HqiA, a novel quorum-quenching enzyme which expands the AHL lactonase family

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Torres, Marta ^a,b   Uroz, Stéphane ^c   Salto, Rafael ^a   Fauchery, Laure ^c   Quesada, Emilia ^a,b   Llamas, Inmaculada ^a,b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOXYLESTERASE; N-ACYL HOMOSERINE LACTONASE;

DELTAPROTEOBACTERIA; DNA SEQUENCE; ENZYMOLOGY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HORIZONTAL GENE TRANSFER; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; METAGENOMICS; MICROBIOLOGY; MULTIGENE FAMILY; OPEN READING FRAME; PECTOBACTERIUM CAROTOVORUM; PHYSIOLOGY; PROCEDURES; QUORUM SENSING; SPAIN;

BACTERIAL PROTEINS; CARBOXYLIC ESTER HYDROLASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DELTAPROTEOBACTERIA; GENE TRANSFER, HORIZONTAL; MASS SPECTROMETRY; METAGENOMICS; MULTIGENE FAMILY; OPEN READING FRAMES; PECTOBACTERIUM CAROTOVORUM; QUORUM SENSING; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SPAIN;

EID: 85018386844     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-01176-7     Document Type: Article

References (94)

1. Hornby, J. M. et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67, 2982-2992 (2001).
2. Fuqua, W. C., Winans, S. C. & Greenberg, E. P. Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176, 269-275 (1994).
3. Whitehead, N. A., Barnard, A. M. L., Slater, H., Simpson, N. J. L. & Salmond, G. P. C. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25, 365-404 (2001).
4. Williams, P., Winzer, K., Chan, W. C. & Cámara, M. Look whos talking: communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362, 1119-1134 (2007).
5. Uroz, S., Dessaux, Y. & Oger, P. Quorum sensing and quorum quenching: The yin and yang of bacterial communication. ChemBioChem 10, 205-216 (2009).
6. González, J. E. & Keshavan, N. D. Messing with bacterial quorum sensing. Microbiol. Mol. Biol. Rev. 70, 859-875 (2006).
7. González, J. E. & Marketon, M. M. Quorum sensing in nitrogen-fixing Rhizobia. Microbiol. Mol. Biol. Rev. 67, 574-592 (2003).
8. Hao, Y., Winans, S. C., Glick, B. R. & Charles, T. C. Identification and characterization of new LuxR/LuxI-Type quorum sensing systems from metagenomic libraries. Environ. Microbiol. 12, 105-117 (2010).
9. Nasuno, E. et al. Phylogenetically novel LuxI/LuxR-Type quorum sensing systems isolated using a metagenomic approach. Appl. Environ. Microbiol. 78, 8067-8074 (2012).
10. Llamas, I. et al. Quorum sensing in halophilic bacteria: detection of N-Acyl-homoserine lactones in the exopolysaccharideproducing species of Halomonas. Extremophiles 9, 333-341 (2005).
11. Tahrioui, A., Schwab, M., Quesada, E. & Llamas, I. Quorum sensing in some representative species of Halomonadaceae. Life 3, 260-275 (2013).
12. Uroz, S. et al. Novel bacteria degrading N-Acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149, 1981-1989 (2003).
13. Kalia, V. C. & Purohit, H. J. Quenching the quorum sensing system: potential antibacterial drug targets. Crit. Rev. Microbiol. 37, 121-140 (2011).
14. Rasmussen, T. B. et al. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151, 1325-1340 (2016).
15. Uroz, S. & Heinonsalo, J. Degradation of N-Acyl homoserine lactone quorum sensing signal molecules by forest root-Associated fungi. FEMS Microbiol. Ecol. 65, 271-278 (2008).
16. Dong, Y. & Zhang, L. Quorum sensing and quorum-quenching enzymes. J. Microbiol. 43, 101-109 (2005).
17. Teplitski, M., Robinson, J. B. & Bauer, W. D. Plants secrete substances that mimic bacterial N-Acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact. 13, 637-648 (2000).
18. Givskov, M. et al. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bact. 178, 6618-6622 (1996).
19. Manefield, M. et al. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145, 283-291 (1999).
20. Park, S. et al. Identification of extracellular N-Acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71, 2632-2641 (2005).
