Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains

Shady Mansour Kamal; Morten Levin Rybtke; Manfred Nimtz; Stefanie Sperlein; Christian Giske; Janja Trček; Julien Deschamps; Romain Briandet; Luciana Dini; Lothar Jänsch; Tim Tolker-Nielsen; Changhan Lee; Ute Römling

doi:10.3389/fmicb.2019.01372

Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains

Shady Mansour Kamal, Morten Levin Rybtke, Manfred Nimtz, Stefanie Sperlein, Christian Giske, Janja Trček, Julien Deschamps, Romain Briandet, Luciana Dini, Lothar Jänsch, Tim Tolker-Nielsen, Changhan Lee, Ute Römling^*

^*Corresponding author for this work

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Abstract

Pseudomonas aeruginosa is an environmental bacterium and a nosocomial pathogen with clone C one of the most prevalent clonal groups. The P. aeruginosa clone C specific genomic island PACGI-1 harbors a xenolog of ftsH encoding a functionally diverse membrane-spanning ATP-dependent metalloprotease on the core genome. In the aquatic isolate P. aeruginosa SG17M, the core genome copy ftsH1 significantly affects growth and dominantly mediates a broad range of phenotypes, such as secretion of secondary metabolites, swimming and twitching motility and resistance to aminoglycosides, while the PACGI-1 xenolog ftsH2 backs up the phenotypes in the ftsH1 mutant background. The two proteins, with conserved motifs for disaggregase and protease activity present in FtsH1 and FtsH2, have the ability to form homo- and hetero-oligomers with ftsH2 distinctively expressed in the late stationary phase of growth. However, mainly FtsH1 degrades a major substrate, the heat shock transcription factor RpoH. Pull-down experiments with substrate trap-variants inactive in proteolytic activity indicate both FtsH1 and FtsH2 to interact with the inhibitory protein HflC, while the phenazine biosynthesis protein PhzC was identified as a substrate of FtsH1. In summary, as an exception in P. aeruginosa, clone C harbors two copies of the ftsH metallo-protease, which cumulatively are required for the expression of a diversity of phenotypes.

Original language	English
Article number	1372
Journal	Frontiers in Microbiology
Volume	10
Issue number	JULY
Number of pages	18
ISSN	1664-302X
DOIs	https://doi.org/10.3389/fmicb.2019.01372
Publication status	Published - 2019

Keywords

Autolysis
Clone C strains
FtsH protease
Heat shock factor RpoH
Phenazine
Pseudomonas aeruginosa
Secondary metabolite
Virulence

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Two FtsH Proteases Contribute to Fitness and Adaptation of Pseudomonas aeruginosa Clone C StrainsFinal published version, 3.2 MBLicence: CC BY

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Kamal, S. M., Rybtke, M. L., Nimtz, M., Sperlein, S., Giske, C., Trček, J., Deschamps, J., Briandet, R., Dini, L., Jänsch, L., Tolker-Nielsen, T., Lee, C., & Römling, U. (2019). Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains. Frontiers in Microbiology, 10(JULY), Article 1372. https://doi.org/10.3389/fmicb.2019.01372

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title = "Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains",

abstract = "Pseudomonas aeruginosa is an environmental bacterium and a nosocomial pathogen with clone C one of the most prevalent clonal groups. The P. aeruginosa clone C specific genomic island PACGI-1 harbors a xenolog of ftsH encoding a functionally diverse membrane-spanning ATP-dependent metalloprotease on the core genome. In the aquatic isolate P. aeruginosa SG17M, the core genome copy ftsH1 significantly affects growth and dominantly mediates a broad range of phenotypes, such as secretion of secondary metabolites, swimming and twitching motility and resistance to aminoglycosides, while the PACGI-1 xenolog ftsH2 backs up the phenotypes in the ftsH1 mutant background. The two proteins, with conserved motifs for disaggregase and protease activity present in FtsH1 and FtsH2, have the ability to form homo- and hetero-oligomers with ftsH2 distinctively expressed in the late stationary phase of growth. However, mainly FtsH1 degrades a major substrate, the heat shock transcription factor RpoH. Pull-down experiments with substrate trap-variants inactive in proteolytic activity indicate both FtsH1 and FtsH2 to interact with the inhibitory protein HflC, while the phenazine biosynthesis protein PhzC was identified as a substrate of FtsH1. In summary, as an exception in P. aeruginosa, clone C harbors two copies of the ftsH metallo-protease, which cumulatively are required for the expression of a diversity of phenotypes.",

