A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida

Fructose uptake in the soil bacterium Pseudomonas putida occurs through a canonical phosphoenolpyruvate (PEP)-dependent sugar transport system (PTSFru). The logic of the genetic circuit that rules its functioning is puzzling: the transcription of the fruBKA operon, encoding all the components of PTS...

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Main Authors: Chavarría Vargas, Max, Goñi Moreno, Ángel, de Lorenzo, Víctor, Nikel Mayer, Pablo Iván
Format: Artículo
Language: Inglés
Published: 2018
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Online Access: https://hdl.handle.net/10669/74178
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spelling 741782021-04-12T21:24:00Z A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida Chavarría Vargas, Max Goñi Moreno, Ángel de Lorenzo, Víctor Nikel Mayer, Pablo Iván Cra regulator Metabolic memory PTS sugar transport Pseudomonas putida Glyceraldehyde-3-P dehydrogenase, Nutrient shifts Phosphoenolpyruvate Fructose uptake in the soil bacterium Pseudomonas putida occurs through a canonical phosphoenolpyruvate (PEP)-dependent sugar transport system (PTSFru). The logic of the genetic circuit that rules its functioning is puzzling: the transcription of the fruBKA operon, encoding all the components of PTSFru, can escape the repression exerted by the catabolite repressor/activator protein Cra solely in the presence of intracellular fructose-1-P, an agonist formed only when fructose has been already transported. To study this apparently incongruous regulatory architecture, the changes in the transcriptome brought about by a seamless Δcra deletion in P. putida strain KT2440 were inspected under different culture conditions. The few genes found to be upregulated in the cra mutant unexpectedly included PP_3443, encoding a bona fide glyceraldehyde-3-P dehydrogenase. An in silico model was developed to explore emergent properties that could result from such connections between sugar uptake with Cra and PEP. Simulation of fructose transport revealed that sugar uptake called for an extra supply of PEP (obtained through the activity of PP_3443) that was kept (i.e., memorized) even when the carbohydrate disappeared from the medium. This feature was traced to the action of two sequential inverters that connect the availability of exogenous fructose to intracellular PEP levels via Cra/PP_3443. The loss of such memory caused a much longer lag phase in cells shifted from one growth condition to another. The term “metabolic widget” is proposed to describe a merged biochemical and regulatory patch that tailors a given node of the cell molecular network to suit species-specific physiological needs. Ministry of Economy and Competitiveness/[RTC-2014-1777-3]/MINECO/España Ministry of Economy and Competitiveness/[BIO-2015-66960-C3-2-R]/MINECO/España European Union/[EVOPROG (FP7-ICT-610730)]/UE/ European Union/[ARISYS (ERC-2012-ADG-322797)]/UE/ European Union/[EmPowerPutida (EU-H2020-BIOTEC-2014-2015-6335536]/UE/ UCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias Básicas::Centro de Investigaciones en Productos Naturales (CIPRONA) 2018-03-01T20:30:52Z 2018-03-01T20:30:52Z 2016 artículo científico e00154-16 https://hdl.handle.net/10669/74178 10.1128/mSystems.00154-16 PMC5141268 en_US Atribución 4.0 Internacional http://creativecommons.org/licenses/by/4.0/ application/pdf Systems, Vol. 1, Núm 6, 2016
institution Universidad de Costa Rica
collection Repositorio KERWA
language Inglés
topic Cra regulator
Metabolic memory
PTS sugar transport
Pseudomonas putida
Glyceraldehyde-3-P dehydrogenase,
Nutrient shifts
Phosphoenolpyruvate
spellingShingle Cra regulator
Metabolic memory
PTS sugar transport
Pseudomonas putida
Glyceraldehyde-3-P dehydrogenase,
Nutrient shifts
Phosphoenolpyruvate
Chavarría Vargas, Max
Goñi Moreno, Ángel
de Lorenzo, Víctor
Nikel Mayer, Pablo Iván
A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
description Fructose uptake in the soil bacterium Pseudomonas putida occurs through a canonical phosphoenolpyruvate (PEP)-dependent sugar transport system (PTSFru). The logic of the genetic circuit that rules its functioning is puzzling: the transcription of the fruBKA operon, encoding all the components of PTSFru, can escape the repression exerted by the catabolite repressor/activator protein Cra solely in the presence of intracellular fructose-1-P, an agonist formed only when fructose has been already transported. To study this apparently incongruous regulatory architecture, the changes in the transcriptome brought about by a seamless Δcra deletion in P. putida strain KT2440 were inspected under different culture conditions. The few genes found to be upregulated in the cra mutant unexpectedly included PP_3443, encoding a bona fide glyceraldehyde-3-P dehydrogenase. An in silico model was developed to explore emergent properties that could result from such connections between sugar uptake with Cra and PEP. Simulation of fructose transport revealed that sugar uptake called for an extra supply of PEP (obtained through the activity of PP_3443) that was kept (i.e., memorized) even when the carbohydrate disappeared from the medium. This feature was traced to the action of two sequential inverters that connect the availability of exogenous fructose to intracellular PEP levels via Cra/PP_3443. The loss of such memory caused a much longer lag phase in cells shifted from one growth condition to another. The term “metabolic widget” is proposed to describe a merged biochemical and regulatory patch that tailors a given node of the cell molecular network to suit species-specific physiological needs.
format Artículo
author Chavarría Vargas, Max
Goñi Moreno, Ángel
de Lorenzo, Víctor
Nikel Mayer, Pablo Iván
author_sort Chavarría Vargas, Max
title A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
title_short A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
title_full A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
title_fullStr A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
title_full_unstemmed A Metabolic Widget Adjusts the Phosphoenolpyruvate-Dependent Fructose Influx in Pseudomonas putida
title_sort metabolic widget adjusts the phosphoenolpyruvate-dependent fructose influx in pseudomonas putida
publishDate 2018
url https://hdl.handle.net/10669/74178
_version_ 1769153413161943040
score 11.959122