Genome comparisons provide insights into the role of secondary metabolites in the pathogenic phase of the Photorhabdus life cycle

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Tobias, Nicholas J ^a   Mishra, Bagdevi ^a,b   Gupta, Deepak K ^a,b   Sharma, Rahul ^b   Thines, Marco ^a,b   Stinear, Timothy P ^c   Bode, Helge B ^a  

^a GOETHE UNIVERSITY   (Germany)

^b SENCKENBERG DEUTSCHES ENTOMOLOGISCHES INSTITUT   (Germany)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Photorhabdus; Secondary metabolites; Sequencing; Symbiosis

Indexed keywords

GENE CLUSTER; GENE LOCUS; GENUS; HUMAN; IMMUNE RESPONSE; INSECT; LIFE CYCLE; METABOLITE; NEMATODE; NONHUMAN; PHOTORHABDUS; SPECIES; SYMBIOSIS; ANIMAL; BACTERIAL GENOME; COMPARATIVE STUDY; CONSERVED SEQUENCE; DNA BASE COMPOSITION; DNA SEQUENCE; GENETICS; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PROCEDURES; SECONDARY METABOLISM;

BACTERIAL PROTEIN;

ANIMALS; BACTERIAL PROTEINS; BASE COMPOSITION; BASE SEQUENCE; CONSERVED SEQUENCE; GENOME, BACTERIAL; INSECTS; MULTIGENE FAMILY; NEMATODA; PHOTORHABDUS; SECONDARY METABOLISM; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84988349442     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2862-4     Document Type: Article

References (96)

