Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440

Autores
Nikel, Pablo Ivan; Chavarría, Max; Martínez García, Esteban; Taylor, Ann C.; de Lorenzo, Víctor
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background Accumulation of inorganic polyphosphate (polyP), a persistent trait throughout the whole Tree of Life, is claimed to play a fundamental role in enduring environmental insults in a large variety of microorganisms. The share of polyP in the tolerance of the soil bacterium Pseudomonas putida KT2440 to a suite of physicochemical stresses has been studied on the background of its capacity as a host of oxidative biotransformations. Results Cells lacking polyphosphate kinase (Ppk), which expectedly presented a low intracellular polyP level, were more sensitive to a number of harsh external conditions such as ultraviolet irradiation, addition of β-lactam antibiotics and heavy metals (Cd2+ and Cu2+). Other phenotypes related to a high-energy phosphate load (e.g., swimming) were substantially weakened as well. Furthermore, the ppk mutant was consistently less tolerant to solvents and its survival in stationary phase was significantly affected. In contrast, the major metabolic routes were not significantly influenced by the loss of Ppk as diagnosed from respiration patterns of the mutant in phenotypic microarrays. However, the catalytic vigour of the mutant decreased to about 50% of that in the wild-type strain as estimated from the specific growth rate of cells carrying the catabolic TOL plasmid pWW0 for m- xylene biodegradation. The catalytic phenotype of the mutant was restored by over-expressing ppk in trans. Some of these deficits could be explained by the effect of the ppk mutation on the expression profile of the rpoS gene, the stationary phase sigma factor, which was revealed by the analysis of a P rpoS  → rpoS‘-’lacZ translational fusion. Still, every stress-related effect of lacking Ppk in P. putida was relatively moderate as compared to some of the conspicuous phenotypes reported for other bacteria. Conclusions While polyP can be involved in a myriad of cellular functions, the polymer seems to play a relatively secondary role in the genetic and biochemical networks that ultimately enable P. putida to endure environmental stresses. Instead, the main value of polyP could be ensuring a reservoire of energy during prolonged starvation. This is perhaps one of the reasons for polyP persistence in live systems despite its apparent lack of essentiality.
Fil: Nikel, Pablo Ivan. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Biotecnológicas - Instituto Tecnológico Chascomús. Instituto de Investigaciones Biotecnológicas (sede Chascomús); Argentina
Fil: Chavarría, Max. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Universidad de Costa Rica; Costa Rica
Fil: Martínez García, Esteban. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España
Fil: Taylor, Ann C.. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Harvard College; Estados Unidos
Fil: de Lorenzo, Víctor. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España
Materia
PSEUDOMONAS PUTIDA KT2440
POLYPHOSPHATE
STRESS RESISTANCE
BIOTRANSFORMATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/12527

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network_name_str CONICET Digital (CONICET)
spelling Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440Nikel, Pablo IvanChavarría, MaxMartínez García, EstebanTaylor, Ann C.de Lorenzo, VíctorPSEUDOMONAS PUTIDA KT2440POLYPHOSPHATESTRESS RESISTANCEBIOTRANSFORMATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background Accumulation of inorganic polyphosphate (polyP), a persistent trait throughout the whole Tree of Life, is claimed to play a fundamental role in enduring environmental insults in a large variety of microorganisms. The share of polyP in the tolerance of the soil bacterium Pseudomonas putida KT2440 to a suite of physicochemical stresses has been studied on the background of its capacity as a host of oxidative biotransformations. Results Cells lacking polyphosphate kinase (Ppk), which expectedly presented a low intracellular polyP level, were more sensitive to a number of harsh external conditions such as ultraviolet irradiation, addition of β-lactam antibiotics and heavy metals (Cd2+ and Cu2+). Other phenotypes related to a high-energy phosphate load (e.g., swimming) were substantially weakened as well. Furthermore, the ppk mutant was consistently less tolerant to solvents and its survival in stationary phase was significantly affected. In contrast, the major metabolic routes were not significantly influenced by the loss of Ppk as diagnosed from respiration patterns of the mutant in phenotypic microarrays. However, the catalytic vigour of the mutant decreased to about 50% of that in the wild-type strain as estimated from the specific growth rate of cells carrying the catabolic TOL plasmid pWW0 for m- xylene biodegradation. The catalytic phenotype of the mutant was restored by over-expressing ppk in trans. Some of these deficits could be explained by the effect of the ppk mutation on the expression profile of the rpoS gene, the stationary phase sigma factor, which was revealed by the analysis of a P rpoS  → rpoS‘-’lacZ translational fusion. Still, every stress-related effect of lacking Ppk in P. putida was relatively moderate as compared to some of the conspicuous phenotypes reported for other bacteria. Conclusions While polyP can be involved in a myriad of cellular functions, the polymer seems to play a relatively secondary role in the genetic and biochemical networks that ultimately enable P. putida to endure environmental stresses. Instead, the main value of polyP could be ensuring a reservoire of energy during prolonged starvation. This is perhaps one of the reasons for polyP persistence in live systems despite its apparent lack of essentiality.Fil: Nikel, Pablo Ivan. