Fatty acid hydrolysis of acyl marinobactin siderophores by Marinobacter acylases

Biochemistry

Volumn 54, Issue 3, 2015, Pages 744-752

  Kem, Michelle P ^a   Naka, Hiroaki ^b   Iinishi, Akira ^a,c   Haygood, Margo G ^b   Butler, Alison ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c ROHTO Pharmaceutical Co Ltd   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; GENES; HYDROLYSIS; IRON;

ACID HYDROLYSIS; AMINO ACID SEQUENCE; CHEMICAL EQUATIONS; HOMOSERINE LACTONES; LIMITING CONDITION; MARINE BACTERIUM; PSEUDOMONAS AERUGINOSA; SIGNALING MOLECULES;

FATTY ACIDS;

AMIDASE; FATTY ACID; FERRIC ION; SIDEROPHORE; APOPROTEIN; BACTERIAL PROTEIN; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; IRON; OLIGOPEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DELETION MUTANT; ELECTROSPRAY MASS SPECTROMETRY; ENVIRONMENTAL TEMPERATURE; ESCHERICHIA COLI; HETEROLOGOUS EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; MARINOBACTER; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RALSTONIA SOLANACEARUM; ACYLATION; ANALOGS AND DERIVATIVES; CHEMISTRY; ENZYMOLOGY; GENE INACTIVATION; GENETICS; METABOLISM; MUTATION; REVERSED PHASE LIQUID CHROMATOGRAPHY;

MARINOBACTER; MARINOBACTER SP.; PSEUDOMONAS AERUGINOSA;

4-BUTYROLACTONE; ACYLATION; AMIDOHYDROLASES; APOPROTEINS; BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, REVERSE-PHASE; FATTY ACIDS; GENE KNOCKOUT TECHNIQUES; HYDROLYSIS; IRON; MARINOBACTER; MUTATION; OLIGOPEPTIDES; SIDEROPHORES;

EID: 84921879636     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5013673     Document Type: Article

References (50)

