1887

Abstract

Different model systems have, over the years, contributed to our current understanding of the molecular mechanisms underpinning the various types of interaction between bacteria and their animal hosts. The genus comprises Gram-negative insect pathogenic bacteria that are normally found as symbionts that colonize the gut of the infective juvenile stage of soil-dwelling nematodes from the family . The nematodes infect susceptible insects and release the bacteria into the insect haemolymph where the bacteria grow, resulting in the death of the insect. At this stage the nematodes feed on the bacterial biomass and, following several rounds of reproduction, the nematodes develop into infective juveniles that leave the insect cadaver in search of new hosts. Therefore has three distinct and obligate roles to play during this life-cycle: (1) must kill the insect host; (2) must be capable of supporting nematode growth and development; and (3) must be able to colonize the gut of the next generation of infective juveniles before they leave the insect cadaver. In this review I will discuss how genetic analysis has identified key genes involved in mediating, and regulating, the interaction between and each of its invertebrate hosts. These studies have resulted in the characterization of several new families of toxins and a novel inter-kingdom signalling molecule and have also uncovered an important role for phase variation in the regulation of these different roles.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000907
2020-03-25
2021-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/166/4/335.html?itemId=/content/journal/micro/10.1099/mic.0.000907&mimeType=html&fmt=ahah

References

  1. Kergunteuil A, Bakhtiari M, Formenti L, Xiao Z, Defossez E et al. Biological control beneath the feet: a review of crop protection against insect root herbivores. Insects 2016; 7:E70 [View Article]
    [Google Scholar]
  2. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M et al. Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 2015; 132:1–41 [View Article]
    [Google Scholar]
  3. Machado RAR, Wüthrich D, Kuhnert P, Arce CCM, Thönen L et al. Whole-genome-based revisit of Photorhabdus phylogeny: proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov. Int J Syst Evol Microbiol 2018; 68:2664–2681 [View Article]
    [Google Scholar]
  4. Adeolu M, Alnajar S, Naushad S, S. Gupta R, Garrity GM. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article]
    [Google Scholar]
  5. Gerrard JG, McNevin S, Alfredson D, Forgan-Smith R, Fraser N. Photorhabdus species: bioluminescent bacteria as emerging human pathogens?. Emerg Infect Dis 2013; 9:251–254 [View Article]
    [Google Scholar]
  6. Weissfeld AS, Halliday RJ, Simmons DE, Trevino EA, Vance PH et al. Photorhabdus asymbiotica, a pathogen emerging on two continents that proves that there is no substitute for a well-trained clinical microbiologist. J Clin Microbiol 2005; 43:4152–4155 [View Article][PubMed]
    [Google Scholar]
  7. Gerrard J, Joyce S, Clarke D, ffrench-Constant R, Nimmo G et al. Nematode Symbiont for Photorhabdus asymbiotica . Emerg Infect Dis 2006; 12:1562–1564 [View Article]
    [Google Scholar]
  8. Plichta KL, Joyce SA, Clarke D, Waterfield N, Stock SP. Heterorhabditis gerrardi n. sp. (Nematoda: Heterorhabditidae): the hidden host of Photorhabdus asymbiotica (Enterobacteriaceae: gamma-proteobacteria). J Helminthol 2009; 83:309–320 [View Article][PubMed]
    [Google Scholar]
  9. Stock SP, Kaya HK. A multivariate analysis of morphometric characters of Heterorhabditis species (Nemata: Heterorhabditidae) and the role of morphometrics in the taxonomy of species of the genus. J Parasitol 1996; 82:806–813 [View Article]
    [Google Scholar]
  10. Molyneux AS, Bedding RA. Penetration of Insect Cuticle By Infective Juveniles of Heterorhabditis Spp (Heterorhabditidae: Nematoda). Nematologica 1982; 28:354–359
    [Google Scholar]
