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Sequential immunosuppressive activities of bacterial secondary metabolites from the entomopahogenic bacterium Xenorhabdus nematophila

  • Microbial Pathogenesis and Host-Microbe Interaction
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Abstract

The entomopathogenic bacterium Xenorhabdus nematophila secretes at least eight bacterial metabolites that play crucial roles suppressing target insect immune responses by inhibiting eicosanoid biosynthesis. We analyzed sequential changes in bacterial metabolite production during bacterial growth and analyzed their individual immunosuppressive activities against the insect host, Spodoptera exigua. X. nematophila exhibited a typical bacterial growth pattern in both insect host and culture medium, and eight metabolites were secreted at different time points. At the early growth phase (6–12 h), Ac-FGV and PHPP were detected in significant amounts in the culture broth. At this early phase, both Ac-FGV (18 μg/ml) and oxindole (110 μg/ml) levels significantly inhibited phenoloxidase and phospholipase A2 activities in S. exigua hemolymph. At the late growth phase (12–36 h), all eight metabolites were detected at significant levels (10–140 μg/ml) in the culture broth and were sufficient to induce hemocyte toxicity. These results suggest that X. nematophila sequentially produces immunosuppressive metabolites that might sequentially and cooperatively inhibit different steps of insect immune responses.

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References

  • Akhurst, R.J. 1980. Morphological and functional dimorphism in Xenorhabdus ssp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121, 303–309.

    Google Scholar 

  • Aymeric, J.L., Givaudan, A., and Duvic, B. 2010. Imd pathway is involved in the interaction of Drosophila melanogaster with the entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus luminescens. Mol. Immunol. 47, 2342–2348.

    Article  CAS  PubMed  Google Scholar 

  • Boonsuepsakul, S., Luepromchai, E., and Rongnoparut, P. 2008. Characterization of Anopheles minimus CYP6AA3 expressed in a recombinant baculovirus system. Arch. Insect Biochem. Physiol. 69, 13–21.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 71, 248–254.

    Article  Google Scholar 

  • Cerenius, L. and Söberhäll, K. 2004. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198, 116–126.

    Article  CAS  PubMed  Google Scholar 

  • Cho, S. and Kim, Y. 2004. Hemocyte apoptosis is induced by entomopathogenic bacteria, Xenorhabdus and Photorhabdus, in Bombyx mori. J. Asia Pac. Entomol. 7, 195–200.

    Article  Google Scholar 

  • Cinque, B., Fanini, D., Di Marzio, L., Palumbo, O., La Torre, C., Donato, V., Velardi, E., Bruscoli, S., Riccardi, C., and Cifone, M.G. 2008. Involvement of cPLA2 inhibition in dexamethasone-induced thymocyte apoptosis. J. Immunopathol. Pharmacol. 21, 539–551.

    CAS  Google Scholar 

  • Costa-Junior, H.M., Hamaty, F.C., da Silva Farias, R., Einicker-Lamas, M., da Silva, M.H., and Persechini, P.M. 2006. Apoptosis-inducing factor of a cytotoxic T cell line: involvement of a secretory phospholipase A2. Cell Tissue Res. 324, 255–266.

    Article  CAS  PubMed  Google Scholar 

  • Cowles, K. and Goodrich-Blair, H. 2005. Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell. Microbiol. 7, 209–219.

    Article  CAS  PubMed  Google Scholar 

  • Dunphy, G.B. and Webster, J.M. 1984. Interaction of Xenorhabdus nematophila subsp. nematophila with the hemolymph of Galleria mellonella. J. Insect Physiol. 30, 883–889.

    Article  Google Scholar 

  • Foukas, L.C., Atsoulas, H.L., Paraskevopoulou, N., Metheniti, A., Lambropoulou, M., and Marmaras, V.J. 1998. Phagocytosis of Escherichia coli by insect hemocytes requires both activation of the Ras/mitogen-activated protein kinase signal transduction pathway for attachment and β3 integrin for internalization. J. Biol. Chem. 273, 14813–14818.

    Article  CAS  PubMed  Google Scholar 

  • Fraga, B.M., Diaz, C.E., Guadano, A., and Gonzalez-Coloma, A. 2005. Diterpenes from Salvia broussonetii transformed roots and their insecticidal activity. J. Argric. Food Chem. 53, 5200–5206.

