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Insecticidal Toxin Complexes from Photorhabdus luminescens

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The Molecular Biology of Photorhabdus Bacteria

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 402))

Abstract

Various bacterial toxins have potent insecticidal activity. Recently, the Toxin complexes (Tc’s) of Photorhabdus and Xenorhabdus species have become an increased focus of current research. These large tripartite toxins with molecular masses >1.4 megadaltons consist of three components termed A, B, and C (or TcA, TcB, and TcC). While TcA is involved in receptor binding and toxin translocation, TcC possesses the specific toxin enzyme activity and TcB is a linker between components TcA and TcC. Here, a structure function analysis of the toxins is described and the application of Tc toxins as potential insecticides is discussed.

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References

  • Aktories K (2011) Bacterial protein toxins that modify host regulatory GTPases. Nat Rev Microbiol 9(7):487-498. doi: 10.1038/nrmicro2592, [pii] nrmicro2592

    Google Scholar 

  • Aktories K, Bärmann M, Ohishi I, Tsuyama S, Jakobs KH, Habermann E (1986) Botulinum C2 toxin ADP-ribosylates actin. Nature 322:390–392

    Article  CAS  PubMed  Google Scholar 

  • Aktories K, Lang AE, Schwan C, Mannherz HG (2011) Actin as target for modification by bacterial protein toxins. FEBS J 278(23):4526–4543. doi:10.1111/j.1742-4658.2011.08113.x

    Google Scholar 

  • Aktories K, Wegner A (1989) ADP-ribosylation of actin by clostridial toxins. J Cell Biol 109:1385–1387

    Article  CAS  PubMed  Google Scholar 

  • Aktories K, Wegner A (1992) Mechanisms of the cytopathic action of actin-ADP-ribosylating toxins. Mol Microbiol 6:2905–2908

    Article  CAS  PubMed  Google Scholar 

  • Bowen D, Rocheleau TA, Blackburn M, Andreev O, Golubeva E, Bhartia R (1998) Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280(5372):2129–2132

    Google Scholar 

  • Bowen DJ, Ensign JC (1998) Purification and characterization of a high-molecular-weight insecticidal protein complex produced by the entomopathogenic bacterium photorhabdus luminescens. Appl Environ Microbiol 64(8):3029–3035

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D’Ascenzo M, Deng WL, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang X, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100(18):10181–10186. doi:10.1073/pnas.1731982100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busby JN, Landsberg MJ, Simpson RM, Jones SA, Hankamer B, Hurst MR, Lott JS (2012) Structural analysis of Chi1 Chitinase from Yen-Tc: the multisubunit insecticidal ABC toxin complex of Yersinia entomophaga. J Mol Biol 415(2):359–371. doi:10.1016/j.jmb.2011.11.018

    Article  CAS  PubMed  Google Scholar 

  • Busby JN, Panjikar S, Landsberg MJ, Hurst MR, Lott JS (2013) The BC component of ABC toxins is an RHS-repeat-containing protein encapsulation device. Nature 501(7468):547–550. doi: 10.1038/nature12465, [pii] nature12465

    Google Scholar 

  • Cherfils J, Zeghouf M (2013) Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 93(1):269–309. doi: 10.1152/physrev.00003.2012, [pii] 93/1/269

    Google Scholar 

  • Daborn PJ, Waterfield N, Blight MA, Ffrench-Constant RH (2001) Measuring virulence factor expression by the pathogenic bacterium Photorhabdus luminescens in culture and during insect infection. J Bacteriol 183(20):5834–5839. doi:10.1128/JB.183.20.5834-5839.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169–186. doi:10.1146/annurev-biophys-042910-155359 [doi]

  • ffrench-Constant R, Waterfield N (2006) An ABC guide to the bacterial toxin complexes. Adv Appl Microbiol 58:169–183

    Google Scholar 

  • ffrench-Constant RH, Bowen DJ (2000) Novel insecticidal toxins from nematode-symbiotic bacteria. Cell Mol Life Sci 57(5):828–833

    Google Scholar 

  • ffrench-Constant RH, Dowling A, Waterfield NR (2007) Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 49 (4):436–451

    Google Scholar 

  • Fieldhouse RJ, Merrill AR (2008) Needle in the haystack: structure-based toxin discovery. Trends Biochem Sci 33(11):546–556. doi: 10.1016/j.tibs.2008.08.003, [pii] S0968-0004(08)00188-6

    Google Scholar 

  • Forst S, Dowds B, Boemare N, Stackebrandt E (1997) Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51:47–72

    Article  CAS  PubMed  Google Scholar 

  • Forst S, Nealson K (1996) Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiol Rev 60(1):21–43

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Mata R, Burridge K (2007) Catching a GEF by its tail. Trends Cell Biol 17(1):36–43. doi: 10.1016/j.tcb.2006.11.004, [pii] S0962-8924(06)00326-6

