Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors

Nature

Volumn 496, Issue 7446, 2013, Pages 508-512

  Russell, Alistair B ^a   Leroux, Michele ^a   Hathazi, Krisztina ^b   Agnello, Danielle M ^a   Ishikawa, Takahiko ^b   Wiggins, Paul A ^a,c   Wai, Sun Nyunt ^b   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UMEÅ UNIVERSITY   (Sweden)

^c University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CYTOPLASM PROTEIN; MALTOSE BINDING PROTEIN; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPASE; PHOSPHOLIPASE D; PROPIDIUM IODIDE; VENOM;

ANTAGONISM; ENZYME; EUKARYOTE; EVOLUTION; INFECTIOUS DISEASE; MEMBRANE; MICROBIAL COMMUNITY; PATHOGEN; SECRETION; SUBSTRATE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CONVERGENT EVOLUTION; DEPOLARIZATION; ENZYME ACTIVITY; HOST CELL; LIPID VESICLE; MAMMAL CELL; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; TYPE VI SECRETION SYSTEM;

ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; EVOLUTION, MOLECULAR; PHOSPHATIDYLETHANOLAMINES; PHOSPHOLIPASE D; PHYLOGENY; PSEUDOMONAS AERUGINOSA; SPECIES SPECIFICITY; SUBSTRATE SPECIFICITY; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); EUKARYOTA; HEXAPODA; PSEUDOMONAS AERUGINOSA; REPTILIA;

EID: 84876798141     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12074     Document Type: Article

References (48)

