Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins

BMC Genomics

Volumn 12, Issue , 2011, Pages

  De Maayer, Pieter ^a   Venter, Stephanus N ^a   Kamber, Tim ^b   Duffy, Brion ^b   Coutinho, Teresa A ^a   Smits, Theo H M ^b  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b AGROSCOPE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HCP PROTEIN; UNCLASSIFIED DRUG; VGRG PROTEIN; BACTERIAL DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; CONTROLLED STUDY; DNA BASE COMPOSITION; ERWINIA; ERWINIA BILLINGIAE; GENE LOCUS; GENOMIC ISLAND; GENOMICS; HCP GENE; NONHUMAN; PANTOEA; PROTEIN DOMAIN; TYPE VI SECRETION SYSTEM; VGRG GENE; BACTERIAL SECRETION SYSTEM; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENETICS; METABOLISM; PHYLOGENY;

ERWINIA; ERWINIA BILLINGIAE; PANTOEA; PANTOEA SP.;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BASE COMPOSITION; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; ERWINIA; GENETIC LOCI; GENOMIC ISLANDS; PANTOEA; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 82055181715     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-576     Document Type: Article

References (61)

1. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Giford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, Walz T, Joachimiak A, Mekalanos JJ. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006, 312:1526-1530. 10.1126/science.1128393, 2800167, 16763151.
2. Pukatzki S, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 2006, 103:1528-1533. 10.1073/pnas.0510322103, 1345711, 16432199.
3. Jani AJ, Cotter PA. Type VI Secretion: Not just for pathogenesis anymore. Cell Host Microbe 2010, 8:2-6. 10.1016/j.chom.2010.06.012, 2913581, 20638635.
4. Schwarz S, Hood RD, Mougous JD. What is type VI secretion doing in all those bugs?. Trends Microbiol 2010, 18:531-537. 10.1016/j.tim.2010.09.001, 20961764.
5. Aschtgen M-S, Thomas MS, Cascales E. Anchoring the type VI secretion system to the peptidoglycan. Virulence 2010, 1:535-540. 10.4161/viru.1.6.13732, 21178498.
6. Parsons DA, Heffron F. sciS, an icmF homolog in Salmonella enterica serovar Typhimurium limits intracellular replication and decreases virulence. Infect Immun 2005, 73:4338-4345. 10.1128/IAI.73.7.4338-4345.2005, 1168621, 15972528.
7. Chow J, Mazmanian SK. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 2010, 7:265-276. 10.1016/j.chom.2010.03.004, 2859213, 20413095.
8. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Burr T, Takle G, Brurberg M-B, Birch PRJ, Salmond GPC, Toth IK. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Path 2008, 4:e1000093.
9. Robinson JB, Telepnev MV, Zudina IV, Bouyer D, Montenieri JA, Bearden SW, Gage KL, Agaer SL, Foltz SM, Chauhan S, Chopra AK, Motin VL. Evaluation of a Yersinia pestis mutants impaired in a thermoregulated type VI-like secretion system in flea, macrophage and murine models. Microb Pathog 2009, 47:243-251. 10.1016/j.micpath.2009.08.005, 2767420, 19716410.
10. Bladergroen MR, Badelt K, Spaink HP. Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant-Microbe Interact 2003, 16:53-64. 10.1094/MPMI.2003.16.1.53, 12580282.
11. Hood RD, Singh P, Hsu F, Carl MA, Trinidad RRS, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Microbe 2010, 7:25-37.
12. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011, 475:343-347. 10.1038/nature10244, 21776080.
13. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki SL. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci USA 2011, 9:6-10.
14. Blondel CJ, Jiménez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 2009, 10:1-17. 10.1186/1471-2164-10-1, 2671524, 19121221.
15. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources?. BMC Genomics 2009, 10:104-11. 10.1186/1471-2164-10-104, 2660368, 19284603.
16. Pukatzki S, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 2007, 104:15508-15513. 10.1073/pnas.0706532104, 2000545, 17873062.
17. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, Pukatzki S, Burley SK, Almo SC, Mekalanos JJ. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 2009, 106:4154-4159. 10.1073/pnas.0813360106, 2657435, 19251641.
18. Pukatzki S, McAuley SB, Miyata ST. The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 2009, 12:11-17. 10.1016/j.mib.2008.11.010, 19162533.
19. Hachani A, Lossi NS, Hamilton A, Jones C, Bleves S, Albesa-Jové D, Filloux A. Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J Biol Chem 2011, 286:12317-12327. 10.1074/jbc.M110.193045, 3069435, 21325275.
20. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 2009, 5:234-243. 10.1016/j.chom.2009.02.005, 3142922, 19286133.
21. Sarris PF, Skandalis N, Kokkinidis M, Panopoulos NJ. In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Mol Plant Pathol 2010, 11:795-804.
22. Smits THM, Rezzonico F, Kamber T, Blom J, Goesmann A, Frey JE, Duffy B. Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp. BMC Genomics 2010, 23:384-393.
23. Braun EJ. Ultrastructural investigation of resistant and susceptible maize inbreds infected with Erwinia stewartii. Phytopathology 1982, 72:159-166.
24. Coutinho TA, Venter SN. Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 2009, 10:325-335. 10.1111/j.1364-3703.2009.00542.x, 19400836.
25. Kube M, Migdoll AM, Gehring I, Heitmann K, Mayer Y, Kuhl H, Knaust F, Geider K, Reinhardt R. Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genomics 2010, 11:393. 10.1186/1471-2164-11-393, 2897811, 20565991.
26. Pusey PL, Stockwell VO, Rudell DR. Antibiosis and acidification by Pantoea agglomerans strain E325 may contribute to suppression of Erwinia amylovora. Phytopathology 2008, 98:1136-1143. 10.1094/PHYTO-98-10-1136, 18943460.
27. Stockwell VO, Johnson KB, Sugar D, Loper JE. Control of fire blight by Pseudomonas fluorescens A506 and Pantoea vagans C9-1 applied as single strains and mixed inocula. Phytopathology 2010, 100:1330-1339. 10.1094/PHYTO-03-10-0097, 20839963.
28. Smits THM, Rezzonico F, Kamber T, Goesmann A, Ishimaru CA, Frey JE, Stockwell VO, Duffy B. Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoea vagans C9-1. PLoS One 2011, 6:e22247. 10.1371/journal.pone.0022247, 3137637, 21789243.
29. Adams AS, Currie CR, Cardoza Y, Klepzig KD, Raffa KF. Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can J For Res 2009, 39:1133-1147.
30. Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST, Cleland WW, Weimer PJ, Currie CR. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 2009, 326:1120-1123. 10.1126/science.1173036, 19965433.
31. De Maayer P, Chan WY, Venter SN, Toth IK, Birch PRJ, Joubert F, Coutinho TA. Genome sequence of Pantoea ananatis LMG 20103, the causative agent of Eucalyptus blight and dieback. J Bacteriol 2010, 192:2936-2937. 10.1128/JB.00060-10, 2876505, 20348253.
32. Smits THM, Rezzonico F, Kamber T, Goesmann A, Ishimaru CA, Stockwell VO, Frey JE, Duffy B. Genome sequence of the biocontrol agent Pantoea vagans C9-1. J Bacteriol 2010, 192:6486-6487. 10.1128/JB.01122-10, 3008540, 20952567.
33. Smits THM, Jaenicke S, Rezzonico F, Kamber T, Goesmann A, Frey JE, Duffy B. Complete genome sequence of the fire blight pathogen Erwinia pyrifoliae DSM 12163T and comparative genomic insights into plant pathogenicity. BMC Genomics 2010, 4:2.