1. Kwak Y, Shin JH. Complete genome sequence of Photorhabdus temperata subsp. thracensis 39-8, an entomopathogenic bacterium for the improved commercial bioinsecticide. J Biotechnol. 2015;214:115-6.
2. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, Taourit S, Bocs S, Boursaux-Eude C, Chandler M, Charles JF, et al. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol. 2003;21:1307-13.
3. Park GS, Khan AR, Hong SJ, Jang EK, Ullah I, Jung BK, Choi J, Yoo NK, Park KJ, Shin JH. Draft Genome Sequence of Entomopathogenic Bacterium Photorhabdus temperata Strain M1021, Isolated from Nematodes. Genome Announc. 2013;1(5);e00747-13. doi: 10.1128/genomeA.00747-13.
4. Tailliez P, Laroui C, Ginibre N, Paule A, Pages S, Boemare N. Phylogeny of photorhabdus and xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. Vietnamensis sp. nov., P. Luminescens subsp. Caribbeanensis subsp. nov., P. Luminescens subsp. Hainanensis subsp. nov., P. Temperata subsp. Khanii subsp. nov., P. Temperata subsp. Tasmaniensis subsp. nov., and the reclassification of P. Luminescens subsp. Thracensis as P. Temperata subsp. Thracensis comb. nov. Int J Syst Evol Microbiol. 2010;60:1921-37.
5. Hazir S, Stackebrandt E, Lang E, Schumann P, Ehlers RU, Keskin N. Two new subspecies of photorhabdus luminescens, isolated from Heterorhabditis bacteriophora (nematoda: heterorhabditidae): photorhabdus luminescens subsp. Kayaii subsp. nov. And photorhabdus luminescens subsp. Thracensis subsp. nov. Syst Appl Microbiol. 2004;27:36-42.
6. Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, Vlisidou I, Barron A, Bignell A, Clark L, Ormond D, et al. Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics. 2009;10:302.
7. Fischer-Le Saux M, Viallard V, Brunel B, Normand P, Boemare NE. Polyphasic classification of the genus photorhabdus and proposal of new taxa: P. Luminescens subsp. Luminescens subsp. nov., P. Luminescens subsp. Akhurstii subsp. nov., P. Luminescens subsp. Laumondii subsp. nov., P. Temperata sp. nov., P. Temperata subsp. Temperata subsp. nov. And P. Asymbiotica sp. nov. Int J Syst Bacteriol. 1999;49(4):1645-56.
8. Han R, Ehlers RU. Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. J Invertebr Pathol. 2000;75:55-8.
9. Gerrard JG, Vohra R, Nimmo GR. Identification of Photorhabdus asymbiotica in cases of human infection. Commun Dis Intell Q Rep. 2003;27:540-1.
10. Kronenwerth M, Bozhuyuk KA, Kahnt AS, Steinhilber D, Gaudriault S, Kaiser M, Bode HB. Characterisation of taxlllaids A-G; natural products from Xenorhabdus indica. Chemistry. 2014;20:17478-87.
11. Lang G, Kalvelage T, Peters A, Wiese J, Imhoff JF. Linear and cyclic peptides from the entomopathogenic bacterium Xenorhabdus nematophilus. J Nat Prod. 2008;71:1074-7.
12. Oka M, Numata K, Nishiyama Y, Kamei H, Konishi M, Oki T, Kawaguchi H. Chemical modification of the antitumor antibiotic glidobactin. J Antibiot (Tokyo). 1988;41:1812-22.
13. Oka M, Ohkuma H, Kamei H, Konishi M, Oki T, Kawaguchi H. Glidobactins D, E, F, G and H; minor components of the antitumor antibiotic glidobactin. J Antibiot (Tokyo). 1988;41:1906-9.
14. Schimming O, Fleischhacker F, Nollmann FI, Bode HB. Yeast homologous recombination cloning leading to the novel peptides ambactin and xenolindicin. Chembiochem. 2014;15:1290-4.
15. Velasco A, Acebo P, Gomez A, Schleissner C, Rodriguez P, Aparicio T, Conde S, Munoz R, de la Calle F, Garcia JL, Sanchez-Puelles JM. Molecular characterization of the safracin biosynthetic pathway from Pseudomonas fluorescens A2-2: designing new cytotoxic compounds. Mol Microbiol. 2005;56:144-54.
16. Zhou Q, Dowling A, Heide H, Wohnert J, Brandt U, Baum J, Ffrench-Constant R, Bode HB. Xentrivalpeptides A-Q: depsipeptide diversification in Xenorhabdus. J Nat Prod. 2012;75:1717-22.
17. Brachmann AO, Joyce SA, Jenke-Kodama H, Schwar G, Clarke DJ, Bode HB. A type II polyketide synthase is responsible for anthraquinone biosynthesis in Photorhabdus luminescens. Chembiochem. 2007;8:1721-8.
18. Goodrich-Blair H, Clarke DJ. Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol. 2007;64:260-8.
19. Joyce SA, Brachmann AO, Glazer I, Lango L, Schwar G, Clarke DJ, Bode HB. Bacterial biosynthesis of a multipotent stilbene. Angew Chem Int Ed Engl. 2008;47:1942-5.