    Article  CAS  Google Scholar 

  • Gillespie, J.P., Kanost, M.R., and Trenczek, T. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42, 611–643.

    Article  CAS  PubMed  Google Scholar 

  • Goh, H.G., Lee, S.G., Lee, B.P., Choi, K.M., and Kim, J.H. 1990. Simple mass-rearing of beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), on an artificial diet. Kor. J. Appl. Entomol. 29, 180–183.

    Google Scholar 

  • Gupta, A.P. and Campenot, E.S. 1996. Cytoskeletal F-actin polymerization from cytosolic G-actin occurs in the phagocytosing immunocytes of arthropods (Limulus polyphemus and Gromphadorhina poetentosa): dose [cAMP]i play any role? J. Invertebr. Pathol. 68, 118–130.

    Article  CAS  PubMed  Google Scholar 

  • Horohov, D.W. and Dunn, P.E. 1983. Phagocytosis and nodule formation by hemocytes of Manduca sexta following injection of Pseudomonas aeruginosa. J. Invertebr. Pathol. 41, 203–213.

    Article  Google Scholar 

  • Hultmark, D. 2003. Drosophila immunity: paths and patterns. Cell 5, 360–361.

    CAS  Google Scholar 

  • Ji, D. and Kim, Y. 2004. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits the expression of an antibacterial peptide, cecropin, of the beet armyworm, Spodoptera exigua. J. Insect Physiol. 50, 489–496.

    Article  CAS  PubMed  Google Scholar 

  • Kaya, H.K. and Gaugler, R. 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38, 1–206.

    Article  Google Scholar 

  • Kim, Y., Ji, D., Cho, S., and Park, Y. 2005. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression. J. Invertebr. Pathol. 89, 258–264.

    Article  CAS  PubMed  Google Scholar 

  • Kim, G.S. and Kim, Y. 2010. Up-regulation of circulating hemocyte population in response to bacterial challenge is mediated by octopamine and 5-hydroxytryptamine via Rac1 signal in Spodoptera exigua. J. Insect Physiol. 56, 559–566.

    Article  CAS  PubMed  Google Scholar 

  • Kim, G.S., Nalini, M., Lee, D.W., and Kim, Y. 2009. Octopamine and 5-hydroxytryptamine mediate hemocytic phagocytosis and nodule formation via eicosanoids in the beet armyworm, Spodoptera exigua. Arch. Insect Biochem. Physiol. 70, 162–176.

    Article  CAS  PubMed  Google Scholar 

  • Kim, K., Park, Y., Kim, Y., and Lee, Y. 2001. Study on the inoculation augmentation of Paecilomyces japonicus to the silkworm, Bombyx mori, using dexamethasone. Kor. J. Appl. Entomol. 40, 51–58.

    Google Scholar 

  • Lavine, M.D. and Strand, M.R. 2002. Insect hemocytes and their role in cellular immune responses. Insect Biochem. Mol. Biol. 32, 1237–1242.

    Article  Google Scholar 

  • Lee, S., Shrestha, S., Prasad, S.V., and Kim, Y. 2011. Role of a small G protein Ras in cellular response of the beet armyworm, Spo doptera exigua. J. Insect Physiol. 57, 356–362.

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre, B. and Hoffmann, J. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697–743.

    Article  CAS  PubMed  Google Scholar 

  • Marmaras, V.J. and Lampropoulou, M. 2009. Regulators and signaling in insect haemocyte immunity. Cell Signal. 21, 186–195.

    Article  CAS  PubMed  Google Scholar 

  • Nappi, A.J. and Vass, E. 1998. Hydrogen peroxide production in immune-reactive Drosophila melanogaster. J. Parasitol. 84, 1150–1157.

    Article  CAS  PubMed  Google Scholar 

  • Paladi, M. and Tepass, U. 2004. Function of Rho GTPases in embryonic blood cell migration in Drosophila. J. Cell Sci. 117, 6313–6326.

    Article  CAS  PubMed  Google Scholar 

  • Park, D. and Forst, S. 2005. Co-regulation of motility, exoenzyme and antibiotic production by the EnvZ-OmpR-FlhDC-FliA pathway in Xenorhabdus nematophila. Mol. Microbiol. 61, 1397–1412.

