto. New insights on the reorganization of gene transcription in pseudomonas putida kt2440 at elevated pressure. Microbial Cell Factories, 12:30-30, Mar 2013. URL: https://doi.org/10.1186/1475-2859-12-30, doi:10.1186/1475-2859-12-30. This article has 46 citations and is from a peer-reviewed journal.

  2. (wagner2024visualizingchaperoninfunction pages 1-2): Jonathan Wagner, Alonso I. Carvajal, Andreas Bracher, Florian Beck, William Wan, Stefan Bohn, Roman Körner, Wolfgang Baumeister, Ruben Fernandez-Busnadiego, and F. Ulrich Hartl. Visualizing chaperonin function in situ by cryo-electron tomography. Nature, 633:459-464, Aug 2024. URL: https://doi.org/10.1038/s41586-024-07843-w, doi:10.1038/s41586-024-07843-w. This article has 32 citations and is from a highest quality peer-reviewed journal.

  3. (gardner2023structuralbasisof pages 1-2): Scott Gardner, Michele C. Darrow, Natalya Lukoyanova, Konstantinos Thalassinos, and Helen R. Saibil. Structural basis of substrate progression through the bacterial chaperonin cycle. Proceedings of the National Academy of Sciences of the United States of America, Dec 2023. URL: https://doi.org/10.1073/pnas.2308933120, doi:10.1073/pnas.2308933120. This article has 15 citations and is from a highest quality peer-reviewed journal.

  4. (taguchi2023invivoclient pages 1-2): Hideki Taguchi and Ayumi Koike-Takeshita. In vivo client proteins of the chaperonin groel-groes provide insight into the role of chaperones in protein evolution. Frontiers in Molecular Biosciences, Feb 2023. URL: https://doi.org/10.3389/fmolb.2023.1091677, doi:10.3389/fmolb.2023.1091677. This article has 14 citations.

  5. (ito2014geneticandphenotypic pages 2-3): Fumihiro Ito, Takayuki Tamiya, Iwao Ohtsu, Makoto Fujimura, and Fumiyasu Fukumori. Genetic and phenotypic characterization of the heat shock response in pseudomonas putida. MicrobiologyOpen, 3:922-936, Oct 2014. URL: https://doi.org/10.1002/mbo3.217, doi:10.1002/mbo3.217. This article has 28 citations and is from a peer-reviewed journal.

  6. (wagner2024visualizingchaperoninfunction pages 3-4): Jonathan Wagner, Alonso I. Carvajal, Andreas Bracher, Florian Beck, William Wan, Stefan Bohn, Roman Körner, Wolfgang Baumeister, Ruben Fernandez-Busnadiego, and F. Ulrich Hartl. Visualizing chaperonin function in situ by cryo-electron tomography. Nature, 633:459-464, Aug 2024. URL: https://doi.org/10.1038/s41586-024-07843-w, doi:10.1038/s41586-024-07843-w. This article has 32 citations and is from a highest quality peer-reviewed journal.

  7. (dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8): Patricia Domínguez-Cuevas, José-Eduardo González-Pastor, Silvia Marqués, Juan-Luis Ramos, and Víctor de Lorenzo. Transcriptional tradeoff between metabolic and stress-response programs in pseudomonas putida kt2440 cells exposed to toluene*. Journal of Biological Chemistry, 281:11981-11991, Apr 2006. URL: https://doi.org/10.1074/jbc.m509848200, doi:10.1074/jbc.m509848200. This article has 269 citations and is from a domain leading peer-reviewed journal.

  8. (ito2014geneticandphenotypic pages 6-8): Fumihiro Ito, Takayuki Tamiya, Iwao Ohtsu, Makoto Fujimura, and Fumiyasu Fukumori. Genetic and phenotypic characterization of the heat shock response in pseudomonas putida. MicrobiologyOpen, 3:922-936, Oct 2014. URL: https://doi.org/10.1002/mbo3.217, doi:10.1002/mbo3.217. This article has 28 citations and is from a peer-reviewed journal.

