Phenotypic variation and host interactions of Xenorhabdus bovienii SS-2004, the entomopathogenic symbiont of Steinernema jollieti nematodes

Environmental Microbiology

Volumn 14, Issue 4, 2012, Pages 924-939

  Sugar, Darby R ^a   Murfin, Kristen E ^a   Chaston, John M ^a   Andersen, Aaron W ^a   Richards, Gregory R ^a   deLéon, Limaris ^a   Baum, James A ^b   Clinton, William P ^b   Forst, Steven ^c   Goldman, Barry S ^b   Krasomil Osterfeld, Karina C ^b   Slater, Steven ^a   Stock, S Patricia ^d   Goodrich Blair, Heidi ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MONSANTO COMPANY   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ANIMAL; ARTICLE; CLASSIFICATION; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE; MICROBIOLOGY; PHENOTYPE; PHYSIOLOGY; RHABDITIDA; SYMBIOSIS; VIRULENCE; XENORHABDUS;

ADOLESCENT; ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; PHENOTYPE; RHABDITIDA; SYMBIOSIS; VIRULENCE; XENORHABDUS;

BACTERIA (MICROORGANISMS); GALLERIA MELLONELLA; HEXAPODA; MANDUCA SEXTA; NEMATODA; STEINERNEMA JOLLIETI; XENORHABDUS; XENORHABDUS BOVIENII; XENORHABDUS NEMATOPHILA;

EID: 84859422792     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02663.x     Document Type: Article

References (85)

1. Akhurst, R.J. (1980) Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J Gen Microbiol 121: 303-310.
2. Akhurst, R.J. (1982) Antibiotic activity of Xenorhabdus spp. bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol 128: 3061-3065.
3. Akhurst, R.J., and Boemare, N. (1990) Biology and taxonomy of Xenorhabdus. In Entomopathogenic Nematodes in Biological Control. Gaugler, R., and Kaya, H.K. (eds). Boca Raton, FL, USA: CRC Press, pp. 75-87.
4. Akhurst, R.J., and Boemare, N.E. (1988) A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of Xenorhabdus nematophilus to species. J Gen Microbiol 134: 1835-1846.
5. Akhurst, R.J., Smigielski, A.J., Mari, J., Boemare, N., and Mourant, R.G. (1992) Restriction analysis of phase variation in Xenorhabdus spp. (Enterobacteriaceae), entomopathogenic bacteria associated with nematodes. Syst Appl Microbiol 15: 469-473.
6. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
7. Bao, Y., Lies, D.P., Fu, H., and Roberts, G.P. (1991) An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of Gram-negative bacteria. Gene 109: 167-168.
8. Baum, J.A., Bogaert, T., Clinton, W., Heck, G.R., Feldmann, P., Ilagan, O., etal. (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25: 1322-1326.
9. Bird, A.F., and Akhurst, R.J. (1983) The nature of the intestinal vesicle in nematodes of the family Steinernematidae. Int J Parasitol 13: 599-606.
10. Boemare, N.E., and Akhurst, R.J. (1988) Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacteriaceae). J Gen Microbiol 134: 751-761.
11. Boemare, N., Thaler, J.O., and Lanois, A. (1997) Simple bacteriological tests for phenotypic characterization of Xenorhabdus and Photorhabdus phase variants. Symbiosis 22: 167-175.
12. Campos-Herrera, R., Tailliez, P., Pages, S., Ginibre, N., Gutierrez, C., and Boemare, N.E. (2009) Characterization of Xenorhabdus isolates from La Rioja (Northern Spain) and virulence with and without their symbiotic entomopathogenic nematodes (Nematoda: Steinernematidae). J Invertebr Pathol 102: 173-181.
13. Chapuis, E., Emelianoff, V., Paulmier, V., Le Brun, N., Pages, S., Sicard, M., and Ferdy, J.B. (2009) Manifold aspects of specificity in a nematode-bacterium mutualism. J Evol Biol 22: 2104-2117.
