The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content>
ABSTRACT The PII family comprises a group of widely distributed signal transduction proteins ubiquitous in prokaryotes and in the chloroplasts of plants. PII proteins sense the levels of key metabolites ATP, ADP, and 2-oxoglutarate, which affect the PII protein structure and thereby the ability of P...
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American Society for Microbiology
2020
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oai:doaj.org-article:1bdea420a7694a0881314eb9a00172312021-12-02T19:46:19ZThe Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content>10.1128/mSystems.00817-202379-5077https://doaj.org/article/1bdea420a7694a0881314eb9a00172312020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00817-20https://doaj.org/toc/2379-5077ABSTRACT The PII family comprises a group of widely distributed signal transduction proteins ubiquitous in prokaryotes and in the chloroplasts of plants. PII proteins sense the levels of key metabolites ATP, ADP, and 2-oxoglutarate, which affect the PII protein structure and thereby the ability of PII to interact with a range of target proteins. Here, we performed multiple ligand fishing assays with the PII protein orthologue GlnZ from the plant growth-promoting nitrogen-fixing bacterium Azospirillum brasilense to identify 37 proteins that are likely to be part of the PII protein-protein interaction network. Among the PII targets identified were enzymes related to nitrogen and fatty acid metabolism, signaling, coenzyme synthesis, RNA catabolism, and transcription. Direct binary PII-target complex was confirmed for 15 protein complexes using pulldown assays with recombinant proteins. Untargeted metabolome analysis showed that PII is required for proper homeostasis of important metabolites. Two enzymes involved in c-di-GMP metabolism were among the identified PII targets. A PII-deficient strain showed reduced c-di-GMP levels and altered aerotaxis and flocculation behavior. These data support that PII acts as a major metabolic hub controlling important enzymes and the homeostasis of key metabolites such as c-di-GMP in response to the prevailing nutritional status. IMPORTANCE The PII proteins sense and integrate important metabolic signals which reflect the cellular nutrition and energy status. Such extraordinary ability was capitalized by nature in such a way that the various PII proteins regulate different facets of metabolism by controlling the activity of a range of target proteins by protein-protein interactions. Here, we determined the PII protein interaction network in the plant growth-promoting nitrogen-fixing bacterium Azospirillum brasilense. The interactome data along with metabolome analysis suggest that PII functions as a master metabolic regulator hub. We provide evidence that PII proteins act to regulate c-di-GMP levels in vivo and cell motility and adherence behaviors.Edileusa C. M. GerhardtErick ParizeFernanda GravinaFlávia L. D. PontesAdrian R. S. SantosGillize A. T. AraújoAna C. GoedertAlysson H. UrbanskiMaria B. R. SteffensLeda S. ChubatsuFabio O. PedrosaEmanuel M. SouzaKarl ForchhammerElena GanusovaGladys AlexandreGustavo A. de SouzaLuciano F. HuergoAmerican Society for Microbiologyarticleprotein interactionPII proteinc-di-GMPmotilitymetabolic regulationcell motilityMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
protein interaction PII protein c-di-GMP motility metabolic regulation cell motility Microbiology QR1-502 |
| spellingShingle |
protein interaction PII protein c-di-GMP motility metabolic regulation cell motility Microbiology QR1-502 Edileusa C. M. Gerhardt Erick Parize Fernanda Gravina Flávia L. D. Pontes Adrian R. S. Santos Gillize A. T. Araújo Ana C. Goedert Alysson H. Urbanski Maria B. R. Steffens Leda S. Chubatsu Fabio O. Pedrosa Emanuel M. Souza Karl Forchhammer Elena Ganusova Gladys Alexandre Gustavo A. de Souza Luciano F. Huergo The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| description |
ABSTRACT The PII family comprises a group of widely distributed signal transduction proteins ubiquitous in prokaryotes and in the chloroplasts of plants. PII proteins sense the levels of key metabolites ATP, ADP, and 2-oxoglutarate, which affect the PII protein structure and thereby the ability of PII to interact with a range of target proteins. Here, we performed multiple ligand fishing assays with the PII protein orthologue GlnZ from the plant growth-promoting nitrogen-fixing bacterium Azospirillum brasilense to identify 37 proteins that are likely to be part of the PII protein-protein interaction network. Among the PII targets identified were enzymes related to nitrogen and fatty acid metabolism, signaling, coenzyme synthesis, RNA catabolism, and transcription. Direct binary PII-target complex was confirmed for 15 protein complexes using pulldown assays with recombinant proteins. Untargeted metabolome analysis showed that PII is required for proper homeostasis of important metabolites. Two enzymes involved in c-di-GMP metabolism were among the identified PII targets. A PII-deficient strain showed reduced c-di-GMP levels and altered aerotaxis and flocculation behavior. These data support that PII acts as a major metabolic hub controlling important enzymes and the homeostasis of key metabolites such as c-di-GMP in response to the prevailing nutritional status. IMPORTANCE The PII proteins sense and integrate important metabolic signals which reflect the cellular nutrition and energy status. Such extraordinary ability was capitalized by nature in such a way that the various PII proteins regulate different facets of metabolism by controlling the activity of a range of target proteins by protein-protein interactions. Here, we determined the PII protein interaction network in the plant growth-promoting nitrogen-fixing bacterium Azospirillum brasilense. The interactome data along with metabolome analysis suggest that PII functions as a master metabolic regulator hub. We provide evidence that PII proteins act to regulate c-di-GMP levels in vivo and cell motility and adherence behaviors. |
| format |
article |
| author |
Edileusa C. M. Gerhardt Erick Parize Fernanda Gravina Flávia L. D. Pontes Adrian R. S. Santos Gillize A. T. Araújo Ana C. Goedert Alysson H. Urbanski Maria B. R. Steffens Leda S. Chubatsu Fabio O. Pedrosa Emanuel M. Souza Karl Forchhammer Elena Ganusova Gladys Alexandre Gustavo A. de Souza Luciano F. Huergo |
| author_facet |
Edileusa C. M. Gerhardt Erick Parize Fernanda Gravina Flávia L. D. Pontes Adrian R. S. Santos Gillize A. T. Araújo Ana C. Goedert Alysson H. Urbanski Maria B. R. Steffens Leda S. Chubatsu Fabio O. Pedrosa Emanuel M. Souza Karl Forchhammer Elena Ganusova Gladys Alexandre Gustavo A. de Souza Luciano F. Huergo |
| author_sort |
Edileusa C. M. Gerhardt |
| title |
The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| title_short |
The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| title_full |
The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| title_fullStr |
The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| title_full_unstemmed |
The Protein-Protein Interaction Network Reveals a Novel Role of the Signal Transduction Protein PII in the Control of c-di-GMP Homeostasis in <named-content content-type="genus-species">Azospirillum brasilense</named-content> |
| title_sort |
protein-protein interaction network reveals a novel role of the signal transduction protein pii in the control of c-di-gmp homeostasis in <named-content content-type="genus-species">azospirillum brasilense</named-content> |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/1bdea420a7694a0881314eb9a0017231 |
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