  11. Watson RJ, Joyce SA, Spencer GV, Clarke DJ. The exbD gene of Photorhabdus temperata is required for full virulence in insects and symbiosis with the nematode Heterorhabditis . Mol Microbiol 2005; 56:763–773 [View Article]
    [Google Scholar]
  12. Clarke DJ, Dowds BCA. Virulence mechanisms of Photorhabdus sp. strain K122 toward wax moth larvae. J Invertebr Pathol 1995; 66:149–155 [View Article]
    [Google Scholar]
  13. Johnigk S-A, Ehlers R-U. Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica (Nematoda: Heterorhabditidae). Nematology 1999; 1:251–260 [View Article]
    [Google Scholar]
  14. Ciche TA, Kim K-s, Kaufmann-Daszczuk B, Nguyen KCQ, Hall DH. Cell Invasion and Matricide during Photorhabdus luminescens Transmission by Heterorhabditis bacteriophora Nematodes. Appl Environ Microbiol 2008; 74:2275–2287 [View Article]
    [Google Scholar]
  15. Johnigk S-A, Ehlers R-U. Endotokia matricida in hermaphrodites of Heterorhabditis spp. and the effect of the food supply. Nematology 1999; 1:717–726 [View Article]
    [Google Scholar]
  16. Clarke DJ, Dowds BCA. Pathogenicity of Xenorhabdus luminescens . Biochem Soc Trans 1992; 20:65S [View Article]
    [Google Scholar]
  17. Sato K, Yoshiga T, Hasegawa K. Involvement of Vitamin B6 Biosynthesis Pathways in the Insecticidal Activity of Photorhabdus luminescens . Appl Environ Microbiol 2016; 82:3546–3553 [View Article]
    [Google Scholar]
  18. Hillyer JF. Insect immunology and hematopoiesis. Dev Comp Immunol 2016; 58:102–118 [View Article][PubMed]
    [Google Scholar]
  19. Kanost MR, Jiang H, Yu X-Q. Innate immune responses of a lepidopteran insect, Manduca sexta . Immunol Rev 2004; 198:97–105 [View Article][PubMed]
    [Google Scholar]
  20. Ratcliffe NA, Gagen SJ. Studies on the in vivo cellular reactions of insects: an ultrastructural analysis of nodule formation in Galleria mellonella . Tissue and Cell 1977; 9:73–85 [View Article]
    [Google Scholar]
  21. Ratcliffe NA, Gagen SJ. Cellular defense reactions of insect hemocytes in vivo: nodule formation and development in Galleria mellonella and Pieris brassicae larvae. J Invertebr Pathol 1976; 28:373–382 [View Article]
    [Google Scholar]
  22. Eleftherianos I, Revenis C. Role and importance of phenoloxidase in insect hemostasis. J Innate Immun 2011; 3:28–33 [View Article]
    [Google Scholar]
  23. Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 2008; 29:263–271 [View Article]
    [Google Scholar]
  24. Eleftherianos I, ffrench-Constant RH, Clarke DJ, Dowling AJ, Reynolds SE. Dissecting the immune response to the entomopathogen Photorhabdus . Trends Microbiol 2010; 18:552–560 [View Article]
    [Google Scholar]
  25. Eleftherianos I, Baldwin H, ffrench-Constant RH, Reynolds SE. Developmental modulation of immunity: Changes within the feeding period of the fifth larval stage in the defence reactions of Manduca sexta to infection by Photorhabdus . J Insect Physiol 2008; 54:309–318 [View Article]
    [Google Scholar]
  26. Castillo JC, Shokal U, Eleftherianos I. Immune gene transcription in Drosophila adult flies infected by entomopathogenic nematodes and their mutualistic bacteria. J Insect Physiol 2013; 59:179–185 [View Article]
    [Google Scholar]
  27. Arefin B, Kucerova L, Dobes P, Markus R, Strnad H et al. Genome-Wide transcriptional analysis of Drosophila larvae infected by entomopathogenic nematodes shows involvement of complement, recognition and extracellular matrix proteins. J Innate Immun 2014; 6:192–204 [View Article][PubMed]
    [Google Scholar]
  28. Chevée V, Sachar U, Yadav S, Heryanto C, Eleftherianos I. The peptidoglycan recognition protein PGRP-LE regulates the Drosophila immune response against the pathogen Photorhabdus . Microb Pathog 2019; 136:103664 [View Article]
    [Google Scholar]
  29. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U et al. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 2005; 122:461–472 [View Article]
    [Google Scholar]
  30. Bader MW, Navarre WW, Shiau W, Nikaido H, Frye JG et al. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol 2003; 50:219–230 [View Article]
    [Google Scholar]