14. Chaston, J.M., Suen, G., Tucker, S.L., Andersen, A.W., Bhasin, A., Bode, E., etal. (2011) The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes. PLoS ONE 6: e27909.
15. ffrench-Constant, R., and Waterfield, N. (2006) An ABC guide to the bacterial toxin complexes. Adv Appl Microbiol 58: 169-183.
16. Cowles, C.E., and Goodrich-Blair, H. (2004) Characterization of a lipoprotein, NilC, required by Xenorhabdus nematophila for mutualism with its nematode host. Mol Microbiol 54: 464-477.
17. Cowles, C.E., and Goodrich-Blair, H. (2008) The Xenorhabdus nematophila nilABC genes confer the ability of Xenorhabdus spp. to colonize Steinernema carpocapsae nematodes. J Bacteriol 190: 4121-4128.
18. Cowles, K.N., and Goodrich-Blair, H. (2005) Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell Microbiol 2: 209-219.
19. Cowles, K.N., Cowles, C.E., Richards, G.R., Martens, E.C., and Goodrich-Blair, H. (2007) The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol 9: 1311-1323.
20. Daborn, P.J., Waterfield, N., Silva, C.P., Au, C.P., Sharma, S., and ffrench-Constant, R.H. (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci USA 99: 10742-10747.
21. Ehlers, R.-U. (2001) Mass production of entomopathogenic nematodes for plant protection. Appl Microbiol Biotechnol 56: 623-633.
22. Emelianoff, V., Le Brun, N., Pagés, S., Stock, S.P., Tailliez, P., Moulia, C., and Sicard, M. (2008) Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Hérault and Gard (Southern France). J Invertebr Pathol 99: 20-27.
23. Fang, X.L., Li, Z.Z., Wang, Y.H., and Zhang, X. (2011) In vitro and in vivo antimicrobial activity of Xenorhabdus bovienii YL002 against Phytophthora capsici and Botrytis cinerea. J Appl Microbiol 111: 145-154.
24. Fischer-Le Saux, M., Mauleon, H., Constant, P., Brunel, B., and Boemare, N. (1998) PCR-ribotyping of Xenorhabdus and Photorhabdus isolates from the Caribbean region in relation to the taxonomy and geographic distribution of their nematode hosts. Appl Environ Microbiol 64: 4246-4254.
25. Fischer-Le Saux, M., Arteaga-Hernández, E., Mrácek, Z., and Boemare, N. (1999) The bacterial symbiont Xenorhabdus poinarii (Enterbacteriaceae) is harbored by two phylogenetic related host nematodes: the entomopathogenic species Steinernema cubanum and Steinernema glaseri (Nematoda: Steinernematidae). FEMS Microbiol Ecol 29: 149-157.
26. Flores-Lara, Y., Renneckar, D., Forst, S., Goodrich-Blair, H., and Stock, P. (2007) Influence of nematode age and culture conditions on morphological and physiological parameters in the bacterial vesicle of Steinernema carpocapsae (Nematoda: Steinernematidae). J Invertebr Pathol 95: 110-118.
27. Forst, S., and Clarke, D. (2002) Bacteria-nematode symbioses. In Entomopathogenic Nematology. Gaugler, R. (ed.). Wallingford, UK: CABI Publishing, pp. 57-77.
28. Fuchs, S.W., Proschak, A., Jaskolla, T.W., Karas, M., and Bode, H.B. (2011) Structure elucidation and biosynthesis of lysine-rich cyclic peptides in Xenorhabdus nematophila. Org Biomol Chem 9: 3130-3132.
29. Goetsch, M., Owen, H., Goldman, B., and Forst, S. (2006) Analysis of the PixA inclusion body protein of Xenorhabdus nematophila. J Bacteriol 188: 2706-2710.