21. Uroz, S. et al. N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151, 3313-3322 (2005).
22. Uroz, S. et al. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl. Environ. Microbiol. 74, 1357-1366 (2008).
23. Dong, Y., Gusti, A., Zhang, Q., Xu, J. & Zhang, L. Identification of quorum-quenching N-Acyl homoserine lactonases from Bacillus species. Appli. Environ. Microbiol. 68, 1754-1759 (2002).
24. Romero, M., Avendaño-Herrera, R., Magariños, B., Cámara, M. & Otero, A. Acylhomoserine lactone production and degradation by the fish pathogen Tenacibaculum maritimum, a member of the Cytophaga-Flavobacterium-Bacteroidetes (CFB) group. FEMS Microbiol. Lett. 304, 131-139 (2010).
25. Romero, M., Diggle, S. P., Heeb, S., Cámara, M. & Otero, A. Quorum quenching activity in Anabaena sp. PCC 7120: identification of AiiC, a novel AHL-Acylase. FEMS Microbiol. Lett. 280, 73-80 (2008).
26. Romero, M., Martin-Cuadrado, A. B., Roca-Rivada, A., Cabello, A. M. & Otero, A. Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol. Ecol. 75, 205-217 (2011).
27. Mayer, C., Romero, M., Muras, A. & Otero, A. Aii20J, a wide-spectrum thermostable N-Acylhomoserine lactonase from the marine bacterium Tenacibaculum sp. 20J, can quench AHL-mediated acid resistance in Escherichia coli. Appl. Microbiol. Biotechnol. 99, 9523-9539 (2015).
28. Bijtenhoorn, P. et al. BpiB05, a novel metagenome-derived hydrolase acting on N-Acylhomoserine lactones. J. Biotechnol. 155, 86-94 (2011).
29. Romero, M., Martin-Cuadrado, A. & Otero, A. Determination of whether quorum quenching is a common activity in marine bacteria by analysis of cultivable bacteria and metagenomic sequences. Appl. Environ. Microbiol. 78, 6345-6348 (2012).
30. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858 (2015).
31. Cui, X. & Harling, R. N-Acyl-homoserine lactone-mediated quorum sensing blockage, a novel strategy for attenuating pathogenicity of Gram-negative bacterial plant pathogens. Eur. J. Plant Pathol. 111, 327-339 (2005).
32. Pirhonen, M., Flego, D., Heikinheimo, R. & Palva, E. T. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 12, 2467-2476 (1993).
33. Chatterjee, A., Cui, Y., Chakrabarty, P. & Chatterjee, A. K. Regulation of motility in Erwinia carotovora subsp. carotovora: quorumsensing signal controls FlhDC, the global regulator of flagellar and exoprotein genes, by modulating the production of RsmA, an RNA-binding protein. Mol. Plant. Microbe. Interact. 23, 1316-1323 (2010).
34. Grandclément, C., Tannières, M., Moréra, S., Dessaux, Y. & Faure, D. Quorum quenching: role in nature and applied developments. FEMS Microbiol. Rev. 40, 86-116 (2015).
35. Montgomery, K., Charlesworth, J. C., LeBard, R., Visscher, P. T. & Burns, B. P. Quorum sensing in extreme environments. Life 3, 131-148 (2013).
36. Farah, C. et al. Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl. Environ. Microbiol. 71, 7033-7040 (2005).
37. Williamson, L. L. et al. Intracellular screen to identify metagenomic clones that induce or inhibit a quorum-sensing biosensor. Appl. Environ. Microbiol. 71, 6335-6344 (2005).
38. Nichols, D. Cultivation gives context to the microbial ecologist. FEMS Microbiol. Ecol. 60, 351-357 (2007).
39. DAngelo-Picard, C., Faure, D., Penot, I. & Dessaux, Y. Diversity of N-Acyl homoserine lactone-producing and-degrading bacteria in soil and tobacco rhizosphere. Environ. Microbiol. 7, 1796-1808 (2005).
40. Case, R. J., Labbate, M. & Kjelleberg, S. AHL-driven quorum-sensing circuits: Their frequency and function among the Proteobacteria. ISME J. 2, 345-349 (2008).
41. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, 398-431 (2007).
