Involvement of the Pseudomonas aeruginosa MexAB-OprM efflux pump in the secretion of the metallophore pseudopaline.
Bacteria
/ metabolism
Bacterial Outer Membrane Proteins
/ genetics
Bacterial Proteins
/ metabolism
Bodily Secretions
/ metabolism
Drug Resistance, Multiple, Bacterial
/ drug effects
Membrane Transport Proteins
/ genetics
Microbial Sensitivity Tests
Oligopeptides
/ metabolism
Pseudomonas aeruginosa
/ metabolism
MexAB-OprM
Pseudomonas aeruginosa
efflux pump
metallophore
pseudopaline
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
06
02
2020
revised:
07
08
2020
accepted:
28
08
2020
pubmed:
9
9
2020
medline:
24
8
2021
entrez:
8
9
2020
Statut:
ppublish
Résumé
To overcome the metal restriction imposed by the host's nutritional immunity, pathogenic bacteria use high metal affinity molecules called metallophores. Metallophore-mediated metal uptake pathways necessitate complex cycles of synthesis, secretion, and recovery of the metallophore across the bacterial envelope. We recently discovered staphylopine and pseudopaline, two members of a new family of broad-spectrum metallophores important for bacterial survival during infections. Here, we are expending the molecular understanding of the pseudopaline transport cycle across the diderm envelope of the Gram-negative bacterium Pseudomonas aeruginosa. We first explored pseudopaline secretion by performing in vivo quantifications in various genetic backgrounds and revealed the specific involvement of the MexAB-OprM efflux pump in pseudopaline transport across the outer membrane. We then addressed the recovery part of the cycle by investigating the fate of the recaptured metal-loaded pseudopaline. To do so, we combined in vitro reconstitution experiments and in vivo phenotyping in absence of pseudopaline transporters to reveal the existence of a pseudopaline modification mechanism, possibly involved in the metal release following pseudopaline recovery. Overall, our data allowed us to provide an improved molecular model of secretion, recovery, and fate of this important metallophore by P. aeruginosa.
Substances chimiques
Bacterial Outer Membrane Proteins
0
Bacterial Proteins
0
Membrane Transport Proteins
0
MexA protein, Pseudomonas aeruginosa
0
Oligopeptides
0
OprM protein, Pseudomonas aeruginosa
0
pseudopaline
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
84-98Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Andreini, C., Banci, L., Bertini, I. and Rosato, A. (2006) Zinc through the three domains of life. Journal of Proteome Research, 5, 3173-3178.
Andreini, C., Bertini, I., Cavallaro, G., Holliday, G.L. and Thornton, J.M. (2008) Metal ions in biological catalysis: from enzyme databases to general principles. JBIC Journal of Biological Inorganic Chemistry, 13, 1205-1218.
Bleuel, C., Grosse, C., Taudte, N., Scherer, J., Wesenberg, D., Krauss, G.J., et al. (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. Journal of Bacteriology, 187, 6701-6707.
Bleves, S., Viarre, V., Salacha, R., Michel, G.P., Filloux, A. and Voulhoux, R. (2010) Protein secretion systems in Pseudomonas aeruginosa: A wealth of pathogenic weapons. International Journal of Medical Microbiology, 300, 534-543.
Burse, A., Weingart, H. and Ullrich, M.S. (2004) The phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Molecular Plant-Microbe Interactions, 17, 43-54.
Chaturvedi, K.S., Hung, C.S., Crowley, J.R., Stapleton, A.E. and Henderson, J.P. (2012) The siderophore yersiniabactin binds copper to protect pathogens during infection. Nature Chemical Biology, 8, 731-736.
Crouch, M.L., Castor, M., Karlinsey, J.E., Kalhorn, T. and Fang, F.C. (2008) Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Molecular Microbiology, 67, 971-983.
Evans, K., Passador, L., Srikumar, R., Tsang, E., Nezezon, J. and Poole, K. (1998) Influence of the MexAB-OprM multidrug efflux system on quorum sensing in Pseudomonas aeruginosa. Journal of Bacteriology, 180, 5443-5447.
Figurski, D.H. and Helinski, D.R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proceedings of the National Academy of Sciences USA, 76, 1648-1652.
Furrer, J.L., Sanders, D.N., Hook-Barnard, I.G. and McIntosh, M.A. (2002) Export of the siderophore enterobactin in Escherichia coli: Involvement of a 43 kDa membrane exporter. Molecular Microbiology, 44, 1225-1234.
