Applied Microbiology and Biotechnology

, Volume 101, Issue 1, pp 139–145 | Cite as

Another example of enzymatic promiscuity: the polyphosphate kinase of Streptomyces lividans is endowed with phospholipase D activity

  • Catherine Esnault
  • Denis Leiber
  • Claire Toffano-Nioche
  • Zahra Tanfin
  • Marie-Joelle Virolle
Biotechnologically relevant enzymes and proteins

Abstract

Polyphosphate kinases (PPK) from different bacteria, including that of Streptomyces lividans, were shown to contain the typical HKD motif present in phospholipase D (PLD) and showed structural similarities to the latter. This observation prompted us to investigate the PLD activity of PPK of S. lividans, in vitro. The ability of PPK to catalyze the hydrolysis of phosphatidylcholine (PC), the PLD substrate, was assessed by the quantification of [3H]phosphatidic acid (PA) released from [3H]PC-labeled ELT3 cell membranes. Basal cell membrane PLD activity as well as GTPγS-activated PLD activity was higher in the presence than in absence of PPK. After abolition of the basal PLD activity of the membranes by heat or tryptic treatment, the addition of PPK to cell membranes was still accompanied by an increased production of PA demonstrating that PPK also bears a PLD activity. PLD activity of PPK was also assessed by the production of choline from hydrolysis of 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC) in the presence of the Amplex Red reagent and compared to two commercial PLD enzymes. These data demonstrated that PPK is endowed with a weak but clearly detectable PLD activity. The question of the biological signification, if any, of this enzymatic promiscuity is discussed.

Keywords

Polyphosphate kinase Phospholipase D Promiscuous enzyme Lipid droplets 

Notes

Acknowledgments

This work was financed by the University Paris-Sud, the University Pierre and Marie Curie, and the CNRS. Dr. Bruno Collinet is acknowledged for helpful discussions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statements