20. Joyce SA, Clarke DJ. A hexA homologue from Photorhabdus regulates pathogenicity, symbiosis and phenotypic variation. Mol Microbiol. 2003;47:1445-57.
21. Bischoff V, Vignal C, Boneca IG, Michel T, Hoffmann JA, Royet J. Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria. Nat Immunol. 2004;5:1175-80.
22. Filipe SR, Tomasz A, Ligoxygakis P. Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway. EMBO Rep. 2005;6:327-33.
23. Michel T, Reichhart JM, Hoffmann JA, Royet J. Drosophila toll is activated by gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature. 2001;414:756-9.
24. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The toll and Imd pathways are the major regulators of the immune response in drosophila. EMBO J. 2002;21:2568-79.
25. Tanji T, Hu X, Weber AN, Ip YT. Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol Cell Biol. 2007;27:4578-88.
26. Sugumaran M, Nellaiappan K. Lysolecithin--a potent activator of prophenoloxidase from the hemolymph of the lobster, Homarus americanas. Biochem Biophys Res Commun. 1991;176:1371-6.
27. Cerenius L, Soderhall K. The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004;198:116-26.
28. Nappi AJ, Vass E. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res. 1993;6:117-26.
29. Nappi AJ, Christensen BM. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol. 2005;35:443-59.
30. Crawford JM, Portmann C, Zhang X, Roeffaers MB, Clardy J. Small molecule perimeter defense in entomopathogenic bacteria. Proc Natl Acad Sci U S A. 2012;109:10821-6.
31. Felfoldi G, Marokhazi J, Kepiro M, Venekei I. Identification of natural target proteins indicates functions of a serralysin-type metalloprotease, PrtA, in anti-immune mechanisms. Appl Environ Microbiol. 2009;75:3120-6.
32. Heermann R, Fuchs TM. Comparative analysis of the photorhabdus luminescens and the Yersinia enterocolitica genomes: uncovering candidate genes involved in insect pathogenicity. BMC Genomics. 2008;9:40.
33. Thanwisai A, Tandhavanant S, Saiprom N, Waterfield NR, Ke Long P, Bode HB, Peacock SJ, Chantratita N. Diversity of xenorhabdus and photorhabdus spp. And their symbiotic entomopathogenic nematodes from Thailand. PLoS One. 2012;7:e43835.
34. Hurst S, Rowedder H, Michaels B, Bullock H, Jackobeck R, Abebe-Akele F, Durakovic U, Gately J, Janicki E, Tisa LS. Elucidation of the photorhabdus temperata genome and generation of a transposon mutant library to identify motility mutants altered in pathogenesis. J Bacteriol. 2015;197:2201-16.
35. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182-185.
36. Brameyer S, Kresovic D, Bode HB, Heermann R. Dialkylresorcinols as bacterial signaling molecules. Proc Natl Acad Sci U S A. 2015;112:572-7.
37. Seo S, Lee S, Hong Y, Kim Y. Phospholipase A2 inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl Environ Microbiol. 2012;78:3816-23.
38. Fuchs SW, Bozhuyuk KA, Kresovic D, Grundmann F, Dill V, Brachmann AO, Waterfield NR, Bode HB. Formation of 1,3-cyclohexanediones and resorcinols catalyzed by a widely occurring ketosynthase. Angew Chem Int Ed Engl. 2013;52:4108-12.
39. Dudnik A, Bigler L, Dudler R. Heterologous expression of a Photorhabdus luminescens syrbactin-like gene cluster results in production of the potent proteasome inhibitor glidobactin A. Microbiol Res. 2013;168:73-6.
40. Brachmann AO, Brameyer S, Kresovic D, Hitkova I, Kopp Y, Manske C, Schubert K, Bode HB, Heermann R. Pyrones as bacterial signaling molecules. Nat Chem Biol. 2013;9:573-8.
41. Bode HB, Brachmann AO, Jadhav KB, Seyfarth L, Dauth C, Fuchs SW, Kaiser M, Waterfield NR, Sack H, Heinemann SH, Arndt HD. Structure elucidation and activity of kolossin a, the D-/L-pentadecapeptide product of a giant nonribosomal peptide synthetase. Angew Chem Int Ed Engl. 2015;54:10352-5.
42. Bode E, Brachmann AO, Kegler C, Simsek R, Dauth C, Zhou Q, Kaiser M, Klemmt P, Bode HB. Simple "on-demand" production of bioactive natural products. Chembiochem. 2015;16:1115-9.
43. Nollmann FI, Dauth C, Mulley G, Kegler C, Kaiser M, Waterfield NR, Bode HB. Insect-Specific Production of New GameXPeptides in Photorhabdus luminescens TTO1, Widespread Natural Products in Entomopathogenic Bacteria. Chembiochem. 2015;16;205-8. doi: 10.1002/cbic.201402603. Epub 2014 Nov 25