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Biotecnológicas - Instituto Tecnológico Chascomús. Instituto de Investigaciones Biotecnológicas (sede Chascomús); ArgentinaFil: Chavarría, Max. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Universidad de Costa Rica; Costa RicaFil: Martínez García, Esteban. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; EspañaFil: Taylor, Ann C.. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Harvard College; Estados UnidosFil: de Lorenzo, Víctor. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; EspañaBiomed Central2013-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/12527Nikel, Pablo Ivan; Chavarría, Max; Martínez García, Esteban; Taylor, Ann C.; de Lorenzo, Víctor; Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440; Biomed Central; Microbial Cell Factories; 12; 5-2013; 50-621475-2859enginfo:eu-repo/semantics/altIdentifier/url/http://microbialcellfactories.biomedcentral.com/articles/10.1186/1475-2859-12-50info:eu-repo/semantics/altIdentifier/url/http://dx.doi.org/10.1186/1475-2859-12-50info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:09:25Zoai:ri.conicet.gov.ar:11336/12527instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 10:09:25.329CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
title Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
spellingShingle Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
Nikel, Pablo Ivan
PSEUDOMONAS PUTIDA KT2440
POLYPHOSPHATE
STRESS RESISTANCE
BIOTRANSFORMATION
title_short Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
title_full Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
title_fullStr Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
title_full_unstemmed Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
title_sort Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440
dc.creator.none.fl_str_mv Nikel, Pablo Ivan
Chavarría, Max
Martínez García, Esteban
Taylor, Ann C.
de Lorenzo, Víctor
author Nikel, Pablo Ivan
author_facet Nikel, Pablo Ivan
Chavarría, Max
Martínez García, Esteban
Taylor, Ann C.
de Lorenzo, Víctor
author_role author
author2 Chavarría, Max
Martínez García, Esteban
Taylor, Ann C.
de Lorenzo, Víctor
author2_role author
author
author
author
dc.subject.none.fl_str_mv PSEUDOMONAS PUTIDA KT2440
POLYPHOSPHATE
STRESS RESISTANCE
BIOTRANSFORMATION
topic PSEUDOMONAS PUTIDA KT2440
POLYPHOSPHATE
STRESS RESISTANCE
BIOTRANSFORMATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background Accumulation of inorganic polyphosphate (polyP), a persistent trait throughout the whole Tree of Life, is claimed to play a fundamental role in enduring environmental insults in a large variety of microorganisms. The share of polyP in the tolerance of the soil bacterium Pseudomonas putida KT2440 to a suite of physicochemical stresses has been studied on the background of its capacity as a host of oxidative biotransformations. Results Cells lacking polyphosphate kinase (Ppk), which expectedly presented a low intracellular polyP level, were more sensitive to a number of harsh external conditions such as ultraviolet irradiation, addition of β-lactam antibiotics and heavy metals (Cd2+ and Cu2+). Other phenotypes related to a high-energy phosphate load (e.g., swimming) were substantially weakened as well. Furthermore, the ppk mutant was consistently less tolerant to solvents and its survival in stationary phase was significantly affected. In contrast, the major metabolic routes were not significantly influenced by the loss of Ppk as diagnosed from respiration patterns of the mutant in phenotypic microarrays. However, the catalytic vigour of the mutant decreased to about 50% of that in the wild-type strain as estimated from the specific growth rate of cells carrying the catabolic TOL plasmid pWW0 for m- xylene biodegradation. The catalytic phenotype of the mutant was restored by over-expressing ppk in trans. Some of these deficits could be explained by the effect of the ppk mutation on the expression profile of the rpoS gene, the stationary phase sigma factor, which was revealed by the analysis of a P rpoS  → rpoS‘-’lacZ translational fusion. Still, every stress-related effect of lacking Ppk in P. putida was relatively moderate as compared to some of the conspicuous phenotypes reported for other bacteria. Conclusions While polyP can be involved in a myriad of cellular functions, the polymer seems to play a relatively secondary role in the genetic and biochemical networks that ultimately enable P. putida to endure environmental stresses. Instead, the main value of polyP could be ensuring a reservoire of energy during prolonged starvation. This is perhaps one of the reasons for polyP persistence in live systems despite its apparent lack of essentiality.
