Details
Original language | English |
---|---|
Article number | 102201 |
Journal | Journal of Biological Chemistry |
Volume | 298 |
Issue number | 8 |
Early online date | 25 Jun 2022 |
Publication status | Published - Aug 2022 |
Abstract
Fluorescent pseudomonads such as Pseudomonas aeruginosa or Pseudomonas fluorescens produce pyoverdine siderophores that ensure iron-supply in iron-limited environments. After its synthesis in the cytoplasm, the nonfluorescent pyoverdine precursor ferribactin is exported into the periplasm, where the enzymes PvdQ, PvdP, PvdO, PvdN, and PtaA are responsible for fluorophore maturation and tailoring steps. While the roles of all these enzymes are clear, little is known about the role of PvdM, a human renal dipeptidase–related protein that is predicted to be periplasmic and that is essential for pyoverdine biogenesis. Here, we reveal the subcellular localization and functional role of PvdM. Using the model organism P. fluorescens, we show that PvdM is anchored to the periplasmic side of the cytoplasmic membrane, where it is indispensable for the activity of the tyrosinase PvdP. While PvdM does not share the metallopeptidase function of renal dipeptidase, it still has the corresponding peptide-binding site. The substrate of PvdP, deacylated ferribactin, is secreted by a ΔpvdM mutant strain, indicating that PvdM prevents loss of this periplasmic biosynthesis intermediate into the medium by ensuring the efficient transfer of ferribactin to PvdP in vivo. We propose that PvdM belongs to a new dipeptidase-related protein subfamily with inactivated Zn 2+ coordination sites, members of which are usually genetically linked to TonB-dependent uptake systems and often associated with periplasmic FAD-dependent oxidoreductases related to D-amino acid oxidases. We suggest that these proteins are necessary for selective binding, exposure, or transfer of specific D- and L-amino acid–containing peptides and other periplasmic biomolecules in manifold pathways.
Keywords
- Pseudomonas aeruginosa, Pseudomonas fluorescens, bacterial metabolism, biosynthesis, membrane protein, periplasm, pyoverdine maturation, siderophore
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Biochemistry
- Biochemistry, Genetics and Molecular Biology(all)
- Molecular Biology
- Biochemistry, Genetics and Molecular Biology(all)
- Cell Biology
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In: Journal of Biological Chemistry, Vol. 298, No. 8, 102201, 08.2022.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
T1 - PvdM of fluorescent pseudomonads is required for the oxidation of ferribactin by PvdP in periplasmic pyoverdine maturation
AU - Sugue, Michael-Frederick
AU - Burdur, Ali Nazmi
AU - Ringel, Michael Thomas
AU - Dräger, Gerald
AU - Brüser, Thomas
N1 - Funding Information: We gratefully acknowledge the skillful technical assistance of Sybille Traupe, Katrin Gunka, and Inge Reupke (Leibniz University Hannover). T. B. conceptualization; M.-F. S. and M. T. R. methodology; M.-F. S. validation; M.-F. S. A. N. B. G. D. and T. B. investigation; T. B. writing–original draft; M.-F. S. A. N. B. M. T. R. G. D. and T. B. writing–review & editing; M.-F. S. and T. B. visualization; T. B. supervision; T. B. funding acquisition. This work was supported by grant BR 2285/7-1 of the German Research Foundation (DFG) to T. B.
PY - 2022/8
Y1 - 2022/8
N2 - Fluorescent pseudomonads such as Pseudomonas aeruginosa or Pseudomonas fluorescens produce pyoverdine siderophores that ensure iron-supply in iron-limited environments. After its synthesis in the cytoplasm, the nonfluorescent pyoverdine precursor ferribactin is exported into the periplasm, where the enzymes PvdQ, PvdP, PvdO, PvdN, and PtaA are responsible for fluorophore maturation and tailoring steps. While the roles of all these enzymes are clear, little is known about the role of PvdM, a human renal dipeptidase–related protein that is predicted to be periplasmic and that is essential for pyoverdine biogenesis. Here, we reveal the subcellular localization and functional role of PvdM. Using the model organism P. fluorescens, we show that PvdM is anchored to the periplasmic side of the cytoplasmic membrane, where it is indispensable for the activity of the tyrosinase PvdP. While PvdM does not share the metallopeptidase function of renal dipeptidase, it still has the corresponding peptide-binding site. The substrate of PvdP, deacylated ferribactin, is secreted by a ΔpvdM mutant strain, indicating that PvdM prevents loss of this periplasmic biosynthesis intermediate into the medium by ensuring the efficient transfer of ferribactin to PvdP in vivo. We propose that PvdM belongs to a new dipeptidase-related protein subfamily with inactivated Zn 2+ coordination sites, members of which are usually genetically linked to TonB-dependent uptake systems and often associated with periplasmic FAD-dependent oxidoreductases related to D-amino acid oxidases. We suggest that these proteins are necessary for selective binding, exposure, or transfer of specific D- and L-amino acid–containing peptides and other periplasmic biomolecules in manifold pathways.
AB - Fluorescent pseudomonads such as Pseudomonas aeruginosa or Pseudomonas fluorescens produce pyoverdine siderophores that ensure iron-supply in iron-limited environments. After its synthesis in the cytoplasm, the nonfluorescent pyoverdine precursor ferribactin is exported into the periplasm, where the enzymes PvdQ, PvdP, PvdO, PvdN, and PtaA are responsible for fluorophore maturation and tailoring steps. While the roles of all these enzymes are clear, little is known about the role of PvdM, a human renal dipeptidase–related protein that is predicted to be periplasmic and that is essential for pyoverdine biogenesis. Here, we reveal the subcellular localization and functional role of PvdM. Using the model organism P. fluorescens, we show that PvdM is anchored to the periplasmic side of the cytoplasmic membrane, where it is indispensable for the activity of the tyrosinase PvdP. While PvdM does not share the metallopeptidase function of renal dipeptidase, it still has the corresponding peptide-binding site. The substrate of PvdP, deacylated ferribactin, is secreted by a ΔpvdM mutant strain, indicating that PvdM prevents loss of this periplasmic biosynthesis intermediate into the medium by ensuring the efficient transfer of ferribactin to PvdP in vivo. We propose that PvdM belongs to a new dipeptidase-related protein subfamily with inactivated Zn 2+ coordination sites, members of which are usually genetically linked to TonB-dependent uptake systems and often associated with periplasmic FAD-dependent oxidoreductases related to D-amino acid oxidases. We suggest that these proteins are necessary for selective binding, exposure, or transfer of specific D- and L-amino acid–containing peptides and other periplasmic biomolecules in manifold pathways.
KW - Pseudomonas aeruginosa
KW - Pseudomonas fluorescens
KW - bacterial metabolism
KW - biosynthesis
KW - membrane protein
KW - periplasm
KW - pyoverdine maturation
KW - siderophore
UR - http://www.scopus.com/inward/record.url?scp=85134800039&partnerID=8YFLogxK
U2 - 10.1016/j.jbc.2022.102201
DO - 10.1016/j.jbc.2022.102201
M3 - Article
VL - 298
JO - Journal of Biological Chemistry
JF - Journal of Biological Chemistry
SN - 0021-9258
IS - 8
M1 - 102201
ER -