44. Brachmann AO, Kirchner F, Kegler C, Kinski SC, Schmitt I, Bode HB. Triggering the production of the cryptic blue pigment indigoidine from Photorhabdus luminescens. J Biotechnol. 2012;157:96-9.
45. Yim G, Wang HH, Davies J. Antibiotics as signalling molecules. Philos Trans R Soc Lond B Biol Sci. 2007;362:1195-200.
46. Li J, Chen G, Wu H, Webster JM. Identification of two pigments and a hydroxystilbene antibiotic from Photorhabdus luminescens. Appl Environ Microbiol. 1995;61:4329-33.
47. Buscato E, Buttner D, Bruggerhoff A, Klingler FM, Weber J, Scholz B, Zivkovic A, Marschalek R, Stark H, Steinhilber D, et al. From a multipotent stilbene to soluble epoxide hydrolase inhibitors with antiproliferative properties. ChemMedChem. 2013;8:919-23.
48. Mast Y, Weber T, Golz M, Ort-Winklbauer R, Gondran A, Wohlleben W, Schinko E. Characterization of the 'pristinamycin supercluster' of Streptomyces pristinaespiralis. Microb Biotechnol. 2011;4:192-206.
49. Castagnola A, Stock SP. Common virulence factors and tissue targets of entomopathogenic bacteria for biological control of lepidopteran pests. Insects. 2014;5:139-66.
50. Brady SF, Clardy J. Cloning and heterologous expression of isocyanide biosynthetic genes from environmental DNA. Angew Chem Int Ed Engl. 2005;44:7063-5.
51. Saha R, Saha N, Donofrio RS, Bestervelt LL. Microbial siderophores: a mini review. J Basic Microbiol. 2013;53:303-17.
52. Koh EI, Henderson JP. Microbial copper-binding siderophores at the host-pathogen interface. J Biol Chem. 2015;290:18967-74.
53. Sheldon JR, Heinrichs DE. Recent developments in understanding the iron acquisition strategies of gram positive pathogens. FEMS Microbiol Rev. 2015;39:592-630.
54. Schieferdecker S, Konig S, Koeberle A, Dahse HM, Werz O, Nett M. Myxochelins target human 5-lipoxygenase. J Nat Prod. 2015;78:335-8.
55. González-Santoyo I, Córdoba-Aguilar A. Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl. 2012;142:1-16.
56. Mukherjee K, Fischer R, Vilcinskas A. Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front Zool. 2012;9:25.
57. Downer RG, Moore SJ WLD-J, Mandato CA. The effects of eicosanoid biosynthesis inhibitors on prophenoloxidase activation, phagocytosis and cell spreading in galleria mellonella. J Insect Physiol. 1997;43:1-8.
58. Kim Y, Ji D, Cho S, Park Y. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression. J Invertebr Pathol. 2005;89:258-64.
59. Stein ML, Beck P, Kaiser M, Dudler R, Becker CF, Groll M. One-shot NMR analysis of microbial secretions identifies highly potent proteasome inhibitor. Proc Natl Acad Sci U S A. 2012;109:18367-71.
60. Danese PN, Silhavy TJ. The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 1997;11:1183-93.
61. Danese PN, Silhavy TJ. CpxP, a stress-combative member of the Cpx regulon. J Bacteriol. 1998;180:831-9.
62. Raivio TL, Popkin DL, Silhavy TJ. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol. 1999;181:5263-72.
63. Raivio TL, Silhavy TJ. The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol. 1999;2:159-65.
64. Weatherspoon-Griffin N, Yang D, Kong W, Hua Z, Shi Y. The CpxR/CpxA two-component regulatory system up-regulates the multidrug resistance cascade to facilitate Escherichia coli resistance to a model antimicrobial peptide. J Biol Chem. 2014;289:32571-82.
65. Nevesinjac AZ, Raivio TL. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J Bacteriol. 2005;187:672-86.
66. Ma Q, Wood TK. OmpA influences Escherichia coli biofilm formation by repressing cellulose production through the CpxRA two-component system. Environ Microbiol. 2009;11:2735-46.
67. De Wulf P, Kwon O, Lin EC. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J Bacteriol. 1999;181:6772-8.
68. Nagakubo S, Nishino K, Hirata T, Yamaguchi A. The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol. 2002;184:4161-7.
69. Widenhorn KA, Somers JM, Kay WW. Expression of the divergent tricarboxylate transport operon (tctI) of Salmonella typhimurium. J Bacteriol. 1988;170:3223-7.
70. Weston LA, Kadner RJ. Role of uhp genes in expression of the Escherichia coli sugar-phosphate transport system. J Bacteriol. 1988;170:3375-83.