  9. (kim2013indoletoxicityinvolves pages 8-9): Jisun Kim, Hyerim Hong, Aram Heo, and Woojun Park. Indole toxicity involves the inhibition of adenosine triphosphate production and protein folding in pseudomonas putida. FEMS microbiology letters, 343 1:89-99, Jun 2013. URL: https://doi.org/10.1111/1574-6968.12135, doi:10.1111/1574-6968.12135. This article has 72 citations and is from a peer-reviewed journal.

  10. (wagner2024visualizingchaperoninfunction pages 2-3): Jonathan Wagner, Alonso I. Carvajal, Andreas Bracher, Florian Beck, William Wan, Stefan Bohn, Roman Körner, Wolfgang Baumeister, Ruben Fernandez-Busnadiego, and F. Ulrich Hartl. Visualizing chaperonin function in situ by cryo-electron tomography. Nature, 633:459-464, Aug 2024. URL: https://doi.org/10.1038/s41586-024-07843-w, doi:10.1038/s41586-024-07843-w. This article has 32 citations and is from a highest quality peer-reviewed journal.

  11. (taguchi2023invivoclient pages 6-6): Hideki Taguchi and Ayumi Koike-Takeshita. In vivo client proteins of the chaperonin groel-groes provide insight into the role of chaperones in protein evolution. Frontiers in Molecular Biosciences, Feb 2023. URL: https://doi.org/10.3389/fmolb.2023.1091677, doi:10.3389/fmolb.2023.1091677. This article has 14 citations.

  12. (wu2024boostingextracellularfastpetase pages 1-5): Ting Wu, Huashan Sun, Wenyao Wang, Bin Xie, Zhengjie Wang, Jianqi Lu, Anming Xu, W. Dong, Zhou Jie, and Min Jiang. Boosting extracellular fastpetase production in e. coli: a combined approach of cognate chaperones co-expression and vesicle nucleating peptide tag fusion. International journal of biological macromolecules, pages 137857, Nov 2024. URL: https://doi.org/10.1016/j.ijbiomac.2024.137857, doi:10.1016/j.ijbiomac.2024.137857. This article has 10 citations and is from a peer-reviewed journal.

  13. (merkuleva2024theeffectsof pages 8-11): Iuliia A. Merkuleva, Vladimir N. Nikitin, Tatyana D. Belaya, Egor. A. Mustaev, and Dmitriy N. Shcherbakov. The effects of the combined co-expression of groel/es and trigger factor chaperones on orthopoxvirus phospholipase f13 production in e. coli. BioTech, 13:57, Dec 2024. URL: https://doi.org/10.3390/biotech13040057, doi:10.3390/biotech13040057. This article has 4 citations.

  14. (craig2021leveragingpseudomonasstress pages 6-7): Kelly Craig, Brant R. Johnson, and Amy Grunden. Leveraging pseudomonas stress response mechanisms for industrial applications. Frontiers in Microbiology, May 2021. URL: https://doi.org/10.3389/fmicb.2021.660134, doi:10.3389/fmicb.2021.660134. This article has 67 citations and is from a peer-reviewed journal.

Artifacts

Citations

  1. follonier2013newinsightson pages 5-6
  2. ito2014geneticandphenotypic pages 2-3
  3. dominguezcuevas2006transcriptionaltradeoffbetween pages 7-8
  4. ito2014geneticandphenotypic pages 6-8
  5. kim2013indoletoxicityinvolves pages 8-9
  6. gardner2023structuralbasisof pages 1-2
  7. wu2024boostingextracellularfastpetase pages 1-5
  8. merkuleva2024theeffectsof pages 8-11
  9. wagner2024visualizingchaperoninfunction pages 1-2
  10. taguchi2023invivoclient pages 1-2
  11. craig2021leveragingpseudomonasstress pages 6-7
  12. wagner2024visualizingchaperoninfunction pages 3-4
  13. wagner2024visualizingchaperoninfunction pages 2-3
  14. taguchi2023invivoclient pages 6-6
  15. https://doi.org/10.1186/1475-2859-12-30
  16. https://doi.org/10.1038/s41586-024-07843-w
  17. https://doi.org/10.1073/pnas.2308933120
  18. https://doi.org/10.3389/fmolb.2023.1091677
  19. https://doi.org/10.1002/mbo3.217
  20. https://doi.org/10.3389/fmicb.2021.660134
  21. https://doi.org/10.1074/jbc.m509848200
  22. https://doi.org/10.1111/1574-6968.12135
  23. https://doi.org/10.1016/j.ijbiomac.2024.137857
  24. https://doi.org/10.3390/biotech13040057
  25. https://doi.org/10.1186/1475-2859-12-30,
  26. https://doi.org/10.1038/s41586-024-07843-w,
  27. https://doi.org/10.1073/pnas.2308933120,
  28. https://doi.org/10.3389/fmolb.2023.1091677,
  29. https://doi.org/10.1002/mbo3.217,
  30. https://doi.org/10.1074/jbc.m509848200,
  31. https://doi.org/10.1111/1574-6968.12135,
  32. https://doi.org/10.1016/j.ijbiomac.2024.137857,
  33. https://doi.org/10.3390/biotech13040057,
  34. https://doi.org/10.3389/fmicb.2021.660134,