30. Goodrich-Blair, H. (2007) They've got a ticket to ride: Xenorhabdus nematophila-Steinernema carpocapsae symbiosis. Curr Opin Microbiol 10: 225-230.
31. Götz, P., Bowman, A., and Bowman, H.G. (1981) Interactions between insect immunity and an insect-pathogenic nematode with symbiotic bacteria. Proc R Soc Lond B 212: 333-350.
32. Habibi, J., Backus, E.A., Coudron, T.A., and Brandt, S.L. (2001) Effect of different host substrates on hemipteran salivary protein profiles. Entomol Exp Appl 98: 369-375.
33. Habibi, J., Brandt, S.L., Coudron, T.A., Wagner, R.M., Wright, M.K., Backus, E.A., and Huesing, J.E. (2002) Uptake, flow, and digestion of casein and green fluorescent protein in the digestive system of Lygus hesperus Knight. Arch Insect Biochem Physiol 50: 62-74.
34. Hawlena, H., Bashey, F., and Lively, C.M. (2010) The evolution of spite: population structure and bacteriocin-mediated antagonism in two natural populations of xenorhabdus bacteria. Evolution Int J Org Evolution 64: 3198-3204.
35. Herbert, E.E., and Goodrich-Blair, H. (2007) Friend and foe: the two faces of Xenorhabdus nematophila. Nat Rev Microbiol 5: 634-646.
36. Herbert, E.E., Cowles, K.N., and Goodrich-Blair, H. (2007) CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila. Appl Environ Microbiol 73: 7826-7836.
37. Heungens, K., Cowles, C.E., and Goodrich-Blair, H. (2002) Identification of Xenorhabdus nematophila genes required for mutualistic colonization of Steinernema carpocapsae nematodes. Mol Microbiol 45: 1337-1353.
38. Jing, Y., Toubarro, D., Hao, Y., and Simoes, N. (2010) Cloning, characterisation and heterologous expression of an astacin metalloprotease, Sc-AST, from the entomoparasitic nematode Steinernema carpocapsae. Mol Biochem Parasitol 174: 101-108.
39. Kaya, H.K., and Stock, S.P. (1997) Techniques in insect nematology. In Manual of Techniques in Insect Pathology. Lacey, L.A. (ed.). London, UK: Academic Press, pp. 281-324.
40. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E., and Goodfellow, M. (eds). Oxford, UK: Blackwell, pp. 115-175.
41. Leclerc, M.C., and Boemare, N.E. (1991) Plasmids and phase variation in Xenorhabdus spp. Appl Environ Microbiol 57: 2597-2601.
42. Lee, M.M., and Stock, S.P. (2010a) A multigene approach for assessing evolutionary relationships of Xenorhabdus spp. (gamma-Proteobacteria), the bacterial symbionts of entomopathogenic Steinernema nematodes. J Invertebr Pathol 104: 67-74.
43. Lee, M.M., and Stock, S.P. (2010b) A multilocus approach to assessing co-evolutionary relationships between Steinernema spp. (Nematoda: Steinernematidae) and their bacterial symbionts Xenorhabdus spp. (gamma-Proteobacteria: Enterobacteriaceae). Syst Parasitol 77: 1-12.
44. Marchler-Bauer, A., and Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: W327-W331.
45. Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., etal. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: D205-D210.
46. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., etal. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
47. Martens, E.C., and Goodrich-Blair, H. (2005) The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation. Cell Microbiol 7: 1723-1735.
48. Martens, E.C., Heungens, K., and Goodrich-Blair, H. (2003) Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. J Bacteriol 185: 3147-3154.
49. Martens, E.C., Vivas, E.I., Heungens, K., Cowles, C.E., and Goodrich-Blair, H. (2004) Investigating mutualism between entomopathogenic bacteria and nematodes. Nematol Monogr Perspect 2: 447-462.