Fil: Nikel, Pablo Ivan. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico La Plata. Instituto de Investigaciones Biotecnológicas - Instituto Tecnológico Chascomús. Instituto de Investigaciones Biotecnológicas (sede Chascomús); Argentina
Fil: Chavarría, Max. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Universidad de Costa Rica; Costa Rica
Fil: Martínez García, Esteban. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España
Fil: Taylor, Ann C.. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España. Harvard College; Estados Unidos
Fil: de Lorenzo, Víctor. Consejo Superior de Investigaciones Cientificas. Centro Nacional de Biotecnologia; España
description Background Accumulation of inorganic polyphosphate (polyP), a persistent trait throughout the whole Tree of Life, is claimed to play a fundamental role in enduring environmental insults in a large variety of microorganisms. The share of polyP in the tolerance of the soil bacterium Pseudomonas putida KT2440 to a suite of physicochemical stresses has been studied on the background of its capacity as a host of oxidative biotransformations. Results Cells lacking polyphosphate kinase (Ppk), which expectedly presented a low intracellular polyP level, were more sensitive to a number of harsh external conditions such as ultraviolet irradiation, addition of β-lactam antibiotics and heavy metals (Cd2+ and Cu2+). Other phenotypes related to a high-energy phosphate load (e.g., swimming) were substantially weakened as well. Furthermore, the ppk mutant was consistently less tolerant to solvents and its survival in stationary phase was significantly affected. In contrast, the major metabolic routes were not significantly influenced by the loss of Ppk as diagnosed from respiration patterns of the mutant in phenotypic microarrays. However, the catalytic vigour of the mutant decreased to about 50% of that in the wild-type strain as estimated from the specific growth rate of cells carrying the catabolic TOL plasmid pWW0 for m- xylene biodegradation. The catalytic phenotype of the mutant was restored by over-expressing ppk in trans. Some of these deficits could be explained by the effect of the ppk mutation on the expression profile of the rpoS gene, the stationary phase sigma factor, which was revealed by the analysis of a P rpoS  → rpoS‘-’lacZ translational fusion. Still, every stress-related effect of lacking Ppk in P. putida was relatively moderate as compared to some of the conspicuous phenotypes reported for other bacteria. Conclusions While polyP can be involved in a myriad of cellular functions, the polymer seems to play a relatively secondary role in the genetic and biochemical networks that ultimately enable P. putida to endure environmental stresses. Instead, the main value of polyP could be ensuring a reservoire of energy during prolonged starvation. This is perhaps one of the reasons for polyP persistence in live systems despite its apparent lack of essentiality.
publishDate 2013
dc.date.none.fl_str_mv 2013-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/12527
Nikel, Pablo Ivan; Chavarría, Max; Martínez García, Esteban; Taylor, Ann C.; de Lorenzo, Víctor; Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440; Biomed Central; Microbial Cell Factories; 12; 5-2013; 50-62
1475-2859
url http://hdl.handle.net/11336/12527
identifier_str_mv Nikel, Pablo Ivan; Chavarría, Max; Martínez García, Esteban; Taylor, Ann C.; de Lorenzo, Víctor; Accumulation of inorganic polyphosphate enables stress endurance and catalytic vigour in Pseudomonas putida KT2440; Biomed Central; Microbial Cell Factories; 12; 5-2013; 50-62
1475-2859
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://microbialcellfactories.biomedcentral.com/articles/10.1186/1475-2859-12-50
info:eu-repo/semantics/altIdentifier/url/http://dx.doi.org/10.1186/1475-2859-12-50
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Biomed Central
publisher.none.fl_str_mv Biomed Central
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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