1887

Abstract

The entomopathogenic fungi and are ubiquitously distributed in soils. As insect pathogens they adhere to the insect cuticle and penetrate through to the insect haemocoel using a variety of cuticle-hydrolysing enzymes. Once in the insect haemocoel they are able to survive and replicate within, and/or evade, phagocytic haemocyte cells circulating in the haemolymph. The mechanism by which these soil fungi acquire virulence factors for insect infection and insect immune avoidance is unknown. We hypothesize that insect phagocytic cell avoidance in and is the consequence of a survival strategy against soil-inhabiting predatory amoebae. Microscopic examination, phagocytosis assays and amoeba mortality assays showed that these insect pathogenic fungi are phagocytosed by the soil amoeba and can survive and grow within the amoeba, resulting in amoeba death. Mammalian fungal and bacterial pathogens, such as and , respectively, show a remarkable overlap between survival against soil amoebae and survival against human macrophages. The insect immune system, particularly phagocytic haemocytes, is analogous to the mammalian macrophage. Our data suggest that the ability of the fungal insect pathogens and to survive insect phagocytic haemocytes may be a consequence of adaptations that have evolved in order to avoid predation by soil amoebae.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.038216-0
2010-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/7/2164.html?itemId=/content/journal/micro/10.1099/mic.0.038216-0&mimeType=html&fmt=ahah