    Google Scholar 

  • Gatsogiannis C, Lang AE, Meusch D, Pfaumann V, Hofnagel O, Benz R, Aktories K, Raunser S (2013) A syringe-like injection mechanism in Photorhabdus luminescens toxins. Nature 495(7442):520–523. doi: 10.1038/nature11987, [pii] nature11987

    Google Scholar 

  • Gatsogiannis C, Merino F, Prumbaum D, Roderer D, Leidreiter F, Meusch D, Raunser S (2016) Membrane insertion of a Tc toxin in near-atomic detail. Nat Struct Mol Biol. doi:10.1038/nsmb.3281

    PubMed  Google Scholar 

  • Gülke I, Pfeifer G, Liese J, Fritz M, Hofmann F, Aktories K, Barth H (2001) Characterization of the enzymatic component of the ADP-ribosyltransferase toxin CDTa from Clostridium difficile. Infect Immun 69(10):6004–6011

    Article  PubMed  PubMed Central  Google Scholar 

  • Han S, Craig JA, Putnam CD, Carozzi NB, Tainer JA (1999) Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex. Nature Struct Biol 6:932–936

    Article  CAS  PubMed  Google Scholar 

  • Hanna S, El-Sibai M (2013) Signaling networks of Rho GTPases in cell motility. Cell Signal 25(10):1955–1961. doi: 10.1016/j.cellsig.2013.04.009, [pii] S0898-6568(13)00124-1

    Google Scholar 

  • Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9(9):690–701. doi: 10.1038/nrm2476, [pii] nrm2476

    Google Scholar 

  • Hochmann H, Pust S, von FG, Aktories K, Barth H (2006) Salmonella enterica SpvB ADP-ribosylates actin at position arginine-177-characterization of the catalytic domain within the SpvB protein and a comparison to binary clostridial actin-ADP-ribosylating toxins. Biochemistry 45(4):1271–1277

    Google Scholar 

  • Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35(4):208–219. doi: 10.1016/j.tibs.2009.12.003, [pii] S0968-0004(09)00242-4

    Google Scholar 

  • Hurst MR, Glare TR, Jackson TA, Ronson CW (2000) Plasmid-located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J Bacteriol 182(18):5127–5138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst MR, Jones SA, Binglin T, Harper LA, Jackson TA, Glare TR (2011) The main virulence determinant of Yersinia entomophaga MH96 is a broad-host-range toxin complex active against insects. J Bacteriol 193(8):1966–1980. doi:10.1128/JB.01044-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    Article  CAS  PubMed  Google Scholar 

  • Lacey LA, Chauvin RL (1999) Entomopathogenic nematodes for control of diapausing codling moth (Lepidoptera: Tortricidae) in fruit bins. J Econ Entomol 92(1):104–109

    Article  CAS  PubMed  Google Scholar 

  • Lacey LA, Georgis R (2012) Entomopathogenic nematodes for control of insect pests above and below ground with comments on commercial production. J Nematol 44(2):218–225

    PubMed  PubMed Central  Google Scholar 

  • Landsberg MJ, Jones SA, Rothnagel R, Busby JN, Marshall SD, Simpson RM, Lott JS, Hankamer B, Hurst MR (2011) 3D structure of the Yersinia entomophaga toxin complex and implications for insecticidal activity. Proc Natl Acad Sci USA 108(51):20544–20549. doi: 10.1073/pnas.1111155108, [pii] 1111155108

    Google Scholar 

  • Lang AE, Konukiewitz J, Aktories K, Benz R (2013) TcdA1 of Photorhabdus luminescens: Electrophysiological Analysis of Pore Formation and Effector Binding. Biophys J 105(2):376–384. doi: 10.1016/j.bpj.2013.06.003, [pii] S0006-3495(13)00675-9

    Google Scholar 

  • Lang AE, Qu Z, Schwan C, Silvan U, Unger A, Schoenenberger CA, Aktories K, Mannherz HG (2016) Actin ADP-ribosylation at Threonine148 by Photorhabdus luminescens toxin TccC3 induces aggregation of intracellular F-actin. Cell Microbiol. doi:10.1111/cmi.12636

    PubMed  Google Scholar 

  • Lang AE, Schmidt G, Schlosser A, Hey TD, Larrinua IM, Sheets JJ, Mannherz HG, Aktories K (2010) Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 327(5969):1139–1142. doi: 10.1126/science.1184557, [pii] 327/5969/1139

    Google Scholar 

  • Lee SC, Stoilova-McPhie S, Baxter L, Fulop V, Henderson J, Rodger A, Roper DI, Scott DJ, Smith CJ, Morgan JA (2007) Structural characterisation of the insecticidal toxin XptA1, reveals a 1.15 MDa tetramer with a cage-like structure. J Mol Biol 366(5):1558–1568. doi: 10.1016/j.jmb.2006.12.057, [pii] S0022-2836(06)01747-5

