Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes

Abstract Background Crl, identified for curli production, is a small transcription factor that stimulates the association of the σS factor (RpoS) with the RNA polymerase core through direct and specific interactions, increasing the transcription rate of genes during the transition from exponential t...

Full description

Bibliographic Details
Main Authors: A. Santos-Zavaleta, E. Pérez-Rueda, M. Sánchez-Pérez, D. A. Velázquez-Ramírez, J. Collado-Vides
Format: Article
Language:English
Published: BMC 2019-04-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5619-z
_version_ 1819068703532122112
author A. Santos-Zavaleta
E. Pérez-Rueda
M. Sánchez-Pérez
D. A. Velázquez-Ramírez
J. Collado-Vides
author_facet A. Santos-Zavaleta
E. Pérez-Rueda
M. Sánchez-Pérez
D. A. Velázquez-Ramírez
J. Collado-Vides
author_sort A. Santos-Zavaleta
collection DOAJ
description Abstract Background Crl, identified for curli production, is a small transcription factor that stimulates the association of the σS factor (RpoS) with the RNA polymerase core through direct and specific interactions, increasing the transcription rate of genes during the transition from exponential to stationary phase at low temperatures, using indole as an effector molecule. The lack of a comprehensive collection of information on the Crl regulon makes it difficult to identify a dominant function of Crl and to generate any hypotheses concerning its taxonomical distribution in archaeal and bacterial organisms. Results In this work, based on a systematic literature review, we identified the first comprehensive dataset of 86 genes under the control of Crl in the bacterium Escherichia coli K-12; those genes correspond to 40% of the σS regulon in this bacterium. Based on an analysis of orthologs in 18 archaeal and 69 bacterial taxonomical divisions and using E. coli K-12 as a framework, we suggest three main events that resulted in this regulon’s actual form: (i) in a first step, rpoS, a gene widely distributed in bacteria and archaea cellular domains, was recruited to regulate genes involved in ancient metabolic processes, such as those associated with glycolysis and the tricarboxylic acid cycle; (ii) in a second step, the regulon recruited those genes involved in metabolic processes, which are mainly taxonomically constrained to Proteobacteria, with some secondary losses, such as those genes involved in responses to stress or starvation and cell adhesion, among others; and (iii) in a posterior step, Crl might have been recruited in Enterobacteriaceae; because its taxonomical pattern constrained to this bacterial order, however further analysis are necessary. Conclusions Therefore, we suggest that the regulon Crl is highly flexible for phenotypic adaptation, probably as consequence of the diverse growth environments associated with all organisms in which members of this regulatory network are present.
first_indexed 2024-12-21T16:38:22Z
format Article
id doaj.art-be2ac2c21c81474b8d216a6c3d03da04
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-12-21T16:38:22Z
publishDate 2019-04-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-be2ac2c21c81474b8d216a6c3d03da042022-12-21T18:57:10ZengBMCBMC Genomics1471-21642019-04-0120111310.1186/s12864-019-5619-zTracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomesA. Santos-Zavaleta0E. Pérez-Rueda1M. Sánchez-Pérez2D. A. Velázquez-Ramírez3J. Collado-Vides4Programa de Genómica Computacional, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de MéxicoInstituto de Investigaciones en Matemáticas Aplicadas y en Sistemas, Sede Mérida, Universidad Nacional Autónoma de México, Unidad Académica de Ciencias y TecnologíaPrograma de Genómica Computacional, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de MéxicoPrograma de Genómica Computacional, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de MéxicoPrograma de Genómica Computacional, Centro de Ciencias Genómicas, Universidad Nacional Autónoma de MéxicoAbstract Background Crl, identified for curli production, is a small transcription factor that stimulates the association of the σS factor (RpoS) with the RNA polymerase core through direct and specific interactions, increasing the transcription rate of genes during the transition from exponential to stationary phase at low temperatures, using indole as an effector molecule. The lack of a comprehensive collection of information on the Crl regulon makes it difficult to identify a dominant function of Crl and to generate any hypotheses concerning its taxonomical distribution in archaeal and bacterial organisms. Results In this work, based on a systematic literature review, we identified the first comprehensive dataset of 86 genes under the control of Crl in the bacterium Escherichia coli K-12; those genes correspond to 40% of the σS regulon in this bacterium. Based on an analysis of orthologs in 18 archaeal and 69 bacterial taxonomical divisions and using E. coli K-12 as a framework, we suggest three main events that resulted in this regulon’s actual form: (i) in a first step, rpoS, a gene widely distributed in bacteria and archaea cellular domains, was recruited to regulate genes involved in ancient metabolic processes, such as those associated with glycolysis and the tricarboxylic acid cycle; (ii) in a second step, the regulon recruited those genes involved in metabolic processes, which are mainly taxonomically constrained to Proteobacteria, with some secondary losses, such as those genes involved in responses to stress or starvation and cell adhesion, among others; and (iii) in a posterior step, Crl might have been recruited in Enterobacteriaceae; because its taxonomical pattern constrained to this bacterial order, however further analysis are necessary. Conclusions Therefore, we suggest that the regulon Crl is highly flexible for phenotypic adaptation, probably as consequence of the diverse growth environments associated with all organisms in which members of this regulatory network are present.http://link.springer.com/article/10.1186/s12864-019-5619-zCrl regulonStress responseTranscription factorsComparative genomicsBacteriaArchaea
spellingShingle A. Santos-Zavaleta
E. Pérez-Rueda
M. Sánchez-Pérez
D. A. Velázquez-Ramírez
J. Collado-Vides
Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
BMC Genomics
Crl regulon
Stress response
Transcription factors
Comparative genomics
Bacteria
Archaea
title Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
title_full Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
title_fullStr Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
title_full_unstemmed Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
title_short Tracing the phylogenetic history of the Crl regulon through the Bacteria and Archaea genomes
title_sort tracing the phylogenetic history of the crl regulon through the bacteria and archaea genomes
topic Crl regulon
Stress response
Transcription factors
Comparative genomics
Bacteria
Archaea
url http://link.springer.com/article/10.1186/s12864-019-5619-z
work_keys_str_mv AT asantoszavaleta tracingthephylogenetichistoryofthecrlregulonthroughthebacteriaandarchaeagenomes
AT eperezrueda tracingthephylogenetichistoryofthecrlregulonthroughthebacteriaandarchaeagenomes
AT msanchezperez tracingthephylogenetichistoryofthecrlregulonthroughthebacteriaandarchaeagenomes
AT davelazquezramirez tracingthephylogenetichistoryofthecrlregulonthroughthebacteriaandarchaeagenomes
AT jcolladovides tracingthephylogenetichistoryofthecrlregulonthroughthebacteriaandarchaeagenomes