71. Egger LA, Park H, Inouye M. Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells. 1997;2:167-84.
72. Forst SA, Roberts DL. Signal transduction by the EnvZ-OmpR phosphotransfer system in bacteria. Res Microbiol. 1994;145:363-73.
73. Coornaert A, Chiaruttini C, Springer M, Guillier M. Post-transcriptional control of the Escherichia coli PhoQ-PhoP two-component system by multiple sRNAs involves a novel pairing region of GcvB. PLoS Genet. 2013;9:e1003156.
74. Zwir I, Shin D, Kato A, Nishino K, Latifi T, Solomon F, Hare JM, Huang H, Groisman EA. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A. 2005;102:2862-7.
75. Derzelle S, Ngo S, Turlin E, Duchaud E, Namane A, Kunst F, Danchin A, Bertin P, Charles JF. AstR-AstS, a new two-component signal transduction system, mediates swarming, adaptation to stationary phase and phenotypic variation in Photorhabdus luminescens. Microbiology. 2004;150:897-910.
76. Brameyer S, Kresovic D, Bode HB, Heermann R. LuxR solos in Photorhabdus species. Front Cell Infect Microbiol. 2014;4:166.
77. Burlingame R, Chapman PJ. Catabolism of phenylpropionic acid and its 3-hydroxy derivative by Escherichia coli. J Bacteriol. 1983;155:113-21.
78. Prieto MA, Diaz E, Garcia JL. Molecular characterization of the 4-hydroxyphenylacetate catabolic pathway of Escherichia coli W: engineering a mobile aromatic degradative cluster. J Bacteriol. 1996;178:111-20.
79. Caldas C, Cherqui A, Pereira A, Simoes N. Purification and characterization of an extracellular protease from Xenorhabdus nematophila involved in insect immunosuppression. Appl Environ Microbiol. 2002;68:1297-304.
80. ffrench-Constant R, Waterfield N, Daborn P, Joyce S, Bennett H, Au C, Dowling A, Boundy S, Reynolds S, Clarke D. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev. 2003;26:433-56.
81. Lally ET, Hill RB, Kieba IR, Korostoff J. The interaction between RTX toxins and target cells. Trends Microbiol. 1999;7:356-61.
82. Daborn PJ, Waterfield N, Silva CP, Au CP, Sharma S, Ffrench-Constant RH. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci U S A. 2002;99:10742-7.
83. Daborn PJ, Waterfield N, Blight MA, Ffrench-Constant RH. Measuring virulence factor expression by the pathogenic bacterium Photorhabdus luminescens in culture and during insect infection. J Bacteriol. 2001;183:5834-9.
84. Munch A, Stingl L, Jung K, Heermann R. Photorhabdus luminescens genes induced upon insect infection. BMC Genomics. 2008;9:229.
85. Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol. 2006;4:811-25.
86. Kosarewicz A, Konigsmaier L, Marlovits TC. The blueprint of the type-3 injectisome. Philos Trans R Soc Lond B Biol Sci. 2012;367:1140-54.
87. Gendlina I, Held KG, Bartra SS, Gallis BM, Doneanu CE, Goodlett DR, Plano GV, Collins CM. Identification and type III-dependent secretion of the Yersinia pestis insecticidal-like proteins. Mol Microbiol. 2007;64:1214-27.
88. Costa SC, Girard PA, Brehelin M, Zumbihl R. The emerging human pathogen Photorhabdus asymbiotica is a facultative intracellular bacterium and induces apoptosis of macrophage-like cells. Infect Immun. 2009;77:1022-30.
89. Michaux C, Sanguinetti M, Reffuveille F, Auffray Y, Posteraro B, Gilmore MS, Hartke A, Giard JC. SlyA is a transcriptional regulator involved in the virulence of Enterococcus faecalis. Infect Immun. 2011;79:2638-45.
90. Lee YH, Kim JH, Bang IS, Park YK. The membrane-bound transcriptional regulator CadC is activated by proteolytic cleavage in response to acid stress. J Bacteriol. 2008;190:5120-6.
91. Casalino M, Prosseda G, Barbagallo M, Iacobino A, Ceccarini P, Latella MC, Nicoletti M, Colonna B. Interference of the CadC regulator in the arginine-dependent acid resistance system of Shigella and enteroinvasive E. coli. Int J Med Microbiol. 2010;300:289-95.
92. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068-9.
93. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinf. 2011;12:124.
94. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072-5.
95. Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Muller R, Wohlleben W, et al. antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 2015;43:W237-243.
96. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinf. 2009;10:421.