50. Martens, E.C., Russell, F.M., and Goodrich-Blair, H. (2005) Analysis of Xenorhabdus nematophila metabolic mutants yields insight into stages of Steinernema carpocapsae nematode intestinal colonization. Mol Microbiol 51: 28-45.
51. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
52. Mitani, D.K., Kaya, H.K., and Goodrich-Blair, H. (2004) Comparative study of the entomopathogenic nematode, Steinernema carpocapsae, reared on mutant and wild-type Xenorhabdus nematophila. Biol Control 29: 382-391.
53. Morales-Soto, N., and Forst, S.A. (2011) The xnp1 P2-like tail synthesis gene cluster encodes xenorhabdicin and is required for interspecies competition. J Bacteriol 193: 3624-3632.
54. Moureaux, N., Karjalainen, T., Givaudan, A., Bourlioux, P., and Boemare, N. (1995) Biochemical characterization and agglutinating properties of Xenorhabdus nematophilus F1 fimbriae. Appl Environ Microbiol 61: 2707-2712.
55. Mrácek, Z., Nguyen, K.B., Tailliez, P., Boemare, N., and Chen, S. (2006) Steinernema sichuanense n. sp. (Rhabditida, Steinernematidae), a new species of entomopathogenic nematode from the province of Sichuan, east Tibetan Mts., China. J Invertebr Pathol 93: 157-169.
56. Orchard, S.S., and Goodrich-Blair, H. (2004) Identification and functional characterization of a Xenorhabdus nematophila oligopeptide permease. Appl Environ Microbiol 70: 5621-5627.
57. Park, D., Ciezki, K., van der Hoeven, R., Singh, S., Reimer, D., Bode, H.B., and Forst, S. (2009) Genetic analysis of xenocoumacin antibiotic production in the mutualistic bacterium Xenorhabdus nematophila. Mol Microbiol 73: 938-949.
58. Park, Y., Herbert, E.E., Cowles, C.E., Cowles, K.N., Menard, M.L., Orchard, S.S., and Goodrich-Blair, H. (2007) Clonal variation in Xenorhabdus nematophila virulence and suppression of Manduca sexta immunity. Cell Microbiol 9: 645-656.
59. Pechy-Tarr, M., Bruck, D.J., Maurhofer, M., Fischer, E., Vogne, C., Henkels, M.D., etal. (2008) Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ Microbiol 10: 2368-2386.
60. Pinyon, R.A., Hew, F.H., and Thomas, C.J. (2000) Xenorhabdus bovienii T228 phase variation and virulence are independent of RecA function. Microbiology 146: 2815-2824.
61. Poinar, G.O. (1966) The presence of Achromobacter nematophilus in the infective stage of a Neoaplectana sp. (Steinernematidae: Nematoda). Nematologica 12: 105-108.
62. Poinar, G.O., and Thomas, G.M. (1966) Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 (Neoaplectana sp. Steinernematidae). Parasitology 56: 385-390.
63. Popiel, I., Grove, D.L., and Friedman, M.J. (1989) Infective juvenile formation in the insect parasitic nematode Steinernema feltiae. Parasitology 99: 77-81.
64. Richards, G.R., and Goodrich-Blair, H. (2009) Masters of conquest and pillage: Xenorhabdus nematophila global regulators control transitions from virulence to nutrient acquisition. Cell Microbiol 11: 1025-1033.
65. Richards, G.R., and Goodrich-Blair, H. (2010) Examination of Xenorhabdus nematophila lipases in pathogenic and mutualistic host interactions reveals a role for xlpA in nematode progeny production. Appl Environ Microbiol 76: 221-229.
66. Rowe, G.E., and Welch, R.A. (1994) Assays of hemolytic toxins. Methods Enzymol 235: 657-667.
67. San-Blas, E., Gowen, S.R., and Pembroke, B. (2008) Steinernema feltiae: ammonia triggers the emergence of their infective juveniles. Exp Parasitol 119: 180-185.