Ghssein, G., Brutesco, C., Ouerdane, L., Fojcik, C., Izaute, A., Wang, S., et al. (2016) Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science, 352, 1105-1109.
Gi, M., Lee, K.M., Kim, S.C., Yoon, J.H., Yoon, S.S. and Choi, J.Y. (2015) A novel siderophore system is essential for the growth of Pseudomonas aeruginosa in airway mucus. Scientific Reports, 5, 14644.
Greenwald, J., Hoegy, F., Nader, M., Journet, L., Mislin, G.L., Graumann, P.L., et al. (2007) Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa. A role for ferrous iron. Journal of Biological Chemistry, 282, 2987-2995.
Hajjar, C., Fanelli, R., Laffont, C., Brutesco, C., Cullia, G., Tribout, M., et al. (2019) Control by metals of staphylopine dehydrogenase activity during metallophore biosynthesis. Journal of the American Chemical Society, 141, 5555-5562.
Hannauer, M., Braud, A., Hoegy, F., Ronot, P., Boos, A. and Schalk, I.J. (2012) The PvdRT-OpmQ efflux pump controls the metal selectivity of the iron uptake pathway mediated by the siderophore pyoverdine in Pseudomonas aeruginosa. Environmental Microbiology, 14, 1696-1708.
Hermansen, G.M.M., Hansen, M.L., Khademi, S.M.H. and Jelsbak, L. (2018) Intergenic evolution during host adaptation increases expression of the metallophore pseudopaline in Pseudomonas aeruginosa. Microbiology, 164, 1038-1047.
Hirakata, Y., Srikumar, R., Poole, K., Gotoh, N., Suematsu, T., Kohno, S., et al. (2002) Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. Journal of Experimental Medicine, 196, 109-118.
Hood, M.I. and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nature Reviews Microbiology, 10, 525-537.
Horiyama, T. and Nishino, K. (2014) AcrB, AcrD, and MdtABC multidrug efflux systems are involved in enterobactin export in Escherichia coli. PLoS ONE, 9, e108642.
Imperi, F., Tiburzi, F. and Visca, P. (2009) Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A, 106, 20440-20445.
Jeong, J.Y., Yim, H.S., Ryu, J.Y., Lee, H.S., Lee, J.H., Seen, D.S., et al. (2012) One-step sequence- and ligation-independent cloning as a rapid and versatile cloning method for functional genomics studies. Applied and Environment Microbiology, 78, 5440-5443.
Johnstone, T.C. and Nolan, E.M. (2015) Beyond iron: Non-classical biological functions of bacterial siderophores. Dalton Transactions, 44, 6320-6339.
Kaniga, K., Delor, I. and Cornelis, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene, 109, 137-141.
Kessler, E. and Safrin, M. (2014) Elastinolytic and proteolytic enzymes. Methods in Molecular Biology, 1149, 135-169.
Laffont, C., Brutesco, C., Hajjar, C., Cullia, G., Fanelli, R., Ouerdane, L., et al. (2019) Simple rules govern the diversity of bacterial nicotianamine-like metallophores. The Biochemical Journal, 476, 2221-2233.
Lhospice, S., Gomez, N.O., Ouerdane, L., Brutesco, C., Ghssein, G., Hajjar, C., et al. (2017) Pseudomonas aeruginosa zinc uptake in chelating environment is primarily mediated by the metallophore pseudopaline. Scientific Reports, 7, 17132.
Li, X.Z., Plesiat, P. and Nikaido, H. (2015) The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clinical Microbiology Reviews, 28, 337-418.
Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., et al. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proceedings of the National Academy of Sciences USA, 103, 2833-2838.
Mastropasqua, M.C., D'Orazio, M., Cerasi, M., Pacello, F., Gismondi, A., Canini, A., et al. (2017) Growth of Pseudomonas aeruginosa in zinc poor environments is promoted by a nicotianamine-related metallophore. Molecular Microbiology, 106, 543-561.
McFarlane, J.S., Davis, C.L., and Lamb, A.L. (2018) Staphylopine, pseudopaline, and yersinopine dehydrogenases: A structural and kinetic analysis of a new functional class of opine dehydrogenase. Journal of Biological Chemistry, 293, 8009-8019.