42. Riaz, K. et al. A metagenomic analysis of soil bacteria extends the diversity of quorum-quenching lactonases. Environ. Microbiol. 10, 560-570 (2008).
43. Afriat, L., Roodveldt, C., Manco, G. & Tawfik, D. S. The latent promiscuity of newly identified microbial lactonases is linked to recently diverged phosphotriesterase. Biochemistry 45, 13677-13686 (2006).
44. Schipper, C. et al. Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75, 224-233 (2009).
45. Tannières, M. et al. A metagenomic study highlights phylogenetic proximity of quorum-quenching and xenobiotic-degrading amidases of the AS-family. PLoS One 8, e65473 (2013).
46. Uchiyama, T. & Miyazaki, K. Functional metagenomics for enzyme discovery: challenges to efficient screening. Curr. Opin. Biotechnol. 20, 616-622 (2009).
47. Carlier, A. et al. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-Acyl homoserine lactonase activity. Appl. Environ. Microbiol. 69, 4989-4993 (2003).
48. Mei, G., Yan, X., Turak, A., Luo, Z. & Zhang, L. AidH, an alpha/beta-hydrolase fold family member from an Ochrobactrum sp. strain, is a novel N-Acylhomoserine lactonase. Appl. Environ. Microbiol. 76, 4933-4942 (2010).
49. Liu, D. et al. Three-dimensional structure of the quorum-quenching N-Acyl homoserine lactone hydrolase from Bacillus thuringiensis. Proc. Natl. Acad. Sci. 102, 11882-11887 (2005).
50. Zhang, X. H., Wang, L. & Zhang, L. H. Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. 99, 4638-4643 (2002).
51. Chan, K. et al. Characterization of N-Acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol. 11, 51 (2011).
52. Parsons, J. F., Calabrese, K., Eisenstein, E. & Ladner, J. E. Structure and mechanism of Pseudomonas aeruginosa PhzD, an isochorismatase from the phenazine biosynthetic pathway. Biochemistry 42, 5684-5693 (2003).
53. Bokhove, M., Nadal Jimenez, P., Quax, W. J. & Dijkstra, B. W. The quorum-quenching N-Acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket. Proc. Natl. Acad. Sci. 107, 686-691 (2010).
54. Huang, J. J., Petersen, A., Whiteley, M. & Leadbetter, J. R. Identification of QuiP, the product of gene PA1032, as the second acylhomoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 72, 1190-1197 (2006).
55. Wahjudi, M. et al. PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily. Microbiology 157, 2042-2055 (2011).
56. Ollivier, B., Caumette, P., Garcia, J. L. & Mah, R. A. Anaerobic bacteria from hypersaline environments. Microbiol. Rev. 58, 27-38 (1994).
57. Foti, M. et al. Diversity, activity and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl. Environ. Microbiol. 73, 2093-2100 (2007).
58. Scharf, B. E., Hynes, M. F. & Alexandre, G. M. Chemotaxis signaling systems in model beneficial plant-bacteria associations. Plant Mol. Biol. 90, 549-559 (2016).
59. Sourjik, V., Muschler, P., Scharf, B. & Schmitt, R. VisN and VisR are global regulators of chemotaxis, flagellar and motility genes in Sinorhizobium (Rhizobium) meliloti. J. Bacteriol. 182, 782-788 (2000).
60. Hoang, H. H., Gurich, N. & González, J. E. Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J. Bacteriol. 190, 861-871 (2008).
61. Parnell, J. et al. Functional biogeography as evidence of gene transfer in hypersaline microbial communities. PLoS One 5, e12919 (2010).
62. Rhodes, M. E., Spear, J. R., Oren, A. & House, C. H. Differences in lateral gene transfer in hypersaline versus thermal environments. BMC Evol. Biol. 11, 199 (2011).
63. Mongodin, E. et al. The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc. Natl. Acad. Sci. 102, 18147-18152 (2005).
64. Smadja, B. et al. Involvement of N-Acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Mol. Plant. Microbe. Interact. 17, 1269-1278 (2004).
65. Dong, Y. H., Xu, J. L., Li, X. Z. & Zhang, L. H. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. 97, 3526-3531 (2000).
