Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective

Inorganic phosphate (Pi) is a central nutrient and signal molecule for bacteria. Pi limitation was shown to increase the virulence of several phylogenetically diverse pathogenic bacteria with different lifestyles. Hypophosphatemia enhances the risk of death in patients due to general bacteremia and...

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Autores: Matilla, Miguel A., Udaondo, Zulema, Maaß, S., Becher, Dörte, Krell, Tino
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:dnet:digitalcsic_::2252daa6bf5b47e67c52c47ecc6bf758
Acceso en línea:http://hdl.handle.net/10261/305894
Access Level:acceso abierto
Palabra clave:Pseudomonas aeruginosa
Phosphate starvation
Proteomics
Anti-infective
Therapy
Pyocyanin
Quorum sensing
Virulence
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spelling Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspectiveMatilla, Miguel A.Udaondo, ZulemaMaaß, S.Becher, DörteKrell, TinoPseudomonas aeruginosaPhosphate starvationProteomicsAnti-infectiveTherapyPyocyaninQuorum sensingVirulenceInorganic phosphate (Pi) is a central nutrient and signal molecule for bacteria. Pi limitation was shown to increase the virulence of several phylogenetically diverse pathogenic bacteria with different lifestyles. Hypophosphatemia enhances the risk of death in patients due to general bacteremia and was observed after surgical injury in humans. Phosphate therapy, or the reduction of bacterial virulence by the administration of Pi or phosphate-containing compounds, is a promising anti-infective therapy approach that will not cause cytotoxicity or the emergence of antibiotic-resistant strains. The proof of concept of phosphate therapy has been obtained using primarily Pseudomonas aeruginosa (PA). However, a detailed understanding of Pi-induced changes at protein levels is missing. Using pyocyanin production as proxy, we show that the Pi-mediated induction of virulence is a highly cooperative process that occurs between 0.2 to 0.6 mM Pi. We present a proteomics study of PA grown in minimal medium supplemented with either 0.2 mM or 1 mM Pi and rich medium. About half of the predicted PA proteins could be quantified. Among the 1,471 dysregulated proteins comparing growth in 0.2 mM to 1 mM Pi, 1,100 were depleted under Pi-deficient conditions. Most of these proteins are involved in general and energy metabolism, different biosynthetic and catabolic routes, or transport. Pi depletion caused accumulation of proteins that belong to all major families of virulence factors, including pyocyanin synthesis, secretion systems, quorum sensing, chemosensory signaling, and the secretion of proteases, phospholipases, and phosphatases, which correlated with an increase in exoenzyme production and antibacterial activity.This work was supported by grants PID2019-103972GA-I00 (to M.A.M.) and PID2020-112612GB-I00 (to T.K.) from the Spanish Ministry for Science and Innovation/Agencia Estatal de Investigación 10.13039/501100011033 and grant P18-FR-1621 (to T.K.) from the Junta de Andalucía.American Society for MicrobiologyEuropean CommissionMinisterio de Ciencia e Innovación (España)Junta de AndalucíaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320222023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/305894reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103972GA-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-112612GB-I00http://dx.doi.org/10.1128/spectrum.02590-22Síinfo:eu-repo/semantics/openAccessoai:dnet:digitalcsic_::2252daa6bf5b47e67c52c47ecc6bf7582026-05-22T06:33:51Z
dc.title.none.fl_str_mv Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
title Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
spellingShingle Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
Matilla, Miguel A.
Pseudomonas aeruginosa
Phosphate starvation
Proteomics
Anti-infective
Therapy
Pyocyanin
Quorum sensing
Virulence
title_short Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
title_full Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
title_fullStr Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
title_full_unstemmed Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
title_sort Virulence induction in Pseudomonas aeruginosa under inorganic phosphate limitation: a proteomics perspective
dc.creator.none.fl_str_mv Matilla, Miguel A.
Udaondo, Zulema
Maaß, S.
Becher, Dörte
Krell, Tino
author Matilla, Miguel A.
author_facet Matilla, Miguel A.
Udaondo, Zulema
Maaß, S.
Becher, Dörte
Krell, Tino
author_role author
author2 Udaondo, Zulema
Maaß, S.
Becher, Dörte
Krell, Tino
author2_role author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Ciencia e Innovación (España)
Junta de Andalucía
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Pseudomonas aeruginosa
Phosphate starvation
Proteomics
Anti-infective
Therapy
Pyocyanin
Quorum sensing
Virulence
topic Pseudomonas aeruginosa
Phosphate starvation
Proteomics
Anti-infective
Therapy
Pyocyanin
Quorum sensing
Virulence
description Inorganic phosphate (Pi) is a central nutrient and signal molecule for bacteria. Pi limitation was shown to increase the virulence of several phylogenetically diverse pathogenic bacteria with different lifestyles. Hypophosphatemia enhances the risk of death in patients due to general bacteremia and was observed after surgical injury in humans. Phosphate therapy, or the reduction of bacterial virulence by the administration of Pi or phosphate-containing compounds, is a promising anti-infective therapy approach that will not cause cytotoxicity or the emergence of antibiotic-resistant strains. The proof of concept of phosphate therapy has been obtained using primarily Pseudomonas aeruginosa (PA). However, a detailed understanding of Pi-induced changes at protein levels is missing. Using pyocyanin production as proxy, we show that the Pi-mediated induction of virulence is a highly cooperative process that occurs between 0.2 to 0.6 mM Pi. We present a proteomics study of PA grown in minimal medium supplemented with either 0.2 mM or 1 mM Pi and rich medium. About half of the predicted PA proteins could be quantified. Among the 1,471 dysregulated proteins comparing growth in 0.2 mM to 1 mM Pi, 1,100 were depleted under Pi-deficient conditions. Most of these proteins are involved in general and energy metabolism, different biosynthetic and catabolic routes, or transport. Pi depletion caused accumulation of proteins that belong to all major families of virulence factors, including pyocyanin synthesis, secretion systems, quorum sensing, chemosensory signaling, and the secretion of proteases, phospholipases, and phosphatases, which correlated with an increase in exoenzyme production and antibacterial activity.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/305894
url http://hdl.handle.net/10261/305894
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-103972GA-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-112612GB-I00
http://dx.doi.org/10.1128/spectrum.02590-22
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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