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Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor

Streptomyces coelicolor A3(2) is a model microorganism for the study of Streptomycetes, antibiotic production, and secondary metabolism in general. Even though S. coelicolor has an outstanding variety of regulators among bacteria, little effort to globally study its transcription has been made. We m...

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Autores principales: Zorro-Aranda, Andrea, Escorcia-Rodríguez, Juan Miguel, González-Kise, José Kenyi, Freyre-González, Julio Augusto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8857197/
https://www.ncbi.nlm.nih.gov/pubmed/35181703
http://dx.doi.org/10.1038/s41598-022-06658-x
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author Zorro-Aranda, Andrea
Escorcia-Rodríguez, Juan Miguel
González-Kise, José Kenyi
Freyre-González, Julio Augusto
author_facet Zorro-Aranda, Andrea
Escorcia-Rodríguez, Juan Miguel
González-Kise, José Kenyi
Freyre-González, Julio Augusto
author_sort Zorro-Aranda, Andrea
collection PubMed
description Streptomyces coelicolor A3(2) is a model microorganism for the study of Streptomycetes, antibiotic production, and secondary metabolism in general. Even though S. coelicolor has an outstanding variety of regulators among bacteria, little effort to globally study its transcription has been made. We manually curated 29 years of literature and databases to assemble a meta-curated experimentally-validated gene regulatory network (GRN) with 5386 genes and 9707 regulatory interactions (~ 41% of the total expected interactions). This provides the most extensive and up-to-date reconstruction available for the regulatory circuitry of this organism. Only ~ 6% (534/9707) are supported by experiments confirming the binding of the transcription factor to the upstream region of the target gene, the so-called “strong” evidence. While for the remaining interactions there is no confirmation of direct binding. To tackle network incompleteness, we performed network inference using several methods (including two proposed here) for motif identification in DNA sequences and GRN inference from transcriptomics. Further, we contrasted the structural properties and functional architecture of the networks to assess the reliability of the predictions, finding the inference from DNA sequence data to be the most trustworthy approach. Finally, we show two applications of the inferred and the curated networks. The inference allowed us to propose novel transcription factors for the key Streptomyces antibiotic regulatory proteins (SARPs). The curated network allowed us to study the conservation of the system-level components between S. coelicolor and Corynebacterium glutamicum. There we identified the basal machinery as the common signature between the two organisms. The curated networks were deposited in Abasy Atlas (https://abasy.ccg.unam.mx/) while the inferences are available as Supplementary Material.
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spelling pubmed-88571972022-02-22 Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor Zorro-Aranda, Andrea Escorcia-Rodríguez, Juan Miguel González-Kise, José Kenyi Freyre-González, Julio Augusto Sci Rep Article Streptomyces coelicolor A3(2) is a model microorganism for the study of Streptomycetes, antibiotic production, and secondary metabolism in general. Even though S. coelicolor has an outstanding variety of regulators among bacteria, little effort to globally study its transcription has been made. We manually curated 29 years of literature and databases to assemble a meta-curated experimentally-validated gene regulatory network (GRN) with 5386 genes and 9707 regulatory interactions (~ 41% of the total expected interactions). This provides the most extensive and up-to-date reconstruction available for the regulatory circuitry of this organism. Only ~ 6% (534/9707) are supported by experiments confirming the binding of the transcription factor to the upstream region of the target gene, the so-called “strong” evidence. While for the remaining interactions there is no confirmation of direct binding. To tackle network incompleteness, we performed network inference using several methods (including two proposed here) for motif identification in DNA sequences and GRN inference from transcriptomics. Further, we contrasted the structural properties and functional architecture of the networks to assess the reliability of the predictions, finding the inference from DNA sequence data to be the most trustworthy approach. Finally, we show two applications of the inferred and the curated networks. The inference allowed us to propose novel transcription factors for the key Streptomyces antibiotic regulatory proteins (SARPs). The curated network allowed us to study the conservation of the system-level components between S. coelicolor and Corynebacterium glutamicum. There we identified the basal machinery as the common signature between the two organisms. The curated networks were deposited in Abasy Atlas (https://abasy.ccg.unam.mx/) while the inferences are available as Supplementary Material. Nature Publishing Group UK 2022-02-18 /pmc/articles/PMC8857197/ /pubmed/35181703 http://dx.doi.org/10.1038/s41598-022-06658-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Zorro-Aranda, Andrea
Escorcia-Rodríguez, Juan Miguel
González-Kise, José Kenyi
Freyre-González, Julio Augusto
Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title_full Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title_fullStr Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title_full_unstemmed Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title_short Curation, inference, and assessment of a globally reconstructed gene regulatory network for Streptomyces coelicolor
title_sort curation, inference, and assessment of a globally reconstructed gene regulatory network for streptomyces coelicolor
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8857197/
https://www.ncbi.nlm.nih.gov/pubmed/35181703
http://dx.doi.org/10.1038/s41598-022-06658-x
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