  31. Derzelle S, Turlin E, Duchaud E, Pages S, Kunst F et al. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 2004; 186:1270–1279 [View Article]
    [Google Scholar]
  32. Mouammine A, Pages S, Lanois A, Gaudriault S, Jubelin G et al. An antimicrobial peptide-resistant minor subpopulation of Photorhabdus luminescens is responsible for virulence. Sci Rep 2017; 7:1–13 [View Article]
    [Google Scholar]
  33. Guo L et al. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ . Science 1997; 276:250–253 [View Article]
    [Google Scholar]
  34. Gunn JS, Lim KB, Krueger J, Kim K, Guo L et al. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid a modification and polymyxin resistance. Mol Microbiol 1998; 27:1171–1182 [View Article]
    [Google Scholar]
  35. Bennett HPJ, Clarke DJ. The pbgPE operon in Photorhabdus luminescens is required for pathogenicity and symbiosis. J Bacteriol 2005; 187:77–84 [View Article]
    [Google Scholar]
  36. Crawford JM, Portmann C, Zhang X, Roeffaers MBJ, Clardy J. Small molecule perimeter defense in entomopathogenic bacteria. Proc Natl Acad Sci U S A 2012; 109:10821–10826 [View Article]
    [Google Scholar]
  37. Eleftherianos I, Boundy S, Joyce SA, Aslam S, Marshall JW et al. An antibiotic produced by an insect-pathogenic bacterium suppresses host defenses through phenoloxidase inhibition. Proc Natl Acad Sci U S A 2007; 104:2419–2424 [View Article][PubMed]
    [Google Scholar]
  38. Seo S, Lee S, Hong Y, Kim Y. Phospholipase A 2 Inhibitors Synthesized by Two Entomopathogenic Bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata . Appl Environ Microbiol 2012; 78:3816–3823 [View Article]
    [Google Scholar]
  39. Brugirard-Ricaud K, Duchaud E, Givaudan A, Girard PA, Kunst F et al. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell Microbiol 2005; 7:363–371 [View Article]
    [Google Scholar]
  40. Brugirard-Ricaud K, Givaudan A, Parkhill J, Boemare N, Kunst F et al. Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis. J Bacteriol 2004; 186:4376–4381 [View Article]
    [Google Scholar]
  41. Rodou A, Ankrah DO, Stathopoulos C. Toxins and secretion systems of Photorhabdus luminescens . Toxins 2010; 2:1250–1264 [View Article][PubMed]
    [Google Scholar]
  42. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A et al. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens . Nat Biotechnol 2003; 21:1307–1313 [View Article]
    [Google Scholar]
  43. Brillard J, Duchaud E, Boemare N, Kunst F, Givaudan A. The PhlA hemolysin from the entomopathogenic bacterium Photorhabdusluminescens belongs to the two-partner secretion family of hemolysins. J Bacteriol 2002; 184:3871–3878 [View Article]
    [Google Scholar]
  44. Bowen D et al. Insecticidal toxins from the bacterium Photorhabdus luminescens . Science 1998; 280:2129–2132 [View Article]
    [Google Scholar]
  45. Blackburn M, Golubeva E, Bowen D, Ffrench-Constant RH. A novel insecticidal toxin from Photorhabdus luminescens, toxin complex A (TCA), and its histopathological effects on the midgut of Manduca sexta . Appl Environ Microbiol 1998; 64:3036–3041 [View Article]
    [Google Scholar]
  46. Gatsogiannis C, Lang AE, Meusch D, Pfaumann V, Hofnagel O et al. A syringe-like injection mechanism in Photorhabdus luminescens toxins. Nature 2013; 495:520–523 [View Article][PubMed]
    [Google Scholar]
  47. Lang AE, Schmidt G, Schlosser A, Hey TD, Larrinua IM et al. Photorhabdus luminescens toxins ADP-ribosylate actin and RhoA to force actin clustering. Science 2010; 327:1139–1142 [View Article]
    [Google Scholar]
  48. Waterfield N, Hares M, Yang G, Dowling A, ffrench-Constant R. Potentiation and cellular phenotypes of the insecticidal Toxin complexes of Photorhabdus bacteria. Cell Microbiol 2005; 7:373–382 [View Article]
    [Google Scholar]
  49. Yang G, Hernández-Rodríguez CS, Beeton ML, Wilkinson P, ffrench-Constant RH et al. Pdl1 is a putative lipase that enhances Photorhabdus toxin complex secretion. PLoS Pathog 2012; 8:e1002692 [View Article]
    [Google Scholar]