keywords = "Autolysis, Clone C strains, FtsH protease, Heat shock factor RpoH, Phenazine, Pseudomonas aeruginosa, Secondary metabolite, Virulence",

author = "Kamal, {Shady Mansour} and Rybtke, {Morten Levin} and Manfred Nimtz and Stefanie Sperlein and Christian Giske and Janja Tr{\v c}ek and Julien Deschamps and Romain Briandet and Luciana Dini and Lothar J{\"a}nsch and Tim Tolker-Nielsen and Changhan Lee and Ute R{\"o}mling",

year = "2019",

doi = "10.3389/fmicb.2019.01372",

language = "English",

volume = "10",

journal = "Frontiers in Microbiology",

issn = "1664-302X",

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TY - JOUR

T1 - Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains

AU - Kamal, Shady Mansour

AU - Rybtke, Morten Levin

AU - Nimtz, Manfred

AU - Sperlein, Stefanie

AU - Giske, Christian

AU - Trček, Janja

AU - Deschamps, Julien

AU - Briandet, Romain

AU - Dini, Luciana

AU - Jänsch, Lothar

AU - Tolker-Nielsen, Tim

AU - Lee, Changhan

AU - Römling, Ute

PY - 2019

Y1 - 2019

N2 - Pseudomonas aeruginosa is an environmental bacterium and a nosocomial pathogen with clone C one of the most prevalent clonal groups. The P. aeruginosa clone C specific genomic island PACGI-1 harbors a xenolog of ftsH encoding a functionally diverse membrane-spanning ATP-dependent metalloprotease on the core genome. In the aquatic isolate P. aeruginosa SG17M, the core genome copy ftsH1 significantly affects growth and dominantly mediates a broad range of phenotypes, such as secretion of secondary metabolites, swimming and twitching motility and resistance to aminoglycosides, while the PACGI-1 xenolog ftsH2 backs up the phenotypes in the ftsH1 mutant background. The two proteins, with conserved motifs for disaggregase and protease activity present in FtsH1 and FtsH2, have the ability to form homo- and hetero-oligomers with ftsH2 distinctively expressed in the late stationary phase of growth. However, mainly FtsH1 degrades a major substrate, the heat shock transcription factor RpoH. Pull-down experiments with substrate trap-variants inactive in proteolytic activity indicate both FtsH1 and FtsH2 to interact with the inhibitory protein HflC, while the phenazine biosynthesis protein PhzC was identified as a substrate of FtsH1. In summary, as an exception in P. aeruginosa, clone C harbors two copies of the ftsH metallo-protease, which cumulatively are required for the expression of a diversity of phenotypes.

AB - Pseudomonas aeruginosa is an environmental bacterium and a nosocomial pathogen with clone C one of the most prevalent clonal groups. The P. aeruginosa clone C specific genomic island PACGI-1 harbors a xenolog of ftsH encoding a functionally diverse membrane-spanning ATP-dependent metalloprotease on the core genome. In the aquatic isolate P. aeruginosa SG17M, the core genome copy ftsH1 significantly affects growth and dominantly mediates a broad range of phenotypes, such as secretion of secondary metabolites, swimming and twitching motility and resistance to aminoglycosides, while the PACGI-1 xenolog ftsH2 backs up the phenotypes in the ftsH1 mutant background. The two proteins, with conserved motifs for disaggregase and protease activity present in FtsH1 and FtsH2, have the ability to form homo- and hetero-oligomers with ftsH2 distinctively expressed in the late stationary phase of growth. However, mainly FtsH1 degrades a major substrate, the heat shock transcription factor RpoH. Pull-down experiments with substrate trap-variants inactive in proteolytic activity indicate both FtsH1 and FtsH2 to interact with the inhibitory protein HflC, while the phenazine biosynthesis protein PhzC was identified as a substrate of FtsH1. In summary, as an exception in P. aeruginosa, clone C harbors two copies of the ftsH metallo-protease, which cumulatively are required for the expression of a diversity of phenotypes.

KW - Autolysis

KW - Clone C strains

KW - FtsH protease

KW - Heat shock factor RpoH

KW - Phenazine

KW - Pseudomonas aeruginosa

KW - Secondary metabolite

KW - Virulence

U2 - 10.3389/fmicb.2019.01372

DO - 10.3389/fmicb.2019.01372

M3 - Journal article

C2 - 31338071

AN - SCOPUS:85069496683

SN - 1664-302X

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

IS - JULY

M1 - 1372

ER -

Two FtsH proteases contribute to fitness and adaptation of pseudomonas aeruginosa Clone C strains

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