1. Martinez, J., Carter-Franklin, J., Mann, E., Martin, J., Haygood, M., and Butler, A. (2003) Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium Proc. Natl. Acad. Sci. U.S.A. 100, 3754-3759
2. Homann, V., Sandy, M., Tincu, J., Templeton, A., Tebo, B., and Butler, A. (2009) Loihichelins A-F, a Suite of Amphiphilic Siderophores Produced by the Marine Bacterium Halomonas LOB-5 J. Nat. Prod. 72, 884-888
3. Vraspir, J., Holt, P., and Butler, A. (2011) Identification of new members within suites of amphiphilic marine siderophores BioMetals 24, 85-92
4. Martinez, J., Zhang, G., Holt, P., Jung, H., Carrano, C., Haygood, M., and Butler, A. (2000) Self-assembling amphiphilic siderophores from marine bacteria Science 287, 1245-1247
5. Martinez, J. and Butler, A. (2007) Marine amphiphilic siderophores: Marinobactin structure, uptake, and microbial partitioning J. Inorg. Biochem. 101, 1692-1698
6. Zane, H., Naka, H., Rosconi, F., Sandy, M., Haygood, M., and Butler, A. (2014) Biosynthesis of Amphi-enterobactin Siderophores by Vibrio harveyi BAA-1116: Identification of a Bifunctional Nonribosomal Peptide Synthetase Condensation Domain J. Am. Chem. Soc. 136, 5615-5618
7. Gauglitz, J. and Butler, A. (2013) Amino acid variability in the peptide composition of a suite of amphiphilic peptide siderophores from an open ocean Vibrio species JBIC, J. Biol. Inorg. Chem. 18, 489-497
8. Ratledge, C. (2004) Iron, mycobacteria and tuberculosis Tuberculosis 84, 110-130
9. Kreutzer, M., Kage, H., and Nett, M. (2012) Structure and Biosynthetic Assembly of Cupriachelin, a Photoreactive Siderophore from the Bioplastic Producer Cupriavidus necator H16 J. Am. Chem. Soc. 134, 5415-5422
10. Rosconi, F., Davyt, D., Martinez, V., Martinez, M., Abin-Carriquiry, J., Zane, H., Butler, A., de Souza, E., and Fabiano, E. (2013) Identification and structural characterization of serobactins, a suite of lipopeptide siderophores produced by the grass endophyte Herbaspirillum seropedicae Environ. Microbiol. 15, 916-927
11. Kreutzer, M. and Nett, M. (2012) Genomics-driven discovery of taiwachelin, a lipopeptide siderophore from Cupriavidus taiwanensis Org. Biomol. Chem. 10, 9338-9343
12. Yeterian, E., Martin, L., Guillon, L., Journet, L., Lamont, I., and Schalk, I. (2010) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation Amino Acids 38, 1447-1459
13. Jimenez, P., Koch, G., Papaioannou, E., Wahjudi, M., Krzeslak, J., Coenye, T., Cool, R., and Quax, W. (2010) Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions Microbiology 156, 49-59
14. Bokhove, M., Jimenez, P., Quax, W., and Dijkstra, B. (2010) The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket Proc. Natl. Acad. Sci. U.S.A. 107, 686-691
15. Wahjudi, M., Papaioannou, E., Hendrawati, O., van Assen, A., van Merkerk, R., Cool, R., Poelarends, G., and Ouax, W. (2011) PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily Microbiology 157, 2042-2055
16. Drake, E. and Gulick, A. (2011) Structural Characterization and High-Throughput Screening of Inhibitors of PvdQ, an NTN Hydrolase Involved in Pyoverdine Synthesis ACS Chem. Biol. 6, 1277-1286
17. Hannauer, M., Schafer, M., Hoegy, F., Gizzi, P., Wehrung, P., Mislin, G., Budzikiewicz, H., and Schalk, I. (2012) Biosynthesis of the pyoverdine siderophore of Pseudomonas aeruginosa involves precursors with a myristic or a myristoleic acid chain FEBS Lett. 586, 96-101
18. Koch, G., Jimenez, P., Muntendam, R., Chen, Y., Papaioannou, E., Heeb, S., Camara, M., Williams, P., Cool, R., and Quax, W. (2010) The acylase PvdQ has a conserved function among fluorescent Pseudomonas spp Environ. Microbiol. Rep. 2, 433-439
19. Romero, M., Diggle, S., Heeb, S., Camara, M., and Otero, A. (2008) Quorum quenching activity in Anabaena sp. PCC 7120: Identification of AiiC, a novel AHL-acylase FEMS Microbiol. Lett. 280, 73-80
20. Huang, J., Petersen, A., Whiteley, M., and Leadbetter, J. (2006) Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1 Appl. Environ. Microbiol. 72, 1190-1197
21. Park, S., Kang, H., Jang, H., Lee, J., Koo, B., and Yum, D. (2005) Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching Appl. Environ. Microbiol. 71, 2632-2641
22. Lin, Y., Xu, J., Hu, J., Wang, L., Ong, S., Leadbetter, J., and Zhang, L. (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes Mol. Microbiol. 47, 849-860
23. Miller, M. and Bassler, B. (2001) Quorum sensing in bacteria Annu. Rev. Microbiol. 55, 165-199
24. Sio, C., Otten, L., Cool, R., Diggle, S., Braun, P., Bos, R., Daykin, M., Camara, M., Williams, P., and Quax, W. (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1 Infect. Immun. 74, 1673-1682