  50. Pinheiro VB, Ellar DJ. Expression and insecticidal activity of Yersinia pseudotuberculosis and Photorhabdus luminescens toxin complex proteins. Cell Microbiol 2007; 9:2372–2380 [View Article]
    [Google Scholar]
  51. Hurst MR, Glare TR, Jackson TA, Ronson CW. 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 2000; 182:5127–5138 [View Article][PubMed]
    [Google Scholar]
  52. Waterfield NR, Bowen DJ, Fetherston JD, Perry RD, ffrench-Constant RH. The tc genes of Photorhabdus: a growing family. Trends Microbiol 2001; 9:185–191 [View Article]
    [Google Scholar]
  53. Jank T, Lang AE, Aktories K. Rho-modifying bacterial protein toxins from Photorhabdus species. Toxicon 2016; 116:17–22 [View Article]
    [Google Scholar]
  54. Lang AE, Schmidt G, Sheets JJ, Aktories K. Targeting of the actin cytoskeleton by insecticidal toxins from Photorhabdus luminescens . Naunyn Schmiedebergs Arch Pharmacol 2011; 383:227–235 [View Article]
    [Google Scholar]
  55. Pfaumann V, Lang AE, Schwan C, Schmidt G, Aktories K. The actin and Rho-modifying toxins PTC3 and PTC5 of P hotorhabdus luminescens : enzyme characterization and induction of MAL/SRF-dependent transcription. Cell Microbiol 2015; 17:579–594 [View Article]
    [Google Scholar]
  56. Meusch D, Gatsogiannis C, Efremov RG, Lang AE, Hofnagel O et al. Mechanism of Tc toxin action revealed in molecular detail. Nature 2014; 508:61–65 [View Article][PubMed]
    [Google Scholar]
  57. Gatsogiannis C, Merino F, Roderer D, Balchin D, Schubert E et al. Tc toxin activation requires unfolding and refolding of a β-propeller. Nature 2018; 563:209–213 [View Article]
    [Google Scholar]
  58. Roderer D, Hofnagel O, Benz R, Raunser S. Structure of a Tc holotoxin pore provides insights into the translocation mechanism. Proc Natl Acad Sci U S A 2019; 116:23083–23090 [View Article]
    [Google Scholar]
  59. Roderer D, Schubert E, Sitsel O, Raunser S. Towards the application of Tc toxins as a universal protein translocation system. Nat Commun 2019; 10:5263 [View Article]
    [Google Scholar]
  60. Daborn PJ, Waterfield N, Silva CP, Au CPY, Sharma S et al. 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; 99:10742–10747 [View Article]
    [Google Scholar]
  61. Vlisidou I, Dowling AJ, Evans IR, Waterfield N, ffrench-Constant RH et al. Drosophila embryos as model systems for monitoring bacterial infection in real time. PLoS Pathog 2009; 5:e1000518 [View Article][PubMed]
    [Google Scholar]
  62. Vlisidou I, Waterfield N, Wood W. Elucidating the in vivo targets of Photorhabdus toxins in real-time using Drosophila embryos. Adv Exp Med Biol 2012; 710:49–57 [View Article][PubMed]
    [Google Scholar]
  63. Dowling AJ, Waterfield NR, Hares MC, Le Goff G, Streuli CH et al. The Mcf1 toxin induces apoptosis via the mitochondrial pathway and apoptosis is attenuated by mutation of the BH3-like domain. Cell Microbiol 2007; 9:2470–2484 [View Article]
    [Google Scholar]
  64. Dowling AJ, Daborn PJ, Waterfield NR, Wang P, Streuli CH et al. The insecticidal toxin makes caterpillars floppy (MCF) promotes apoptosis in mammalian cells. Cell Microbiol 2004; 6:345–353 [View Article]
    [Google Scholar]
  65. Yang G, Dowling AJ, Gerike U, ffrench-Constant RH, Waterfield NR. Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J Bacteriol 2006; 188:2254–2261 [View Article]
    [Google Scholar]
  66. Jiang F, Li N, Wang X, Cheng J, Huang Y et al. Cryo-Em structure and assembly of an extracellular contractile injection system. Cell 2019; 177:370–383 [View Article]
    [Google Scholar]
  67. Vlisidou I, Hapeshi A, Healey JR, Smart K, Yang G et al. The Photorhabdus asymbiotica virulence cassettes deliver protein effectors directly into target eukaryotic cells. Elife 2019; 8:e46259 [View Article][PubMed]
    [Google Scholar]
  68. Chen L, Song N, Liu B, Zhang N, Alikhan N-F et al. Genome-Wide identification and characterization of a superfamily of bacterial extracellular contractile injection systems. Cell Rep 2019; 29:511–521 [View Article]
    [Google Scholar]