    Article  Google Scholar 

  • Park, Y. and Kim, Y. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophila, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 46, 1469–1476.

    Article  CAS  PubMed  Google Scholar 

  • Park, Y., Kim, Y., and Yi, Y. 1999. Identification and characterization of a symbiotic bacterium associated with Steinernema carpocapsae in Korea. J. Asia Pac. Entomol. 2, 105–111.

    Article  Google Scholar 

  • Radvanyi, F., Jordan, L., Russo-Marie, F., and Bon, C. 1989. A sensitive and continuous fluorometric assay for phospholipase A2 using pyrene-labeled phospholipids in the presence of serum albumin. Anal. Biochem. 177, 103–109.

    Article  CAS  PubMed  Google Scholar 

  • Ratcliff, N.A. and Gots, P. 1990. Functional studies on insect haemocytes, including nonself recognition. Res. Immunol. 141, 919–923.

    Article  Google Scholar 

  • Ribeiro, C., Petit, V., and Affolter, M. 2003. Signaling systems, guided cell migration, and organogenesis: insights from genetic studies in Drosophila. Dev. Biol. 260, 1–8.

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute, Inc. 1989. SAS/STAT user’s guide, Release 6.03, Ed. Cary, N.C.

    Google Scholar 

  • Seo, S. and Kim, Y. 2011. Development of “Bt-Plus” biopesticide using entomopathogenic bacteria (Xenorhbadus nematophila, Photorhabdus temperata ssp. temperata) metabolites. Kor. J. Appl. Entomol. 50, 171–178.

    Article  Google Scholar 

  • Seo, S., Lee, S., Hong, Y., and Kim, Y. 2012. Phospholipase A2 inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl. Environ. Microbiol. 78, 3816–3823.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shrestha, S., Hong, Y.P., and Kim, Y. 2010. Two chemical derivatives of bacterial metabolites suppress cellular immune responses and enhance pathogenicity of Bacillus thuringiensis against the diamondback moth, Plutella xylostella. J. Asia Pac. Entomol. 13, 55–60.

    Article  CAS  Google Scholar 

  • Shrestha, S. and Kim, Y. 2007. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocyte phagocytosis of Spodoptera exigua by inhibiting phospholipase A2. J. Invertebr. Pathol. 96, 64–70.

    Article  PubMed  Google Scholar 

  • Shrestha, S. and Kim, Y. 2008. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm, Spodoptera exigua. Insect Biochem. Mol. Biol. 38, 99–112.

    Article  CAS  PubMed  Google Scholar 

  • Shrestha, S. and Kim, Y. 2009. Biochemical characteristics of immune-associated phospholipase A2 and its inhibition by an entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. 47, 774–782.

    Article  CAS  PubMed  Google Scholar 

  • Stanley, D. and Kim, Y. 2011. Prostaglandins and their receptors in insect biology. Front. Endocrinol. 2, 1–11.

    Article  Google Scholar 

  • Vigneux, F., Zumbihl, R., Jubelin, G., Ribeiro, C., Poncet, J., Baghdiguian, S., Givaudan, A., and Brehélin, M. 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. 13, 9571–9580.

    Article  Google Scholar 

  • Williams, M.J., Habayeb, M.S., and Hultmark, D. 2007. Reciprocal regulation of Rac1 and Rho1 in Drosophila circulating immune surveillance cells. J. Cell Sci. 120, 502–511.

    Article  CAS  PubMed  Google Scholar 

  • Winter, P., Rayne, R.C., and Coast, G.M. 2007. The effects of intracellular signaling pathway inhibitors on phagocytosis by haemocytes of Manduca sexta. J. Insect Physiol. 53, 975–982.

    Article  PubMed  Google Scholar 

  • Zettervall, C.J., Anderl, I., Williams, M.J., Palmer, R., Kurucz, E., Ando, I., and Hultmark, D. 2004. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101, 14192–14197.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Yonggyun Kim.

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Eom, S., Park, Y. & Kim, Y. Sequential immunosuppressive activities of bacterial secondary metabolites from the entomopahogenic bacterium Xenorhabdus nematophila . J Microbiol. 52, 161–168 (2014). https://doi.org/10.1007/s12275-014-3251-9

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  • DOI: https://doi.org/10.1007/s12275-014-3251-9

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