    Google Scholar 

  • Lemichez E, Aktories K (2013) Hijacking of Rho GTPases during bacterial infection. Exp Cell Res 319(15):2329–2336

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Burton S, Glancy T, Li ZS, Hampton R, Meade T, Merlo DJ (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat Biotechnol 21(10):1222–1228

    Article  CAS  PubMed  Google Scholar 

  • Mannherz HG, Hannappel E (2009) The beta-thymosins: intracellular and extracellular activities of a versatile actin binding protein family. Cell Motil Cytoskeleton 66(10):839–851. doi:10.1002/cm.20371[doi]

    Article  CAS  PubMed  Google Scholar 

  • Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E, Treisman R (2009) Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat Cell Biol 11(3):257–268. doi: 10.1038/ncb1833, [pii] ncb1833

    Google Scholar 

  • Meusch D, Gatsogiannis C, Efremov RG, Lang AE, Hofnagel O, Vetter IR, Aktories K, Raunser S (2014) Mechanism of Tc toxin action revealed in molecular detail. Nature 508(7494):61–65. doi: 10.1038/nature13015, [pii] nature13015

    Google Scholar 

  • Morgan JA, Sergeant M, Ellis D, Ousley M, Jarrett P (2001) Sequence analysis of insecticidal genes from Xenorhabdus nematophilus PMFI296. Appl Environ Microbiol 67(5):2062–2069. doi:10.1128/AEM.67.5.2062-2069.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O’Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413(6858):848–852

    Article  CAS  PubMed  Google Scholar 

  • Pfaumann V, Lang AE, Schwan C, Schmidt G, Aktories K (2015) The actin and Rho-modifying toxins PTC3 and PTC5 of Photorhabdus luminescens: enzyme characterization and induction of MAL/SRF-dependent transcription. Cell Microbiol 17(4):579–594. doi:10.1111/cmi.12386[doi]

    Article  CAS  PubMed  Google Scholar 

  • Pinto AF, Schuler H (2015) Comparative structural analysis of the putative mono-ADP-ribosyltransferases of the ARTD/PARP family. Curr Top Microbiol Immunol 384:153–166. doi:10.1007/82_2014_417

    CAS  PubMed  Google Scholar 

  • Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326(5957):1208–1212. doi: 10.1126/science.1175862, [pii] 326/5957/1208

    Google Scholar 

  • Posern G, Treisman R (2006) Actin’ together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 16 (11):588–596. doi: 10.1016/j.tcb.2006.09.008, [pii] S0962-8924(06)00269-8

    Google Scholar 

  • Scheffzek K, Ahmadian MR, Wittinghofer A (1998) GTPase-activating proteins: helping hands to complement an active site. Trends Biochem Sci 23(7):257–262. [pii] S0968-0004(98)01224-9

    Google Scholar 

  • Schering B, Bärmann M, Chhatwal GS, Geipel U, Aktories K (1988) ADP-ribosylation of skeletal muscle and non- muscle actin by Clostridium perfringens iota toxin. Eur J Biochem 171:225–229

    Article  CAS  PubMed  Google Scholar 

  • Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K (1997) Gln63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor 1. Nature 387:725–729

    Article  CAS  PubMed  Google Scholar 

  • Schwan C, Stecher B, Tzivelekidis T, van HM, Rohde M, Hardt WD, Wehland J, Aktories K (2009) Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathog 5(10):e1000626. doi:10.1371/journal.ppat.1000626 [doi]

  • Sergeant M, Baxter L, Jarrett P, Shaw E, Ousley M, Winstanley C, Morgan JA (2006) Identification, typing, and insecticidal activity of Xenorhabdus isolates from entomopathogenic nematodes in United Kingdom soil and characterization of the xpt toxin loci. Appl Environ Microbiol 72(9):5895–5907. doi:10.1128/AEM.00217-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sergeant M, Jarrett P, Ousley M, Morgan JA (2003) Interactions of insecticidal toxin gene products from Xenorhabdus nematophilus PMFI296. Appl Environ Microbiol 69(6):3344–3349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheets JJ, Hey TD, Fencil KJ, Burton SL, Ni W, Lang AE, Benz R, Aktories K (2011) Insecticidal toxin complex proteins from Xenorhabdus nematophilus: structure and pore formation. J Biol Chem 286(26):22742–22749. doi: 10.1074/jbc.M111.227009, [pii] M111.227009

    Google Scholar 

  • Silva CP, Waterfield NR, Daborn PJ, Dean P, Chilver T, Au CP, Sharma S, Potter U, Reynolds SE(2002) Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta. Cell Microbiol 4(6):329–339. doi:194 [pii]