📄 View Raw YAML

id: Q88N56
gene_symbol: groES
product_type: PROTEIN
status: COMPLETE
taxon:
  id: NCBITaxon:160488
  label: Pseudomonas putida (strain ATCC 47054 / DSM 6125 / CFBP 8728 / NCIMB 11950 / KT2440)
description: GroES (Cpn10/Hsp10, ~10 kDa) is the bacterial co-chaperonin partner of the GroEL chaperonin. It assembles as a heptameric, dome-shaped ring that binds in an ATP-dependent manner to the apical surface of a GroEL ring, capping the central cavity to form an enclosed nano-cage. Encapsulation of non-native substrate proteins in this chamber provides a folding-permissive environment that promotes productive folding and prevents aggregation, with cyclic GroES binding and release driven by the GroEL ATPase. GroES acts in the cytoplasm and is a constitutive component of the cellular proteostasis machinery; in Pseudomonas putida the groES-groEL operon is part of the sigma-32 (RpoH)-controlled heat-shock regulon and is induced under thermal, solvent, pressure and other proteotoxic stresses. The GroEL/GroES system is essential for viability in most bacteria.
existing_annotations:
- term:
    id: GO:0005524
    label: ATP binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000002
  qualifier: enables
  review:
    summary: ATP binding within the GroEL/GroES chaperonin system is a property of GroEL, not of the GroES co-chaperonin. GroES itself has no nucleotide-binding site; its binding to GroEL is triggered by ATP binding to GroEL.
    action: REMOVE
    reason: This InterPro-based IEA annotation conflates the ATP-dependent GroEL/GroES cycle with intrinsic ATP binding by GroES. GroES does not bind ATP; ATP binding is performed by the GroEL subunit. The annotation is an over-propagation from a family-level signature and is not appropriate for the co-chaperonin.
- term:
    id: GO:0005737
    label: cytoplasm
  evidence_type: IEA
  original_reference_id: GO_REF:0000120
  qualifier: located_in
  review:
    summary: GroES is a soluble cytoplasmic protein that binds cytoplasmic GroEL to form folding chambers. UniProt subcellular location and the conserved biology of the GroEL/GroES system support cytoplasmic localization.
    action: ACCEPT
- term:
    id: GO:0006457
    label: protein folding
  evidence_type: IEA
  original_reference_id: GO_REF:0000120
  qualifier: involved_in
  review:
    summary: Assisting protein folding is the central biological role of GroES, which together with GroEL encapsulates non-native substrates in a folding chamber. This is the core process annotation for the gene. In P. putida KT2440 the groES (PP_1360)-groEL (PP_1361) operon is induced under heat, pressure and aromatic-solvent stress as part of the sigma-32/RpoH proteostasis regulon (see deep research).
    action: ACCEPT
    supported_by:
    - reference_id: file:PSEPK/groES/groES-deep-research-falcon.md
      supporting_text: GroES participates in bacterial proteostasis and the heat-shock/stress response by assisting GroEL-mediated folding; in KT2440 groES/PP_1360 is induced together with groEL and rpoH under pressure and aromatic-solvent stress.
- term:
    id: GO:0044183
    label: protein folding chaperone
  evidence_type: IEA
  original_reference_id: GO_REF:0000002
  qualifier: enables
  review:
    summary: GroES acts as a co-chaperonin that, in cooperation with GroEL, mediates protein folding. This molecular-function term captures the chaperone activity and is a core function annotation.
    action: ACCEPT
- term:
    id: GO:0046872
    label: metal ion binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000118
  qualifier: enables
  review:
    summary: GroES has no established metal-ion-binding function. The co-chaperonin is a small beta-barrel protein whose function is to cap GroEL; metal binding is not part of its mechanism and is not described in UniProt or the structural literature for GroES.