1. Aloulou, A., Ali, Y. B., Bezzine, S., Gargouri, Y. & Gelb, M. H. Phospholipases: an overview. Methods Mol. Biol. 861, 63-85 (2012).
2. Schmiel, D. H. & Miller, V. L. Bacterial phospholipases and pathogenesis. Microbes Infect. 1, 1103-1112 (1999).
3. Wilderman, P. J., Vasil, A. I., Johnson, Z. & Vasil, M. L. Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol. Microbiol. 39, 291-304 (2001).
4. Lesic, B., Starkey, M., He, J., Hazan, R. & Rahme, L. G. Quorumsensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155, 2845-2855 (2009).
5. Sana, T. G. et al. The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J. Biol. Chem. 287, 27095-27105 (2012).
6. Barret, M., Egan, F., Fargier, E., Morrissey, J. P. & O'Gara, F. Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology 157, 1726-1739 (2011).
7. Silverman, J. M., Brunet, Y. R., Cascales, E. & Mougous, J. D. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453-472 (2012).
8. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D.& Mekalanos, J. J. Type VI secretion systemtranslocates a phage tail spike-like protein into target cells where it crosslinks actin. Proc. Natl Acad. Sci. USA 104, 15508-15513 (2007).
9. Russell, A. B. et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347 (2011).
10. Russell, A. B. et al. A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11, 538-549 (2012).
11. Dong, T. G., Ho, B. T., Yoder-Himes, D. R. & Mekalanos, J. J. Identification of T6SSdependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc. Natl Acad. Sci. USA 110, 2623-2628 (2013).
12. Ishikawa, T. et al. Pathoadaptive conditional regulation of the type VI secretion system in Vibrio cholerae O1 strains. Infect. Immun. 80, 575-584 (2012).
13. LeRoux, M. et al. Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc. Natl Acad. Sci. USA 109, 19804-19809 (2012).
14. Mougous, J. D. et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530 (2006).
15. Stace, C. L. & Ktistakis, N. T. Phosphatidic acid-and phosphatidylserine-binding proteins. Biochim. Biophys. Acta 1761, 913-926 (2006).
16. Kim, H. S. et al. Bacterial genome adaptation to niches: divergence of the potential virulence genes in three Burkholderia species of different survival strategies. BMC Genomics 6, 174 (2005).
17. Yildiz, F. H. & Schoolnik, G. K. Role of rpoS in stress survival and virulence of Vibrio cholerae. J. Bacteriol. 180, 773-784 (1998).
18. Stover, C. K. et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406, 959-964 (2000).
19. Palmer, K. L., Aye, L. M. & Whiteley, M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J. Bacteriol. 189, 8079-8087 (2007).
20. Chou, S. et al. Structure of a peptidoglycan amidase effector targeted to Gramnegative bacteria by the type VI secretion system. Cell Rep. 1, 656-664 (2012).
21. Chandler, J. R. et al. Mutational analysis of Burkholderia thailandensis quorum sensing and self-aggregation. J. Bacteriol. 191, 5901-5909 (2009).
22. Vaitkevicius, K. et al. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc. Natl Acad. Sci. USA 103, 9280-9285 (2006).
23. Valeru, S. P. et al. Role ofmelanin pigment in expression of Vibrio cholerae virulence factors. Infect. Immun. 77, 935-942 (2009).
24. Rietsch, A., Vallet-Gely, I., Dove, S. L. & Mekalanos, J. J. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 102, 8006-8011 (2005).
25. Nelson, K. E. et al. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4, 799-808 (2002).
26. Horton, R. M. et al. Gene splicing by overlap extension. Methods Enzymol. 217, 270-279 (1993).
27. Korotkov, K. V. & Hol, W. G. Crystal structure of the pilotin from the enterohemorrhagic Escherichia coli type II secretion system. J. Struct. Biol. http://dx.doi.org/10.1016/j.jsb.2013.02.013 (28 February 2013).
28. Cardona, S. T. & Valvano, M. A. An expression vector containing a rhamnoseinducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54, 219-228 (2005).
29. Hsu, F., Schwarz, S. & Mougous, J. D. TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol. Microbiol. 72, 1111-1125 (2009).
30. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130 (1995).
31. Schell, M. A. et al. Type VI secretion is amajor virulence determinant in Burkholderia mallei. Mol. Microbiol. 64, 1466-1485 (2007).
32. Donnenberg, M. S. & Kaper, J. B. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59, 4310-4317 (1991).
33. Kelley, L. A.&Sternberg, M. J. Protein structure prediction on theWeb: a case study using the Phyre server. Nature Protocols 4, 363-371 (2009).
34. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
35. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).
36. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (2004).
37. Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953-971 (2007).
38. Balsalobre, C. et al. Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol. Microbiol. 59, 99-112 (2006).
39. Imperi, F. et al. Analysis of the periplasmic proteome of Pseudomonas aeruginosa, a metabolically versatile opportunistic pathogen. Proteomics 9, 1901-1915 (2009).
40. Schwarz, S. et al. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6, e1001068 (2010).
41. Termine, E. & Michel, G. P. Transcriptome and secretome analyses of the adaptive response of Pseudomonas aeruginosa to suboptimal growth temperature. Int. Microbiol. 12, 7-12 (2009).
42. von Tigerstrom, R. G. & Stelmaschuk, S. The use of Tween 20 in a sensitive turbidimetric assay of lipolytic enzymes. Can. J. Microbiol. 35, 511-514 (1989).
43. Vance, R. E., Rietsch,A.&Mekalanos, J. J.Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1in vivo. Infect. Immun. 73, 1706-1713 (2005).
44. Mougous, J. D. et al. Identification, function and structure of the mycobacterial sulfotransferase that initiates sulfolipid-1 biosynthesis. Nature Struct. Mol. Biol. 11, 721-729 (2004).
45. Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917 (1959).
46. Bruger, B., Erben, G., Sandhoff, R., Wieland, F. T. & Lehmann, W. D. Quantitative analysis of biological membrane lipids at the low picomole level by nanoelectrospray ionization tandem mass spectrometry. Proc. Natl Acad. Sci. USA 94, 2339-2344 (1997).
47. Devaiah, S. P. et al. Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a PHOSPHOLIPASE Da1 knockout mutant. Phytochemistry 67, 1907-1924 (2006).
48. Welti, R. et al. Profilingmembranelipids in plant stress response. J. Biol. Chem.277, 31994-32002 (2002).