McFarlane, J.S. and Lamb, A.L. (2017) Biosynthesis of an opine metallophore by Pseudomonas aeruginosa. Biochemistry, 56, 5967-5971.
Nguyen, A.T. and Oglesby-Sherrouse, A.G. (2015) Spoils of war: Iron at the crux of clinical and ecological fitness of Pseudomonas aeruginosa. BioMetals, 28, 433-443.
Palmer, K.L., Mashburn, L.M., Singh, P.K. and Whiteley, M. (2005) Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. Journal of Bacteriology, 187, 5267-5277.
Pearson, J.P., Van Delden, C. and Iglewski, B.H. (1999) Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. Journal of Bacteriology, 181, 1203-1210.
Pederick, V.G., Eijkelkamp, B.A., Begg, S.L., Ween, M.P., McAllister, L.J., Paton, J.C., et al. (2015) ZnuA and zinc homeostasis in Pseudomonas aeruginosa. Scientific Reports, 5, 13139.
Poole, K. (2005) Efflux-mediated antimicrobial resistance. Journal of Antimicrobial Chemotherapy, 56, 20-51.
Ramaswamy, V.K., Vargiu, A.V., Malloci, G., Dreier, J. and Ruggerone, P. (2018) Molecular determinants of the promiscuity of MexB and MexY multidrug transporters of Pseudomonas aeruginosa. Frontiers in Microbiology, 9, 1144.
Ramos, J.L., Duque, E., Gallegos, M.T., Godoy, P., Ramos-Gonzalez, M.I., Rojas, A., et al. (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annual Review of Microbiology, 56, 743-768.
Richardot, C., Plesiat, P., Fournier, D., Monlezun, L., Broutin, I. and Llanes, C. (2015) Carbapenem resistance in cystic fibrosis strains of Pseudomonas aeruginosa as a result of amino acid substitutions in porin OprD. International Journal of Antimicrobial Agents, 45, 529-532.
Robinson, A.E., Lowe, J.E., Koh, E.I. and Henderson, J.P. (2018) Uropathogenic enterobacteria use the yersiniabactin metallophore system to acquire nickel. Journal of Biological Chemistry, 293, 14953-14961.
Schalk, I.J. and Cunrath, O. (2016) An overview of the biological metal uptake pathways in Pseudomonas aeruginosa. Environmental Microbiology, 18, 3227-3246.
Shafer, W.M., Balthazar, J.T., Hagman, K.E. and Morse, S.A. (1995) Missense mutations that alter the DNA-binding domain of the MtrR protein occur frequently in rectal isolates of Neisseria gonorrhoeae that are resistant to faecal lipids. Microbiology, 141(Pt 4), 907-911.
Son, M.S., Matthews, W.J. Jr, Kang, Y., Nguyen, D.T. and Hoang, T.T. (2007) In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infection and Immunity, 75, 5313-5324.
Tetard, A., Zedet, A., Girard, C., Plesiat, P. and Llanes, C. (2019) Cinnamaldehyde induces expression of efflux pumps and multidrug resistance in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy, 63(10), e01081-e1119.
Thanassi, D.G., Cheng, L.W. and Nikaido, H. (1997) Active efflux of bile salts by Escherichia coli. Journal of Bacteriology, 179, 2512-2518.
Tsutsumi, K., Yonehara, R., Ishizaka-Ikeda, E., Miyazaki, N., Maeda, S., Iwasaki, K.. et al. (2019) Structures of the wild-type MexAB-OprM tripartite pump reveal its complex formation and drug efflux mechanism. Nature Communications, 10, 1520.
Vega, D.E. and Young, K.D. (2014) Accumulation of periplasmic enterobactin impairs the growth and morphology of Escherichia coli tolC mutants. Molecular Microbiology, 91, 508-521.
Weinberg, E.D. (1975) Nutritional immunity. Host’s attempt to withold iron from microbial invaders. JAMA, 231, 39-41.
Yeterian, E., Martin, L.W., Guillon, L., Journet, L., Lamont, I.L. and Schalk, I.J. (2010) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation. Amino Acids, 38, 1447-1459.
Zhang, J., Zhao, T., Yang, R., Siridechakorn, I., Wang, S., Guo, Q., et al. (2019) De novo synthesis, structural assignment and biological evaluation of pseudopaline, a metallophore produced by Pseudomonas aeruginosa. Chem Sci, 10, 6635-6641.