    action: REMOVE
    reason: This is a TreeGrafter/PANTHER tree-based over-annotation without support in the experimental or structural literature for GroES family proteins. Metal ion binding is not a known molecular function of the co-chaperonin.
- term:
    id: GO:0051087
    label: protein-folding chaperone binding
  evidence_type: IEA
  original_reference_id: GO_REF:0000118
  qualifier: enables
  review:
    summary: GroES binds directly to the GroEL chaperonin, its obligate functional partner, capping the GroEL ring to form the folding chamber. Binding to the GroEL chaperonin is well supported and central to GroES function.
    action: ACCEPT
core_functions:
- description: Co-chaperonin that binds GroEL to form an enclosed nano-cage promoting productive folding of non-native proteins in the cytoplasm
  supported_by:
  - reference_id: PMID:39169181
    supporting_text: GroES binds GroEL to form closed folding chambers that allow non-native proteins to fold while protected from aggregation; in situ cryo-ET visualizes GroEL-GroES complexes operating intracellularly.
    full_text_unavailable: true
  molecular_function:
    id: GO:0044183
    label: protein folding chaperone
  directly_involved_in:
  - id: GO:0006457
    label: protein folding
  locations:
  - id: GO:0005737
    label: cytoplasm
- description: Binds the GroEL chaperonin in an ATP-dependent manner, capping the GroEL ring aperture
  supported_by:
  - reference_id: PMID:38064510
    supporting_text: GroES binding to GroEL is ATP-dependent and roughly doubles the chamber volume to create the encapsulated folding environment.
    full_text_unavailable: true
  molecular_function:
    id: GO:0051087
    label: protein-folding chaperone binding
references:
- id: file:PSEPK/groES/groES-deep-research-falcon.md
  title: Deep research report for groES (Q88N56 / PP_1360) in Pseudomonas putida KT2440
  findings:
  - statement: In KT2440, groES (PP_1360) lies immediately upstream of groEL (PP_1361) and both are induced together with rpoH under elevated pressure and aromatic-solvent stress, consistent with membership in the sigma-32/RpoH heat-shock regulon.
    reference_section_type: RESULTS
- id: GO_REF:0000002
  title: Gene Ontology annotation through association of InterPro records with GO terms
  findings: []
- id: GO_REF:0000118
  title: TreeGrafter-generated GO annotations
  findings: []
- id: GO_REF:0000120
  title: Combined Automated Annotation using Multiple IEA Methods
  findings: []
- id: PMID:39169181
  title: Visualizing chaperonin function in situ by cryo-electron tomography
  findings:
  - statement: GroEL/GroES forms folding chambers operating in the cytoplasm; both asymmetric (GroEL-GroES1) and symmetric (GroEL-GroES2) complexes are abundant and shift toward asymmetric under heat stress.
    reference_section_type: RESULTS
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: PubMed-verified (Wagner et al., Nature 2024, PMID:39169181); supports cytoplasmic localization and GroEL-GroES complex function.
- id: PMID:38064510
  title: Structural basis of substrate progression through the bacterial chaperonin cycle
  findings:
  - statement: GroES binding to GroEL is ATP-dependent and approximately doubles chamber volume to create an encapsulated folding environment.
    reference_section_type: RESULTS
  reference_review:
    relevance: HIGH
    correctness: VERIFIED
    review_notes: Original YAML cited PMID:38092042 for this Gardner et al. 2023 PNAS paper (DOI 10.1073/pnas.2308933120), but that PMID resolves to an unrelated AIDS immunology article. Corrected to PMID:38064510, which PubMed confirms is "Structural basis of substrate progression through the bacterial chaperonin cycle" (Gardner et al., PNAS 2023); supports ATP-dependent GroES-GroEL binding and chamber formation.