Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems

Abstract Azotobacter vinelandii, a strict aerobic, nitrogen fixing bacterium in the Pseudomonadaceae family, exhibits a preferential use of acetate over glucose as a carbon source. In this study, we show that GluP (Avin04150), annotated as an H+-coupled glucose-galactose symporter, is the glucose tr...

Full description

Bibliographic Details
Main Authors: Elva Quiroz-Rocha, Renata Moreno, Armando Hernández-Ortíz, Juan Carlos Fragoso-Jiménez, Luis Felipe Muriel-Millán, Josefina Guzmán, Guadalupe Espín, Fernando Rojo, Cinthia Núñez
Format: Article
Language:English
Published: Nature Publishing Group 2017-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-00980-5
id doaj-2b504a2754e644e2905d941e1b063a43
record_format Article
spelling doaj-2b504a2754e644e2905d941e1b063a432020-12-08T00:56:45ZengNature Publishing GroupScientific Reports2045-23222017-04-017111510.1038/s41598-017-00980-5Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systemsElva Quiroz-Rocha0Renata Moreno1Armando Hernández-Ortíz2Juan Carlos Fragoso-Jiménez3Luis Felipe Muriel-Millán4Josefina Guzmán5Guadalupe Espín6Fernando Rojo7Cinthia Núñez8Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CSIC, Darwin 3, CantoblancoDepartamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Ingeniería Celular y Biocatálisis, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoDepartamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CSIC, Darwin 3, CantoblancoDepartamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de MéxicoAbstract Azotobacter vinelandii, a strict aerobic, nitrogen fixing bacterium in the Pseudomonadaceae family, exhibits a preferential use of acetate over glucose as a carbon source. In this study, we show that GluP (Avin04150), annotated as an H+-coupled glucose-galactose symporter, is the glucose transporter in A. vinelandii. This protein, which is widely distributed in bacteria and archaea, is uncommon in Pseudomonas species. We found that expression of gluP was under catabolite repression control thorugh the CbrA/CbrB and Crc/Hfq regulatory systems, which were functionally conserved between A. vinelandii and Pseudomonas species. While the histidine kinase CbrA was essential for glucose utilization, over-expression of the Crc protein arrested cell growth when glucose was the sole carbon source. Crc and Hfq proteins from either A. vinelandii or P. putida could form a stable complex with an RNA A-rich Hfq-binding motif present in the leader region of gluP mRNA. Moreover, in P. putida, the gluP A-rich Hfq-binding motif was functional and promoted translational inhibition of a lacZ reporter gene. The fact that gluP is not widely distributed in the Pseudomonas genus but is under control of the CbrA/CbrB and Crc/Hfq systems demonstrates the relevance of these systems in regulating metabolism in the Pseudomonadaceae family.https://doi.org/10.1038/s41598-017-00980-5
collection DOAJ
language English
format Article
sources DOAJ
author Elva Quiroz-Rocha
Renata Moreno
Armando Hernández-Ortíz
Juan Carlos Fragoso-Jiménez
Luis Felipe Muriel-Millán
Josefina Guzmán
Guadalupe Espín
Fernando Rojo
Cinthia Núñez
spellingShingle Elva Quiroz-Rocha
Renata Moreno
Armando Hernández-Ortíz
Juan Carlos Fragoso-Jiménez
Luis Felipe Muriel-Millán
Josefina Guzmán
Guadalupe Espín
Fernando Rojo
Cinthia Núñez
Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
Scientific Reports
author_facet Elva Quiroz-Rocha
Renata Moreno
Armando Hernández-Ortíz
Juan Carlos Fragoso-Jiménez
Luis Felipe Muriel-Millán
Josefina Guzmán
Guadalupe Espín
Fernando Rojo
Cinthia Núñez
author_sort Elva Quiroz-Rocha
title Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
title_short Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
title_full Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
title_fullStr Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
title_full_unstemmed Glucose uptake in Azotobacter vinelandii occurs through a GluP transporter that is under the control of the CbrA/CbrB and Hfq-Crc systems
title_sort glucose uptake in azotobacter vinelandii occurs through a glup transporter that is under the control of the cbra/cbrb and hfq-crc systems
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-04-01
description Abstract Azotobacter vinelandii, a strict aerobic, nitrogen fixing bacterium in the Pseudomonadaceae family, exhibits a preferential use of acetate over glucose as a carbon source. In this study, we show that GluP (Avin04150), annotated as an H+-coupled glucose-galactose symporter, is the glucose transporter in A. vinelandii. This protein, which is widely distributed in bacteria and archaea, is uncommon in Pseudomonas species. We found that expression of gluP was under catabolite repression control thorugh the CbrA/CbrB and Crc/Hfq regulatory systems, which were functionally conserved between A. vinelandii and Pseudomonas species. While the histidine kinase CbrA was essential for glucose utilization, over-expression of the Crc protein arrested cell growth when glucose was the sole carbon source. Crc and Hfq proteins from either A. vinelandii or P. putida could form a stable complex with an RNA A-rich Hfq-binding motif present in the leader region of gluP mRNA. Moreover, in P. putida, the gluP A-rich Hfq-binding motif was functional and promoted translational inhibition of a lacZ reporter gene. The fact that gluP is not widely distributed in the Pseudomonas genus but is under control of the CbrA/CbrB and Crc/Hfq systems demonstrates the relevance of these systems in regulating metabolism in the Pseudomonadaceae family.
url https://doi.org/10.1038/s41598-017-00980-5
work_keys_str_mv AT elvaquirozrocha glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT renatamoreno glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT armandohernandezortiz glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT juancarlosfragosojimenez glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT luisfelipemurielmillan glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT josefinaguzman glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT guadalupeespin glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT fernandorojo glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
AT cinthianunez glucoseuptakeinazotobactervinelandiioccursthroughagluptransporterthatisunderthecontrolofthecbracbrbandhfqcrcsystems
_version_ 1724395538017681408