25. Schaefer, A., Taylor, T., Beatty, J., and Greenberg, E. (2002) Long-chain acyl-homoserine lactone quorum-sensing regulation of Rhodobacter capsulatus gene transfer agent production J. Bacteriol. 184, 6515-6521
26. Wurst, J., Drake, E., Theriault, J., Jewett, I., VerPlank, L., Perez, J., Dandapani, S., Palmer, M., Moskowitz, S., Schreiber, S., Munoz, B., and Gulick, A. (2014) Identification of Inhibitors of PvdQ, an Enzyme Involved in the Synthesis of the Siderophore Pyoverdine ACS Chem. Biol. 9, 1536-1544
27. Clevenger, K., Wu, R., Er, J., Liu, D., and Fast, W. (2013) Rational Design of a Transition State Analogue with Picomolar Affinity for Pseudomonas aeruginosa PvdQ, a Siderophore Biosynthetic Enzyme ACS Chem. Biol. 8, 2192-2200
28. Gauglitz, J., Inishi, A., Ito, Y., and Butler, A. (2014) Microbial Tailoring of Acyl Peptidic Siderophores Biochemistry 53, 2624-2631
29. Gao, W., Cui, Z., Li, Q., Xu, G., Jia, X., and Zheng, L. (2013) Marinobacter nanhaiticus sp nov., polycyclic aromatic hydrocarbon-degrading bacterium isolated from the sediment of the South China Sea Antonie Van Leeuwenhoek 103, 485-491
30. Bachmann, B., Ravel, J., and Hopwood, D. (2009) Methods for In Silico Prediction of Microbial Polyketide and Nonribosomal Peptide Biosynthetic Pathways from DNA Sequence Data. In Complex Enzymes in Microbial Natural Product Biosynthesis, Part a: Overview Articles and Peptides, Vol. 458, pp 181-217, Academic Press, New York.
31. Rose, T., Henikoff, J., and Henikoff, S. (2003) CODEHOP (COnsensus-DEgenerate hybrid oligonucleotide primer) PCR primer design Nucleic Acids Res. 31, 3763-3766
32. Korbie, D. and Mattick, J. (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification Nat. Protoc. 3, 1452-1456
33. Senanayake, S. and Brian, D. (1995) Precise large deletions by the PCR-based overlap extension method Mol. Biotechnol. 4, 13-15
34. Milton, D., OToole, R., Horstedt, P., and WolfWatz, H. (1996) Flagellin A is essential for the virulence of Vibrio anguillarum J. Bacteriol. 178, 1310-1319
35. Steinmetz, M. and Richter, R. (1994) Plasmids designed to alter the antibiotic-resistance expressed by insertion mutations in Bacillus subtilis, through in vivo recombination Gene 142, 79-83
36. Morales, V., Backman, A., and Bagdasarian, M. (1991) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants Gene 97, 39-47
37. Oinonen, C. and Rouvinen, J. (2000) Structural comparison of Ntn-hydrolases Protein Sci. 9, 2329-2337
38. Clevenger, K., Wu, R., Liu, D., and Fast, W. (2014) n-Alkylboronic Acid Inhibitors Reveal Determinants of Ligand Specificity in the Quorum-Quenching and Siderophore Biosynthetic Enzyme PvdQ Biochemistry 53, 6679-6686
39. Brannigan, J., Dodson, G., Duggleby, H., Moody, P., Smith, J., Tomchick, D., and Murzin, A. (1995) A protein catalytic framework with an N-terminal nucleophile is capable of self-activation Nature 378, 416-419
40. Shepherd, R. and Lindow, S. (2009) Two Dissimilar N-Acyl-Homoserine Lactone Acylases of Pseudomonas syringae Influence Colony and Biofilm Morphology Appl. Environ. Microbiol. 75, 45-53
41. Crosa, J. and Walsh, C. (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria Microbiol. Mol. Biol. Rev. 66, 223-249
42. Schalk, I. and Guillon, L. (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: Implications for metal homeostasis Environ. Microbiol. 15, 1661-1673
43. Rausch, C., Hoof, I., Weber, T., Wohlleben, W., and Huson, D. (2007) Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution BMC Evol. Biol. 7
44. Patricelli, M. and Cravatt, B. (2001) Characterization and manipulation of the acyl chain selectivity of fatty acid amide hydrolase Biochemistry 40, 6107-6115
45. Chen, C., Chen, C., Liao, C., and Lee, C. (2009) A probable aculeacin A acylase from the Ralstonia solanacearum GMI1000 is N-acyl-homoserine lactone acylase with quorum-quenching activity BMC Microbiol. 9
46. Xu, G., Martinez, J., Groves, J., and Butler, A. (2002) Membrane affinity of the amphiphilic marinobactin siderophores J. Am. Chem. Soc. 124, 13408-13415
47. Hanzelka, B., Parsek, M., Val, D., Dunlap, P., Cronan, J., and Greenberg, E. (1999) Acylhomoserine lactone synthase activity of the Vibrio fischeri AinS protein J. Bacteriol. 181, 5766-5770
48. Laue, R., Jiang, Y., Chhabra, S., Jacob, S., Stewart, G., Hardman, A., Downie, J., O'Gara, F., and Williams, P. (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase Microbiology 146, 2469-2480
49. Ng, W. and Bassler, B. (2009) Bacterial Quorum-Sensing Network Architectures Annu. Rev. Genet. 43, 197-222
50. Duran, R. (2010) Marinobacter. In Handbook of hydrocarbon and lipid microbiology (Timmis, K. N., Ed.) pp 1726-1735, Springer, Berlin.