66. Oueriaghli, N., Béjar, V., Quesada, E. & Martínez-Checa, F. Molecular ecology techniques reveal both spatial and temporal variations in the diversity of archaeal communities within the athalassohaline environment of Rambla Salada, Spain. Microb. Ecol. 66, 297-311 (2013).
67. Parkinson, J. S. CheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J. Bacteriol 126, 758-770 (1976).
68. Parkinson, J. S. Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J. Bacteriol. 135, 45-53 (1978).
69. McClean, K. H. et al. Quorum sensing and Chromobacteriurn violaceum: exploitation of violacein production and inhibition for the detection of N-Acyl homoserine lactones. Microbiology 143, 3703-3711 (1997).
70. Morohoshi, T., Kato, M., Fukamachi, K., Kato, N. & Ikeda, T. N-Acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC 12472. FEMS Microbiol. Lett. 279, 124-130 (2008).
71. Chilton, M. D. et al. Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc. Natl. Acad. Sci. 71, 3672-3676 (1974).
72. Yates, E. A. et al. N-Acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 70, 5635-5646 (2002).
73. Uroz, S. & Oger, P. M. In Metagenomics: Methods and Protocols (eds Streit, W. & Rolf, D.) 271-286 (Springer, 2017).
74. Torres, M. et al. Selection of the N-Acylhomoserine lactone-degrading bacterium Alteromonas stellipolaris PQQ-42 and of its potential for biocontrol in aquaculture. Front. Microbiol. 7, 646 (2016).
75. Marketon, M. M. & Gonzalez, M. M. Identication of two quorum-sensing systems in Sinorhizobium meliloti. Society 184, 3466-3475 (2002).
76. Ortori, C. A. et al. Comprehensive profiling of N-Acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole-linear ion trap mass spectrometry. Anal. Bioanal. Chem. 387, 497-511 (2007).
77. Milton, D. L. et al. The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl) homoserine lactone and N-hexanoylhomoserine lactone. J. Bacteriol. 183, 3537-3547 (2001).
78. Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, 206-214 (2014).
79. Besemer, J. & Borodovsky, M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res. 33, 451-454 (2005).
80. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
81. Gao, F. & Zhang, C. GC-Profile: A web-based tool for visualizing and analyzing the variation of GC content in genomic sequences. Nucleic Acids Res. 34, 686-691 (2006).
82. Gouy, M., Guindon, S. & Gascuel, O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221-224 (2010).
83. Sievers, F. & Higgins, D. Clustal Omega, accurate alignment of very large numbers of sequences. Methods Mol. Biol. 1079, 105-116 (2014).
84. Heeb, S. et al. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-Associated bacteria. Mol. Plant. Microbe. Interact. 13, 232-237 (2000).
85. Parks, T., Leuther, K., Howard, E., Johnston, S. & Dougherty, W. Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem. 216, 413-417 (1994).
86. Bradford, M. M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem 72, 248-254 (1976).
87. Sambrook, J. & Russell, D. Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor Laboratory Press, 2001).
88. Barrow, G. I. & Feltham, R. K. A. Cowan and Steels Manual for the Identification of Medical Bacteria (eds Barrow, G. I. & Feltham, R. K. A.) (Cambridge University Press, 1993).
89. Jeffries, C. D., Holtmian, D. F. & Guse, D. G. Rapid method for determining the activity of microorganisms on nucleic acids. J. Bacteriol. 73, 590-591 (1957).
90. Rui, H., Liu, Q., Ma, Y., Wang, Q. & Zhang, Y. Roles of LuxR in regulating extracellular alkaline serine protease A, extracellular polysaccharide and mobility of Vibrio alginolyticus. FEMS Microbiol. Lett. 285, 155-162 (2008).
91. OMay, C. & Tufenkji, N. The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials. Appl. Environ. Microbiol. 77, 3061-3067 (2011).
92. Banakar, S. P. & Thippeswamy, B. Isolation, production and partial purification of fungal extracellular pectinolytic enzymes from the forest soils of Bhadra wildlife sanctuary. J. Biochem. Tech. 3, 138-143 (2012).
93. Pikovskaya, R. I. Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17, 362-370 (1948).
94. Rasband, W. ImageJ. US National Institutes of Health, Bethesda, Maryland, USA. http://imagej.nih.gov/ij (2012).