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Bowman EP, Uhlinger DJ, Lambeth JD (1993) Neutrophil phospholipase D is activated by a membrane-associated Rho family small molecular weight GTP-binding protein. J Biol Chem 268:21509–21512PubMedGoogle Scholar
  2. Brown MR, Kornberg A (2004) Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci U S A 101:16085–16087CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cheek S, Ginalski K, Zhang H, Grishin NV (2005) A comprehensive update of the sequence and structure classification of kinases. BMC Struct Biol 5:6. doi: 10.1186/1472-6807-5-6 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chouayekh H, Virolle MJ (2002) The polyphosphate kinase plays a negative role in the control of antibiotic production in Streptomyces lividans. Mol Microbiol 43:919–930CrossRefPubMedGoogle Scholar
  5. Exton JH (2002) Regulation of phospholipase D. FEBS Lett 531:58–61CrossRefPubMedGoogle Scholar
  6. Fei W, Shui G, Zhang Y, Krahmer N, Ferguson C, Kapterian TS, Lin RC, Dawes IW, Brown AJ, Li P, Huang X, Parton RG, Wenk MR, Walther TC, Yang H (2011) A role for phosphatidic acid in the formation of “supersized” lipid droplets. PLoS Genet 7:e1002201. doi: 10.1371/journal.pgen.1002201 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ghorbel S, Kormanec J, Artus A, Virolle MJ (2006b) Transcriptional studies and regulatory interactions between the phoR-phoP operon and the phoU, mtpA, and ppk genes of Streptomyces lividans TK24. J Bacteriol 188:677–686CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ghorbel S, Smirnov A, Chouayekh H, Sperandio B, Esnault C, Kormanec J, Virolle MJ (2006a) Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J Bacteriol 188:6269–6276Google Scholar
  9. Holbrook PG, Pannell LK, Daly JW (1991) Phospholipase D-catalyzed hydrolysis of phosphatidylcholine occurs with P-O bond cleavage. Biochim Biophys Acta 1084:155–158CrossRefPubMedGoogle Scholar
  10. Imamura S, Horiuti Y (1979) Purification of Streptomyces chromofuscus phospholipase D by hydrophobic affinity chromatography on palmitoyl cellulose. J Biochem 85:79–95PubMedGoogle Scholar
  11. Jensen M, Cool RH, Mortensen KK, Clark BF, Parmeggiani A (1989) Structure-function relationships of elongation factor Tu. Isolation and activity of the guanine-nucleotide-binding domain. Eur J Biochem 182:247–255CrossRefPubMedGoogle Scholar
  12. Kato J, Yamamoto T, Yamada K, Ohtake H (1993) Cloning, sequence and characterization of the polyphosphate kinase-encoding gene (ppk) of Klebsiella aerogenes. Gene 137:237–242CrossRefPubMedGoogle Scholar
  13. Khersonsky O, Tawfik DS (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 79:471–505. doi: 10.1146/annurev-biochem-030409-143718 CrossRefPubMedGoogle Scholar
  14. Koonin EV (1996) A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins. Trends Biochem Sci 21:242–243CrossRefPubMedGoogle Scholar
  15. Leiros I, Hough E, D’Arrigo P, Carrea G, Pedrocchi-Fantoni G, Secundo F, Servi S (2000) Crystallization and preliminary X-ray diffraction studies of phospholipase D from Streptomyces sp. Acta Crystallogr D Biol Crystallogr 56:466–468CrossRefPubMedGoogle Scholar
  16. Le Maréchal P, Decottignies P, Marchand CH, Degrouard J, Jaillard D, Dulermo T, Froissard M, Smirnov A, Chapuis V, Virolle MJ (2013) Comparative proteomic analysis of Streptomyces lividans wild-type and ppk mutant strains reveals the importance of storage lipids for antibiotic biosynthesis. Appl Environ Microbiol 79:5907–5917CrossRefPubMedPubMedCentralGoogle Scholar
  17. Le Stunff H, Dokhac L, Bourgoin S, Bader MF, Harbon S (2000) Phospholipase D in rat myometrium: occurrence of a membrane-bound ARF6 (ADP-ribosylation factor 6)-regulated activity controlled by betagamma subunits of heterotrimeric G-proteins. Biochem J 352(Pt 2):491–499CrossRefPubMedPubMedCentralGoogle Scholar
  18. Newman L, Drees B, Forte L, Hamilton J (1994) Parathyroid hormone (PTH) secretion: stimulation of PTH secretion by a peptide derived from the adenosine diphosphate-ribosylation factor. Endocrinology 135:576–582PubMedGoogle Scholar
  19. Olson SC, Bowman EP, Lambeth JD (1991) Phospholipase D activation in a cell-free system from human neutrophils by phorbol 12-myristate 13-acetate and guanosine 5′-O-(3-thiotriphosphate). Activation is calcium dependent and requires protein factors in both the plasma membrane and cytosol. J Biol Chem 266:17236–17242PubMedGoogle Scholar
  20. Oude Weernink PA, López de Jesús M, Schmidt M (2007) Phospholipase D signaling: orchestration by PIP2 and small GTPases. Naunyn Schmiedeberg’s Arch Pharmacol 374:399–411CrossRefGoogle Scholar
  21. Ponting CP, Kerr ID (1996) A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Sci 5:914–922CrossRefPubMedPubMedCentralGoogle Scholar
  22. Rao NN, Gómez-García MR, Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78:605–647. doi: 10.1146/annurev.biochem.77.083007.093039 CrossRefPubMedGoogle Scholar
  23. Robin P, Chouayekh S, Bole-Feysot C, Leiber D, Tanfin Z (2005) Contribution of phospholipase D in endothelin-1-mediated extracellular signal-regulated kinase activation and proliferation in rat uterine leiomyoma cells. Biol Reprod 72:69–77CrossRefPubMedGoogle Scholar
  24. Selvy PE, Lavieri RR, Lindsley CW, Brown HA (2011) Phospholipase D: enzymology, functionality, and chemical modulation. Chem Rev 111:6064–6119. doi: 10.1021/cr200296t CrossRefPubMedPubMedCentralGoogle Scholar
  25. Sharfstein ST, Keasling JD (1994) Polyphosphate metabolism in Escherichia coli. Ann N Y Acad Sci 745:77–91CrossRefPubMedGoogle Scholar
  26. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. doi: 10.1038/msb.2011.75 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Yang H, Roberts MF (2003) Phosphohydrolase and transphosphatidylation reactions of two Streptomyces phospholipase D enzymes: covalent versus noncovalent catalysis. Protein Sci 12:2087–2098CrossRefPubMedPubMedCentralGoogle Scholar
  28. Zhu Y, Huang W, Lee SS, Xu W (2005) Crystal structure of a polyphosphate kinase and its implications for polyphosphate synthesis. EMBO Rep 6:681–687CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Catherine Esnault
    • 1
    • 2
  • Denis Leiber
    • 3
  • Claire Toffano-Nioche
    • 4
  • Zahra Tanfin
    • 5
  • Marie-Joelle Virolle
    • 1
  1. 1.Institute of Integrative Biology of the Cell (I2BC), Group “Energetic Metabolism of Streptomyces”, CEA, CNRSUniversity of Paris-Sud, INRA, University Paris-SaclayGif-sur-Yvette CedexFrance
  2. 2.Sorbonne Universities, UPMC University of Paris 06ParisFrance
  3. 3.INSERM U1063University of AngersAngersFrance
  4. 4.Institute of Integrative Biology of the Cell (I2BC), Group “RNA Sequence, Structure & Function”, CEA, CNRSUniversity of Paris-Sud, INRA, University Paris-SaclayGif-sur-Yvette CedexFrance
  5. 5.Institut de Biologie Animale, Intégrative et Cellulaire (IBAIC), INSERM U1174University of Paris-SudOrsay CedexFrance

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