  69. Rocchi I, Ericson CF, Malter KE, Zargar S, Eisenstein F et al. A bacterial phage Tail-like structure kills eukaryotic cells by injecting a nuclease effector. Cell Rep 2019; 28:295–301 [View Article]
    [Google Scholar]
  70. Ericson CF, Eisenstein F, Medeiros JM, Malter KE, Cavalcanti GS et al. A contractile injection system stimulates tubeworm metamorphosis by translocating a proteinaceous effector. eLife 2019; 8:e46845 [View Article]
    [Google Scholar]
  71. Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ et al. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 2014; 343:529–533 [View Article][PubMed]
    [Google Scholar]
  72. Li Y, Hu X, Zhang X, Liu Z, Ding X et al. Photorhabdus luminescens PirAB-fusion protein exhibits both cytotoxicity and insecticidal activity. FEMS Microbiol Lett 2014; 356:23–31 [View Article]
    [Google Scholar]
  73. Ahantarig A, Chantawat N, Waterfield NR, ffrench-Constant R, Kittayapong P. PirAB toxin from Photorhabdus asymbiotica as a Larvicide against dengue vectors. Appl Environ Microbiol 2009; 75:4627–4629 [View Article]
    [Google Scholar]
  74. Waterfield N, George Kamita S, Hammock BD, Ffrench-Constant R. The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity. FEMS Microbiol Lett 2005; 245:47–52 [View Article]
    [Google Scholar]
  75. Bogdanović X, Schneider S, Levanova N, Wirth C, Trillhaase C et al. A cysteine protease–like domain enhances the cytotoxic effects of the Photorhabdus asymbiotica toxin PaTox. J Biol Chem 2019; 294:1035–1044 [View Article]
    [Google Scholar]
  76. Jank T, Bogdanović X, Wirth C, Haaf E, Spoerner M et al. A bacterial toxin catalyzing tyrosine glycosylation of Rho and deamidation of Gq and Gi proteins. Nat Struct Mol Biol 2013; 20:1273–1280 [View Article]
    [Google Scholar]
  77. Jank T, Trillhaase C, Brozda N, Steinemann M, Schwan C et al. Intracellular plasma membrane guidance of Photorhabdus asymbiotica toxin is crucial for cell toxicity. FASEB J. 2015; 29:2789–2802 [View Article]
    [Google Scholar]
  78. Ciche TA, Ensign JC. For the insect pathogen Photorhabdus luminescens, which end of a nematode is out?. Appl Environ Microbiol 2003; 69:1890–1897 [View Article][PubMed]
    [Google Scholar]
  79. Strauch O, Ehlers R-U. Food signal production of Photorhabdus luminescens inducing the recovery of entomopathogenic nematodes Heterorhabditis spp. in liquid culture. Appl Microbiol Biotechnol 1998; 50:369–374 [View Article]
    [Google Scholar]
  80. Joyce SA, Brachmann AO, Glazer I, Lango L, Schwär G et al. Bacterial biosynthesis of a multipotent stilbene. Angew Chem Int Ed Engl 2008; 47:1942–1945 [View Article][PubMed]
    [Google Scholar]
  81. Williams JS, Thomas M, Clarke DJ. The gene stlA encodes a phenylalanine ammonia-lyase that is involved in the production of a stilbene antibiotic in Photorhabdus luminescens TT01. Microbiology 2005; 151:2543–2550 [View Article]
    [Google Scholar]
  82. Chalabaev S, Turlin E, Bay S, Ganneau C, Brito-Fravallo E et al. Cinnamic acid, an autoinducer of its own biosynthesis, is processed via Hca enzymes in Photorhabdus luminescens . Appl Environ Microbiol 2008; 74:1717–1725 [View Article]
    [Google Scholar]
  83. Paik S, Kim GH, Park JS. A symbiotic bacterium Photorhabdus luminescens as a rich source of cinnamic acid and its analogue. J Ind Eng Chem 2005; 11:475–477
    [Google Scholar]
  84. Brachmann AO, Reimer D, Lorenzen W, Augusto Alonso E, Kopp Y et al. Reciprocal cross talk between fatty acid and antibiotic biosynthesis in a nematode symbiont. Angew Chem Int Ed 2012; 51:12086–12089 [View Article]
    [Google Scholar]
  85. Bai X, Adams BJ, Ciche TA, Clifton S, Gaugler R et al. A Lover and a fighter: the genome sequence of an entomopathogenic nematode Heterorhabditis bacteriophora . PLoS One 2013; 8:e69618 [View Article]
    [Google Scholar]
  86. Somvanshi VS, Gahoi S, Banakar P, Thakur PK, Kumar M et al. A transcriptomic insight into the infective juvenile stage of the insect parasitic nematode, Heterorhabditis indica . BMC Genomics 2016; 17:224–17 [View Article]
    [Google Scholar]