References

  1. Bergin D., Reeves E. P., Renwick J., Wientjes F. B., Kavanagh K. 2005; Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73:4161–4170
    [Google Scholar]
  2. Bidochka M. J., Khachatourians G. G. 1987; Hemocytic defense response to the entomopathogenic fungus Beauveria bassiana in the migratory grasshopper Melanoplus sanguinipes. Entomol Exp Appl 45:151–156
    [Google Scholar]
  3. Bidochka M. J., Kamp A. M., DeCroos A. M. N. 2000; Insect pathogenic fungi: from genes to populations. In Fungal Pathology pp 171–193 Edited by Kronstad J. W. Dordrecht: Kluwer Academic Press;
    [Google Scholar]
  4. Bidochka M. J., Kamp A. M., Lavender T. M., DeKoning J., De Croos J. N. A. 2001; Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species?. Appl Environ Microbiol 67:1335–1342
    [Google Scholar]
  5. Bidochka M. J., Menzies F. V., Kamp A. M. 2002; Genetic groups of the insect-pathogenic fungus Beauveria bassiana are associated with habitat and thermal growth preferences. Arch Microbiol 178:531–537
    [Google Scholar]
  6. Chakraborty S., Old K. M. 1982; Mycophagous soil amoeba: interactions with three plant pathogenic fungi. Soil Biol Biochem 14:247–255
    [Google Scholar]
  7. Chakraborty S., Old K. M., Warcup J. H. 1983; Amoebae from a take-all suppressive soil which feed on Gaeumannomyces graminis tritici and other soil fungi. Soil Biol Biochem 15:17–24
    [Google Scholar]
  8. Cho E. M., Boucias D., Keyhani N. O. 2006a; EST analysis of cDNA libraries from the entomopathogenic fungus Beauveria ( Cordyceps) bassiana. II. Fungal cells sporulating on chitin and producing oosporein. Microbiology 152:2855–2864
    [Google Scholar]
  9. Cho E. M., Liu L., Farmerie W., Keyhani N. O. 2006b; EST analysis of cDNA libraries from the entomopathogenic fungus Beauveria ( Cordyceps) bassiana. I. Evidence for stage-specific gene expression in aerial conidia, in vitro blastospores and submerged conidia. Microbiology 152:2843–2854
    [Google Scholar]
  10. Cirillo J. D., Falkow S., Tompkins L. S., Bermudez L. E. 1997; Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 65:3759–3767
    [Google Scholar]
  11. Davies B., Chattings L. S., Edwards S. W. 1991; Superoxide generation during phagocytosis by Acanthamoeba castellanii: similarities to the respiratory burst of immune phagocytes. J Gen Microbiol 137:705–710
    [Google Scholar]
  12. Essig A., Heinemann M., Simnacher U., Marre R. 1997; Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl Environ Microbiol 63:1396–1399
    [Google Scholar]
  13. Fang W., Pei Y., Bidochka M. J. 2006; Transformation of Metarhizium anisopliae mediated by Agrobacterium tumefaciens. Can J Microbiol 52:623–626
    [Google Scholar]
  14. Gotz P., Boman H. G. 1985; Insect immunity. In Comprehensive Insect Physiology, Biochemistry and Pharmacology , vol. III pp 453–485 Edited by Kerkut G. A., Gilbert L. I. Oxford: Pergamon Press;
    [Google Scholar]
  15. Holder D. J., Keyhani N. O. 2005; Adhesion of the entomopathogenic fungus Beauveria ( Cordyceps) bassiana to substrata. Appl Environ Microbiol 71:5260–5266
    [Google Scholar]
  16. Holder D. J., Kirkland B. H., Lewis M. W., Keyhani N. O. 2007; Surface characteristics of the entomopathogenic fungus Beauveria ( Cordyceps) bassiana. Microbiology 153:3448–3457
    [Google Scholar]
  17. Hou R. F., Chang J. 1985; Cellular defense response to Beauveria bassiana in the silkworm, Bombyx mori. Appl Entomol Zool (Jpn 20:118–125
    [Google Scholar]
  18. Kurtti T. J., Keyhani N. O. 2008; Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae. Microbiology 154:1700–1709
    [Google Scholar]
  19. Levitz S. M. 2001; Does amoeboid reasoning explain the evolution and maintenance of virulence factors in Cryptococcus neoformans?. Proc Natl Acad Sci U S A 98:14760–14762
    [Google Scholar]
  20. Ly T. M., Muller H. E. 1990; Ingested Listeria monocytogenes survive and multiply in protozoa. J Med Microbiol 33:51–54
    [Google Scholar]
  21. Malliaris S. D., Steenbergen J. N., Casadevall A. 2004; Cryptococcus neoformans var. gattii can exploit Acanthamoeba castellanii for growth. Med Mycol 42:149–158
    [Google Scholar]
  22. Marolda C. L., Hauroder B., John M. A., Michel R., Valvano M. A. 1999; Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145:1509–1517
    [Google Scholar]
  23. Mylonakis E., Moreno R., El Khoury J. B., Idnurm A., Heitman J., Calderwood S. B., Ausubel F. M., Diener A. 2005; Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73:3842–3850
    [Google Scholar]
  24. Old K. M., Darbyshire J. F. 1978; Soil fungi as food for giant amoebae. Soil Biol Biochem 10:93–100
    [Google Scholar]
  25. Pendland J. C., Hung S. Y., Boucias D. G. 1993; Evasion of host defense by in vivo-produced protoplast-like cells of the insect mycopathogen Beauveria bassiana. J Bacteriol 175:5962–5969
    [Google Scholar]
  26. Roberts D. W., Hajek A. E. 1992; Entomopathogenic fungi as bioinsecticides. In Frontiers of Industrial Mycology pp 144–159 Edited by Leatham G. F. New York: Chapman and Hall;
    [Google Scholar]
  27. Scully L. R., Bidochka M. J. 2006; Developing insect models for the study of current and emerging human pathogens. FEMS Microbiol Lett 263:1–9
    [Google Scholar]
  28. Steenbergen J. N., Shuman H. A., Casadevall A. 2001; Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98:15245–15250
    [Google Scholar]
  29. Steenbergen J. N., Nosanchuk J. D., Malliaris S. D., Casadevall A. 2004; Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect Immun 72:3478–3488
    [Google Scholar]
  30. Swanson M. S., Hammer B. K. 2000; Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54:567–613
    [Google Scholar]
  31. Wang C., St. Leger R. J. 2006; A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci U S A 103:6647–6652
    [Google Scholar]
  32. Wang C., Hu G., St. Leger R. J. 2005; Differential gene expression by Metarhizium anisopliae growing in root exudate and host ( Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol 42:704–718
    [Google Scholar]
  33. Zimmermann G. 1986; The “ Galleria bait method” for detection of entomopathogenic fungi in soil. J Appl Entomol 102:212–215
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.038216-0
Loading
/content/journal/micro/10.1099/mic.0.038216-0
Loading

Data & Media loading...

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