    Google Scholar 

  • Simon NC, Aktories K, Barbieri JT (2014) Novel bacterial ADP-ribosylating toxins: structure and function. Nat Rev Microbiol 12(9):599–611. doi: 10.1038/nrmicro3310, [pii] nrmicro3310

    Google Scholar 

  • Tezcan-Merdol D, Nyman T, Lindberg U, Haag F, Koch-Nolte F, Rhen M (2001) Actin is ADP-ribosylated by the Salmonella enterica virulence-associated protein SpvB. Mol Microbio 39:606–619

    Article  CAS  Google Scholar 

  • Thumkeo D, Watanabe S, Narumiya S (2013) Physiological roles of Rho and Rho effectors in mammals. Eur J Cell Biol 92(10–11):303–315. doi: 10.1016/j.ejcb.2013.09.002, [pii] S0171-9335(13)00058-7

    Google Scholar 

  • Vandekerckhove J, Schering B, Bärmann M, Aktories K (1987) Clostridium perfringens iota toxin ADP-ribosylates skeletal muscle actin in Arg-177. FEBS Lett 225:48–52

    Article  CAS  PubMed  Google Scholar 

  • Vandekerckhove J, Schering B, Bärmann M, Aktories K (1988) Botulinum C2 toxin ADP-ribosylates cytoplasmic β/g-actin in arginine 177. J Biol Chem 263:696–700

    CAS  PubMed  Google Scholar 

  • Vilches S, Wilhelms M, Yu HB, Leung KY, Tomas JM, Merino S (2008) Aeromonas hydrophila AH-3 AexT is an ADP-ribosylating toxin secreted through the type III secretion system. Microb Pathog 44(1):1–12. doi: 10.1016/j.micpath.2007.06.004, [pii] S0882-4010(07)00084-8

    Google Scholar 

  • Visschedyk DD, Perieteanu AA, Turgeon ZJ, Fieldhouse RJ, Dawson JF, Merrill AR (2010) Photox, a novel actin-targeting mono-ADP-ribosyltransferase from Photorhabdus luminescens. J Biol Chem 285(18):13525–13534. doi: 10.1074/jbc.M109.077339, [pii] M109.077339

    Google Scholar 

  • Vogelsgesang M, Pautsch A, Aktories K (2007) C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins. Naunyn Schmiedebergs Arch Pharmacol 374(5–6):347–360

    Article  CAS  PubMed  Google Scholar 

  • Waterfield N, Dowling A, Sharma S, Daborn PJ, Potter U, ffrench-Constant RH (2001a) Oral toxicity of Photorhabdus luminescens W14 toxin complexes in Escherichia coli. Appl Environ Microbiol 67(11):5017–5024

    Google Scholar 

  • Waterfield N, Hares M, Yang G, Dowling A, ffrench-Constant R (2005) Potentiation and cellular phenotypes of the insecticidal Toxin complexes of Photorhabdus bacteria. Cell Microbiol 7(3):373–382

    Google Scholar 

  • Waterfield NR, Bowen DJ, Fetherston JD, Perry RD, ffrench-Constant RH (2001b) The tc genes of Photorhabdus: a growing family. Trends Microbiol 9(4):185–191

    Google Scholar 

  • Wegner A, Aktories K (1988) ADP-ribosylated actin caps the barbed ends of actin filaments. J Biol Chem 263:13739–13742

    CAS  PubMed  Google Scholar 

  • Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, Vlisidou I, Barron A, Bignell A, Clark L, Ormond D, Mayho M, Bason N, Smith F, Simmonds M, Churcher C, Harris D, Thompson NR, Quail M, Parkhill J, ffrench-Constant RH (2009) Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 10:302. doi: 10.1186/1471-2164-10-302, [pii] 1471-2164-10-302

    Google Scholar 

  • Yang G, Waterfield NR (2013) The role of TcdB and TccC subunits in secretion of the Photorhabdus Tcd toxin complex. PLoS Pathog 9(10):e1003644. doi:10.1371/journal.ppat.1003644

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Institute for Experimental and Clinical Pharmacology and Toxicology, Albert-Ludwigs University of Freiburg, Albertstr. 25, 79104, Freiburg, Germany

    Joel Sheets & Klaus Aktories

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  1. Joel Sheets
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  2. Klaus Aktories
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Correspondence to Klaus Aktories .

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  1. Centre for Ecology and Conservation, University of Exeter, Penryn, United Kingdom

    Richard H. ffrench-Constant

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Sheets, J., Aktories, K. (2016). Insecticidal Toxin Complexes from Photorhabdus luminescens . In: ffrench-Constant, R. (eds) The Molecular Biology of Photorhabdus Bacteria . Current Topics in Microbiology and Immunology, vol 402. Springer, Cham. https://doi.org/10.1007/82_2016_55

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