  87. Moshayov A, Koltai H, Glazer I. Molecular characterisation of the recovery process in the entomopathogenic nematode Heterorhabditis bacteriophora . Int J Parasitol 2013; 43:843–852 [View Article]
    [Google Scholar]
  88. Bargmann C, Horvitz H. Control of larval development by chemosensory neurons in Caenorhabditis elegans . Science 1991; 251:1243–1246 [View Article]
    [Google Scholar]
  89. Hallem EA, Rengarajan M, Ciche TA, Sternberg PW. Nematodes, bacteria, and flies: a tripartite model for nematode parasitism. Current Biology 2007; 17:898–904 [View Article]
    [Google Scholar]
  90. Richardson WH, Schmidt TM, Nealson KH. Identification of an anthraquinone pigment and a hydroxystilbene antibiotic from Xenorhabdus luminescens . Appl Environ Microbiol 1988; 54:1602–1605 [View Article]
    [Google Scholar]
  91. Paul VJ, Frautschy S, Fenical W, Nealson KH. Antibiotics in microbial ecology: Isolation and structure assignment of several new antibacterial compounds from the insect-symbiotic bacteria Xenorhabdus spp. J Chem Ecol 1981; 7:589–597
    [Google Scholar]
  92. Qin N, Tan X, Jiao Y, Liu L, Zhao W et al. RNA-Seq-based transcriptome analysis of methicillin-resistant Staphylococcus aureus biofilm inhibition by ursolic acid and resveratrol. Sci Rep 2015; 4:5467 [View Article]
    [Google Scholar]
  93. Hapeshi A, Benarroch JM, Clarke DJ, Waterfield NR. Iso-propyl stilbene: a life cycle signal?. Microbiology 2019; 165:516–526 [View Article]
    [Google Scholar]
  94. Brameyer S, Kresovic D, Bode HB, Heermann R. Dialkylresorcinols as bacterial signaling molecules. Proc Natl Acad Sci U S A 2015; 112:572–577 [View Article]
    [Google Scholar]
  95. Brachmann AO, Brameyer S, Kresovic D, Hitkova I, Kopp Y et al. Pyrones as bacterial signaling molecules. Nat Chem Biol 2013; 9:573–578 [View Article]
    [Google Scholar]
  96. Park HB, Sampathkumar P, Perez CE, Lee JH, Tran J et al. Stilbene epoxidation and detoxification in a Photorhabdus luminescens -nematode symbiosis. J. Biol. Chem. 2017; 292:6680–6694 [View Article]
    [Google Scholar]
  97. Smith SH, Jayawickreme C, Rickard DJ, Nicodeme E, Bui T et al. Tapinarof Is a Natural AhR Agonist that Resolves Skin Inflammation in Mice and Humans. J Invest Dermatol 2017; 137:2110–2119 [View Article][PubMed]
    [Google Scholar]
  98. Robbins K, Bissonnette R, Maeda-Chubachi T, Ye L, Peppers J et al. Phase 2, randomized dose-finding study of tapinarof (GSK2894512 cream) for the treatment of plaque psoriasis. J Am Acad Dermatol 2019; 80:714–721 [View Article]
    [Google Scholar]
  99. Peppers J, Paller AS, Maeda-Chubachi T, Wu S, Robbins K et al. A phase 2, randomized dose-finding study of tapinarof (GSK2894512 cream) for the treatment of atopic dermatitis. J Am Acad Dermatol 2019; 80:89–98 [View Article]
    [Google Scholar]
  100. Rowley CA, Kendall MM. To B12 or not to B12: five questions on the role of cobalamin in host-microbial interactions. PLoS Pathog 2019; 15:e1007479 [View Article]
    [Google Scholar]
  101. Yilmaz LS, Walhout AJM. Worms, bacteria, and micronutrients: an elegant model of our diet. Trends Genet 2014; 30:496–503 [View Article][PubMed]
    [Google Scholar]
  102. Rodionov DA, Vitreschak AG, Mironov AA, Gelfand MS. Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 2003; 278:41148–41159 [View Article][PubMed]
    [Google Scholar]
  103. Bowen DJ, Ensign JC. Isolation and characterization of intracellular protein inclusions produced by the entomopathogenic bacterium Photorhabdus luminescens . Appl Environ Microbiol 2001; 67:4834–4841 [View Article][PubMed]
    [Google Scholar]
  104. Bintrim SB, Ensign JC. Insertional inactivation of genes encoding the crystalline inclusion proteins of Photorhabdus luminescens results in mutants with pleiotropic phenotypes. J Bacteriol 1998; 180:1261–1269 [View Article][PubMed]
    [Google Scholar]
  105. Ciche TA, Blackburn M, Carney JR, Ensign JC. Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogen mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 2003; 69:4706–4713 [View Article][PubMed]
    [Google Scholar]
