Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae

ABSTRACT Mycoplasma pneumoniae (Mpn, class Mollicutes) is both an important human pathogen and a model organism. We performed a proteome-wide investigation of intrinsically disordered regions (IDRs) in Mpn. Compared to other bacteria, a considerable fraction of the Mpn proteome (17%) is embedded in...

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Main Authors: Uberto Pozzoli, Diego Forni, Federica Arrigoni, Alessandra Mozzi, Rachele Cagliani, Luca De Gioia, Manuela Sironi
Format: Article
Language:English
Published: American Society for Microbiology 2025-08-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.00968-25
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author Uberto Pozzoli
Diego Forni
Federica Arrigoni
Alessandra Mozzi
Rachele Cagliani
Luca De Gioia
Manuela Sironi
author_facet Uberto Pozzoli
Diego Forni
Federica Arrigoni
Alessandra Mozzi
Rachele Cagliani
Luca De Gioia
Manuela Sironi
author_sort Uberto Pozzoli
collection DOAJ
description ABSTRACT Mycoplasma pneumoniae (Mpn, class Mollicutes) is both an important human pathogen and a model organism. We performed a proteome-wide investigation of intrinsically disordered regions (IDRs) in Mpn. Compared to other bacteria, a considerable fraction of the Mpn proteome (17%) is embedded in IDRs, which are abundant in membrane, non-essential proteins, as well as in proteins that mediate cytoadherence and virulence. Notably, proteins that form the attachment organelle, a specialized structure, are particularly rich in IDRs. Likewise, analysis of protein architectures indicated that some Mollicute-specific domains are preferentially associated with IDRs. Perusal of proteome-wide data also revealed that, as in eukaryotes, structural disorder associates with higher protein degradation rates and that Mpn IDRs are preferential targets of phosphorylation. When we investigated the ensemble features for Mpn IDRs, we used two predictors and benchmarked the results using coarse-grained simulations. We found that ensemble properties are mediated by similar sequence features as in eukaryotes, so that compact IDRs tend to have high residue stickiness, high hydropathy decoration, and few charged residues. We also found that IDRs in attachment organelle proteins are particularly extended and display high conformational entropy. We suggest that these features are exploited for motility through the generation of an entropic force. In summary, our results suggest that structural disorder contributes to very specialized functions in Mpn. Our data also highlight the functional relevance of IDRs, as the minimal proteome of this model organism displays a considerable level of structural disorder.IMPORTANCEWe performed a proteome-wide investigation of intrinsically disordered regions (IDRs) in Mycoplasma pneumoniae (Mpn, class Mollicutes). A considerable fraction of the Mpn proteome (17%) is embedded in IDRs, which tend to be associated with Mollicute-specific domains and are abundant in membrane, non-essential proteins, as well as in proteins that mediate cytoadherence and virulence. As in eukaryotes, structural disorder associates with higher protein degradation rates, and Mpn IDRs are preferential targets of phosphorylation. The ensemble properties of Mpn IDRs are mediated by similar sequence features as in eukaryotes, and IDRs in attachment organelle proteins display high conformational entropy. We suggest that this feature is exploited for motility through the generation of an entropic force. In summary, we show that structural disorder contributes to very specialized functions in Mpn. Our data highlight the functional relevance of IDRs, as the minimal proteome of this model organism displays a considerable level of structural disorder.
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spelling doaj-art-e23d798b69bf4f1eb74aa972464001cf2025-08-20T02:56:39ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-08-0113810.1128/spectrum.00968-25Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniaeUberto Pozzoli0Diego Forni1Federica Arrigoni2Alessandra Mozzi3Rachele Cagliani4Luca De Gioia5Manuela Sironi6Scientific Institute IRCCS E. MEDEA, Computational Biology Unit, Bosisio Parini, ItalyScientific Institute IRCCS E. MEDEA, Computational Biology Unit, Bosisio Parini, ItalyDepartment of Biotechnology and Biosciences, University of Milan-Bicocca, Milan, ItalyScientific Institute IRCCS E. MEDEA, Computational Biology Unit, Bosisio Parini, ItalyScientific Institute IRCCS E. MEDEA, Computational Biology Unit, Bosisio Parini, ItalyDepartment of Biotechnology and Biosciences, University of Milan-Bicocca, Milan, ItalySchool of Medicine and Surgery, University of Milano-Bicocca, Monza, ItalyABSTRACT Mycoplasma pneumoniae (Mpn, class Mollicutes) is both an important human pathogen and a model organism. We performed a proteome-wide investigation of intrinsically disordered regions (IDRs) in Mpn. Compared to other bacteria, a considerable fraction of the Mpn proteome (17%) is embedded in IDRs, which are abundant in membrane, non-essential proteins, as well as in proteins that mediate cytoadherence and virulence. Notably, proteins that form the attachment organelle, a specialized structure, are particularly rich in IDRs. Likewise, analysis of protein architectures indicated that some Mollicute-specific domains are preferentially associated with IDRs. Perusal of proteome-wide data also revealed that, as in eukaryotes, structural disorder associates with higher protein degradation rates and that Mpn IDRs are preferential targets of phosphorylation. When we investigated the ensemble features for Mpn IDRs, we used two predictors and benchmarked the results using coarse-grained simulations. We found that ensemble properties are mediated by similar sequence features as in eukaryotes, so that compact IDRs tend to have high residue stickiness, high hydropathy decoration, and few charged residues. We also found that IDRs in attachment organelle proteins are particularly extended and display high conformational entropy. We suggest that these features are exploited for motility through the generation of an entropic force. In summary, our results suggest that structural disorder contributes to very specialized functions in Mpn. Our data also highlight the functional relevance of IDRs, as the minimal proteome of this model organism displays a considerable level of structural disorder.IMPORTANCEWe performed a proteome-wide investigation of intrinsically disordered regions (IDRs) in Mycoplasma pneumoniae (Mpn, class Mollicutes). A considerable fraction of the Mpn proteome (17%) is embedded in IDRs, which tend to be associated with Mollicute-specific domains and are abundant in membrane, non-essential proteins, as well as in proteins that mediate cytoadherence and virulence. As in eukaryotes, structural disorder associates with higher protein degradation rates, and Mpn IDRs are preferential targets of phosphorylation. The ensemble properties of Mpn IDRs are mediated by similar sequence features as in eukaryotes, and IDRs in attachment organelle proteins display high conformational entropy. We suggest that this feature is exploited for motility through the generation of an entropic force. In summary, we show that structural disorder contributes to very specialized functions in Mpn. Our data highlight the functional relevance of IDRs, as the minimal proteome of this model organism displays a considerable level of structural disorder.https://journals.asm.org/doi/10.1128/spectrum.00968-25Mycoplasma pneumoniaeintrinsically disordered regionAlphaFoldstructural disorderensemble features
spellingShingle Uberto Pozzoli
Diego Forni
Federica Arrigoni
Alessandra Mozzi
Rachele Cagliani
Luca De Gioia
Manuela Sironi
Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
Microbiology Spectrum
Mycoplasma pneumoniae
intrinsically disordered region
AlphaFold
structural disorder
ensemble features
title Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
title_full Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
title_fullStr Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
title_full_unstemmed Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
title_short Systematic analysis of structural disorder in the minimal proteome of Mycoplasma pneumoniae
title_sort systematic analysis of structural disorder in the minimal proteome of mycoplasma pneumoniae
topic Mycoplasma pneumoniae
intrinsically disordered region
AlphaFold
structural disorder
ensemble features
url https://journals.asm.org/doi/10.1128/spectrum.00968-25
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