68. Sergeant, M., Jarrett, P., Ousley, M., and Morgan, J.A. (2003) Interactions of insecticidal toxin gene products from Xenorhabdus nematophilus PMFI296. Appl Environ Microbiol 69: 3344-3349.
69. Sicard, M., Le Brun, N., Pages, S., Godelle, B., Boemare, N., and Moulia, C. (2003) Effect of native Xenorhabdus on the fitness of their Steinernema hosts: contrasting types of interactions. Parasitol Res 91: 520-524.
70. Sierra, G. (1957) A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates. Antonie Van Leeuwenhoek 23: 15-22.
71. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology 1: 784-791.
72. Smits, W.K., Kuipers, O.P., and Veening, J.W. (2006) Phenotypic variation in bacteria: the role of feedback regulation. Nat Rev Microbiol 4: 259-271.
73. Snyder, H.A., Stock, S.P., Kim, S.K., Flores-Lara, Y., and Forst, S. (2007) New insights into the colonization and release process of Xenorhabdus nematophila and the morphology and ultrastructure of the bacterial receptacle of its nematode host, Steinernema carpocapsae. Appl Environ Microbiol 73: 5338-5346.
74. Spiridonov, S.E., Akhmedov, E.N., and Belostotskaya, F.N. (1991) Proliferation of symbiotic bacteria in the intestinal vesicles of invasive larvae of Neoaplectana spp. (Nematoda, Steinernematidae). Helminthologia 28: 141-142.
75. Spiridonov, S.E., Krasomil-Osterfeld, K., and Moens, M. (2004) Steinernema jollieti sp. n. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from the American Midwest. Russ J Nematol 12: 85-95.
76. Tailliez, P., Laroui, C., Ginibre, N., Paule, A., Pages, S., and Boemare, N. (2010) 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 60: 1921-1937.
77. Thaler, J.O., Duvic, B., Givaudan, A., and Boemare, N. (1998) Isolation and entomotoxic properties of the Xenorhabdus namatophilus F1 Lecithinase. Appl Environ Microbiol 64: 2367-2373.
78. Toubarro, D., Lucena-Robles, M., Nascimento, G., Santos, R., Montiel, R., Verissimo, P., etal. (2010) Serine protease-mediated host invasion by the parasitic nematode Steinernema carpocapsae. J Biol Chem 285: 30666-30675.
79. Vigneux, F., Zumbihl, R., Jubelin, G., Ribeiro, C., Poncet, J., Baghdiguian, S., etal. (2007) The xaxAB genes encoding a new apoptotic toxin from the insect pathogen Xenorhabdus nematophila are present in plant and human pathogens. J Biol Chem 282: 9571-9580.
80. Vivas, E.I., and Goodrich-Blair, H. (2001) Xenorhabdus nematophilus as a model for host-bacterium interactions: rpoS is necessary for mutualism with nematodes. J Bacteriol 183: 4687-4693.
81. Volgyi, A., Fodor, A., Szentirmai, A., and Forst, S. (1998) Phase variation in Xenorhabdus nematophilus. Appl Environ Microbiol 64: 1188-1193.
82. Waterfield, N., Dabord, P.J., Dowling, A.J., Yang, G., Hares, M., and ffrench-Constant, R.H. (2003) The insecticidal toxin makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen. FEMS Microbiol Lett 229: 265-270.
83. Wollenberg, M.S., and Ruby, E.G. (2009) Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two Oahu (Hawaii) populations. Appl Environ Microbiol 75: 193-202.
84. Xu, J., and Hurlbert, R.E. (1990) Toxicity of irradiated media for Xenorhabdus spp. Appl Environ Microbiol 56: 815-818.
85. Zhou, X., Kaya, H.K., Heungens, K., and Goodrich-Blair, H. (2002) Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Appl Environ Microbiol 68: 6202-6209.