  106. Watson RJ, Millichap P, Joyce SA, Reynolds S, Clarke DJ. The role of iron uptake in pathogenicity and symbiosis in Photorhabdus luminescens TT01. BMC Microbiol 2010; 10:177 [View Article][PubMed]
    [Google Scholar]
  107. Somvanshi VS, Kaufmann-Daszczuk B, Kim K-S, Mallon S, Ciche TA. Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis. Mol Microbiol 2010; 77:1021–1038 [View Article][PubMed]
    [Google Scholar]
  108. Somvanshi VS, Sloup RE, Crawford JM, Martin AR, Heidt AJ et al. A Single Promoter Inversion Switches Photorhabdus Between Pathogenic and Mutualistic States. Science 2012; 337:88–93 [View Article]
    [Google Scholar]
  109. Easom CA, Joyce SA, Clarke DJ. Identification of genes involved in the mutualistic colonization of the nematode Heterorhabditis bacteriophora by the bacterium Photorhabdus luminescens . BMC Microbiol 2010; 10:45 [View Article][PubMed]
    [Google Scholar]
  110. Easom CA, Clarke DJ. HdfR is a regulator in Photorhabdus luminescens that modulates metabolism and symbiosis with the nematode Heterorhabditis . Environ Microbiol 2012; 14:953–966 [View Article][PubMed]
    [Google Scholar]
  111. McLean F, Berger D, Laetsch DR, Schwartz HT, Blaxter M. Improving the annotation of the Heterorhabditis bacteriophora genome. Gigascience 2018; 7:2012–12 [View Article][PubMed]
    [Google Scholar]
  112. Ratnappan R, Vadnal J, Keaney M, Eleftherianos I, O’Halloran D et al. RNAi-mediated gene knockdown by microinjection in the model entomopathogenic nematode Heterorhabditis bacteriophora . Parasit Vectors 2016; 9:1 [View Article]
    [Google Scholar]
  113. Ciche TA, Sternberg PW. Postembryonic RNAi in Heterorhabditis bacteriophora: a nematode insect parasite and host for insect pathogenic symbionts. BMC Dev Biol 2007; 7:101 [View Article][PubMed]
    [Google Scholar]
  114. Selvan S, Gaugler R, Lewis EE. Biochemical energy reserves of entomopathogenic nematodes. J Parasitol 1993; 79:167–172 [View Article]
    [Google Scholar]
  115. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 2005; 434:732–737 [View Article][PubMed]
    [Google Scholar]
  116. Turlings TCJ, Hiltpold I, Rasmann S. The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 2012; 358:51–60 [View Article]
    [Google Scholar]
  117. Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM et al. A sensory code for host seeking in parasitic nematodes. Curr Biol 2011; 21:377–383 [View Article][PubMed]
    [Google Scholar]
  118. Dillman AR, Guillermin ML, Lee JH, Kim B, Sternberg PW et al. Olfaction shapes host-parasite interactions in parasitic nematodes. Proc Natl Acad Sci U S A 2012; 109:E2324–E2333 [View Article][PubMed]
    [Google Scholar]
  119. Zhang X, Machado RA, Doan CV, Arce CC, Hu L et al. Entomopathogenic nematodes increase predation success by inducing cadaver volatiles that attract healthy herbivores. Elife 2019; 8:e46668 [View Article][PubMed]
    [Google Scholar]
  120. Castillo JC, Creasy T, Kumari P, Shetty A, Shokal U et al. Drosophila anti-nematode and antibacterial immune regulators revealed by RNA-Seq. BMC Genomics 2015; 16:519 [View Article][PubMed]
    [Google Scholar]
  121. Stubbendieck RM, Li H, Currie CR. Convergent evolution of signal-structure interfaces for maintaining symbioses. Curr Opin Microbiol 2019; 50:71–78 [View Article][PubMed]
    [Google Scholar]
  122. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 2018; 16:291–303 [View Article][PubMed]
    [Google Scholar]
  123. Noguez JH, Conner ES, Zhou Y, Ciche TA, Ragains JR et al. A novel ascaroside controls the parasitic life cycle of the entomopathogenic nematode Heterorhabditis bacteriophora . ACS Chem Biol 2012; 7:961–966 [View Article][PubMed]
    [Google Scholar]
  124. Choe A, von Reuss SH, Kogan D, Gasser RB, Platzer EG et al. Ascaroside signaling is widely conserved among nematodes. Curr Biol 2012; 22:772–780 [View Article][PubMed]
    [Google Scholar]
  125. Kaplan F, Alborn HT, von Reuss SH, Ajredini R, Ali JG et al. Interspecific nematode signals regulate dispersal behavior. PLoS One 2012; 7:e38735–38738 [View Article][PubMed]
    [Google Scholar]