34. Kube M, Migdoll AM, Müller I, Kuhl H, Beck A, Reinhardt R, Geider K. The genome of Erwinia tasmaniensis strain Et1/99, a non-pathogenic bacterium in the genus Erwinia. Environ Microbiol 2008, 10:2211-2222. 10.1111/j.1462-2920.2008.01639.x, 18462403.
35. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nature Cell Biol 2007, 9:797-803. 10.1038/ncb1605, 17558395.
36. Jackson AP, Thomas GH, Parkhill J, Thomson NR. Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics 2009, 16:1-16.
37. TIGRFAM database. , http://www.jcvi.org/cgi-bin/tigrfams/
38. Protein families (PFAM) database. , http://pfam.sanger.ac.uk/
39. Pei J, Grishin NV. COG3926 and COG5526: A tale of two new lysozyme-like protein families. Prot Sci 2005, 14:2574-2581.
40. Conserved Orthologous Groups database. , http://www.ncbi.nlm.nih.gov/COG/grace/
41. Protein Databank (PDB). , http://www.pdb.org/
42. Barret M, Egan F, Fargier E, Morrisey JP, O'Gara F. Genomic analysis of the type VI secretion systems in Pseudomonas spp: novel clusters and putative effectors uncovered. Microbiology 2011, 157:1726-1739. 10.1099/mic.0.048645-0, 21474537.
43. Nardini M, Lang DA, Liebeton K, Jaeger K-E, Dijstra BW. Crystal structure of Pseudomonas aeruginosa lipase in the open conformation. J Biol Chem 2000, 275:31219-31225.
44. Ham JH, Melanson RA, Rush MC. Burkholderia glumae: next major pathogen of rice?. Mol Plant Pathol 2011, 12:329-339. 10.1111/j.1364-3703.2010.00676.x, 21453428.
45. Filipek R, Rzychon M, Olesky A, Gruca M, Dubin A, Potempa J, Botchler M. The staphostatin-staphopain complex: a forward binding inhibitor in complex with its target cysteine protease. J Biol Chem 2003, 278:40959-40966. 10.1074/jbc.M302926200, 12874290.
46. Newstead SL, Potter JA, Wilson JC, Xu G, Chien C-H, Watts AG, Withers SG, Taylor GL. The structure of Clostridium perfringens NanI sialidase and its catalytic intermediates. J Biol Chem 2008, 283:9080-9088. 10.1074/jbc.M710247200, 2431023, 18218621.
47. Hoell IA, Dalhus B, Heggset EB, Aspmo SI, Eijsink VGH. Crystal structure and enzymatic properties of a bacterial family 19 chitinase reveal differences from plant enzymes. FEBS J 2006, 273:4889-4900. 10.1111/j.1742-4658.2006.05487.x, 17010167.
48. Fokine A, Miroshnikov KA, Shneider MM, Mesyanzhinov VV, Rossmann MG. Structure of the bacteriophage φKZ lytic transglycosylase gp144. J Biol Chem 2008, 11:7247-7250.
49. Michel-Briand Y, Baysse C. The pyocins of Pseudomonas aeruginosa. Biochimie 2002, 84:499-510. 10.1016/S0300-9084(02)01422-0, 12423794.
50. Zheng J, Leung KY. Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 2007, 66:1192-1206. 10.1111/j.1365-2958.2007.05993.x, 17986187.
51. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
52. National Centre for Biotechnology Information protein database. , http://www.ncbi.nlm.nih.gov/blast
53. Bingle LEH, Bailey CM, Pallen MJ. Type VI secretion: a beginner's guide. Curr Opin Microbiol 2009, 11:3-8.
54. Kumar S, Dudley J, Nei M, Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9:299-306. 10.1093/bib/bbn017, 2562624, 18417537.
55. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
56. Softberry FgenesB bacterial operon and gene prediction server. , http://linux1.softberry.com
57. National Centre for Biotechnology Information open reading frame prediction server. , http://www.ncbi.nlm.nih.gov/gorf/
58. Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res 2004, 32:327-331.
59. National Centre for Biotechnology Information conserved protein domain search server. , http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi
60. Söding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, (33):W244-248.
61. Homology detection and structure prediction by HMM-HMM comparison server. , http://toolkit.tuebingen.mpg.de/hhpred