  126. Hartley CJ, Lillis PE, Owens RA, Griffin CT. Infective juveniles of entomopathogenic nematodes (Steinernema and Heterorhabditis) secrete ascarosides and respond to interspecific dispersal signals. J Invertebr Pathol 2019; 168:107257 [View Article][PubMed]
    [Google Scholar]
  127. ffrench-Constant R, Waterfield N, Daborn P, Joyce S, Bennett H et al. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 2003; 26:433–456 [View Article][PubMed]
    [Google Scholar]
  128. Hu K, Webster JM. Antibiotic production in relation to bacterial growth and nematode development in Photorhabdus--Heterorhabditis infected Galleria mellonella larvae. FEMS Microbiol Lett 2000; 189:219–223 [View Article][PubMed]
    [Google Scholar]
  129. Brachmann AO, Joyce SA, Jenke-Kodama H, Schwär G, Clarke DJ et al. A type II polyketide synthase is responsible for anthraquinone biosynthesis in Photorhabdus luminescens . Chembiochem 2007; 8:1721–1728 [View Article][PubMed]
    [Google Scholar]
  130. Schmidt TM, Kopecky K, Nealson KH. Bioluminescence of the insect pathogen Xenorhabdus luminescens . Appl Environ Microbiol 1989; 55:2607–2612 [View Article][PubMed]
    [Google Scholar]
  131. Clarke DJ. The genetic basis of the symbiosis between Photorhabdus and its invertebrate hosts. Adv Appl Microbiol 2014; 88:1–29 [View Article][PubMed]
    [Google Scholar]
  132. Joyce SA, Clarke DJ. A hexA homologue from Photorhabdus regulates pathogenicity, symbiosis and phenotypic variation. Mol Microbiol 2003; 47:1445–1457 [View Article][PubMed]
    [Google Scholar]
  133. Killiny N. Generous hosts: Why the larvae of greater wax moth, Galleria mellonella is a perfect infectious host model?. Virulence 2018; 9:860–865 [View Article][PubMed]
    [Google Scholar]
  134. Wyatt GR. The biochemistry of insect hemolymph. Annu Rev Entomol 1961; 6:75–102 [View Article]
    [Google Scholar]
  135. Lango L, Clarke DJ. A metabolic switch is involved in lifestyle decisions in Photorhabdus luminescens . Mol Microbiol 2010; 77:1394–1405 [View Article][PubMed]
    [Google Scholar]
  136. Ronneau S, Hallez R. Make and break the alarmone: regulation of (p)ppGpp synthetase/hydrolase enzymes in bacteria. FEMS Microbiol Rev 2019; 191:2248–12
    [Google Scholar]
  137. Bager R, Roghanian M, Gerdes K, Clarke DJ. Alarmone (p)ppGpp regulates the transition from pathogenicity to mutualism in Photorhabdus luminescens . Mol Microbiol 2016; 100:735–747 [View Article][PubMed]
    [Google Scholar]
  138. Engel Y, Windhorst C, Lu X, Goodrich-Blair H, Bode HB. The global regulators LRP, LeuO, and HEXA control secondary metabolism in entomopathogenic bacteria. Front Microbiol 2017; 8:1278–13 [View Article][PubMed]
    [Google Scholar]
  139. Kontnik R, Crawford JM, Clardy J. Exploiting a global regulator for small molecule discovery in Photorhabdus luminescens . ACS Chem Biol 2010; 5:659–665 [View Article][PubMed]
    [Google Scholar]
  140. Langer A, Moldovan A, Harmath C, Joyce SA, Clarke DJ et al. HexA is a versatile regulator involved in the control of phenotypic heterogeneity of Photorhabdus luminescens . PLoS One 2017; 12:e0176535–23 [View Article][PubMed]
    [Google Scholar]
  141. Woodson SA, Panja S, Santiago-Frangos A. Proteins that chaperone RNA regulation. Microbiol Spectr 2018; 6:1–13 [View Article][PubMed]
    [Google Scholar]
  142. Hör J, Gorski SA, Vogel J. Bacterial RNA biology on a genome scale. Mol Cell 2018; 70:785–799 [View Article][PubMed]
    [Google Scholar]
  143. Tobias NJ, Heinrich AK, Eresmann H, Wright PR, Neubacher N et al. Photorhabdus-nematode symbiosis is dependent on hfq-mediated regulation of secondary metabolites. Environ Microbiol 2017; 19:119–129 [View Article][PubMed]
    [Google Scholar]
  144. Lango-Scholey L, Brachmann AO, Bode HB, Clarke DJ. The expression of stlA in Photorhabdus luminescens is controlled by nutrient limitation. PLoS One 2013; 8:e82152 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000907
Loading
/content/journal/micro/10.1099/mic.0.000907
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error