Conidial water affinity is an important characteristic for thermotolerance in entomopathogenic fungi

Biocontrol Science and Technology

Volumn 24, Issue 4, 2014, Pages 448-461

  Souza, Roberta K F ^a   Azevedo, Rosana F F ^a   Lobo, Anderson O ^a   Rangel, Drauzio E N ^a  

^a INSTITUTO DE PESQUISA E DESENVOLVIMENTO   (Brazil)

Author keywords

conidial surface tension; conidial thermotolerance; entomopathogenic fungi; hydrophobicity

Indexed keywords

ENTOMOPATHOGENIC ORGANISM; FUNGUS; GERMINATION; HYDROPHOBICITY; SPORE; SURFACE TENSION; TEMPERATURE TOLERANCE;

EID: 84896868910     PISSN: 09583157     EISSN: 13600478     Source Type: Journal    
DOI: 10.1080/09583157.2013.871223     Document Type: Article

References (59)

1. Ali, S., Wang, Z. Q., Ren, S. X., & Huang, Z. (2011). Superoxide dismutase production by Isaria fumosorosea on metals and its role in stress tolerance and fungal virulence. Biocontrol Science and Technology, 21, 1457-1469. doi:10.1080/09583157.2011.635784
2. Alston, D. G., Rangel, D. E. N., Lacey, L. A., Golez, H. G., Kim, J. J., & Roberts, D. W. (2005). Evaluation of novel fungal and nematode isolates for control of Conotrachelus nenuphar (Coleoptera: Curculionidae) larvae. Biological Control, 35, 163-171. doi:10.1016/j.biocontrol.2005.06.011
3. Arthurs, S., & Thomas, M. B. (2001). Effect of dose, pre-mortem host incubation temperature and thermal behaviour on host mortality, mycosis and sporulation of Metarhizium anisopliae var. acridum in Schistocerca gregaria. Biocontrol Science and Technology, 11, 411-420. doi:10.1080/09583150120055826
4. Bayry, J., Aimanianda, V., Guijarro, J. I., Sunde, M., & Latge, J. P. (2012). Hydrophobins - Unique fungal proteins. Plos Pathogens, 8, e1002700. doi:10.1371/journal.ppat.1002700
5. Boucias, D. G., Pendland, J. C., & Latge, J. P. (1988). Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Applied Environmental Microbiology, 54, 1795-1805.
6. Braga, G. U. L., Flint, S. D., Miller, C. D., Anderson, A. J., & Roberts, D. W. (2001). Variability in response to UV-B among species and strains of Metarhizium isolated from sites at latitudes from 61°N to 54°S. Journal of Invertebrate Pathology, 78, 98-108. doi:10.1006/jipa.2001.5048
7. Braga, G. U. L., Rangel, D. E. N., Flint, S. D., Anderson, A. J., & Roberts, D. W. (2006). Conidial pigmentation is important to tolerance against solar-simulated radiation in the entomopathogenic fungus Metarhizium anisopliae. Photochemistry and Photobiology, 82, 418-422. doi:10.1562/2005-05-08-RA-52
8. Braga, G. U. L., Rangel, D. E. N., Flint, S. D., Miller, C. D., Anderson, A. J., & Roberts, D. W. (2002). Damage and recovery from UV-B exposure in conidia of the entomopathogens Verticillium lecanii and Aphanocladium album. Mycologia, 94, 912-920. doi:10.2307/3761859
9. Bugeme, D. M., Maniania, N. K., Knapp, M., & Boga, H. I. (2008). Effect of temperature on virulence of Beauveria bassiana and Metarhizium anisopliae isolates to Tetranychus evansi. Experimental and Applied Acarology, 46, 275-285. doi:10.1007/s10493-008-9179-1
10. Cole, G. T., Sekiya, T., Kasai, R., Yokoyama, T., & Nozawa, Y. (1979). Surface ultrastructure and chemical composition of the cell walls of conidial fungi. Experimental Mycology, 3, 132-156. doi:10.1016/S0147-5975(79)80025-0
11. Crisan, E. V. (1973). Current concepts of thermophilism and the thermophilic fungi. Mycologia, 65, 1171-1198. doi:10.2307/3758296
12. Cruz, L. P., Gaitan, A. L., & Gongora, C. E. (2006). Exploiting the genetic diversity of Beauveria bassiana for improving the biological control of the coffee berry borer through the use of strain mixtures. Applied Microbiology and Biotechnology, 71, 918-926. doi:10.1007/s00253-005-0218-0
13. De la Rosa, W., Alatorre, R., Barrera, J. F., & Toreillo, C. (2000). Effect of Beauveria bassiana and Metarhizium anisopliae (Deuteromycetes) upon the coffee berry borer (Coleoptera: Scolytidae) under field conditions. Journal of Economic Entomology, 93, 1409-1414. doi:10.1603/0022-0493-93.5.1409
14. du Noüy, P. L. 1925. An interfacial tensiometer for universal use. The Journal of General Physiology, 7, 625-633. doi:10.1085/jgp.7.5.625
15. Ekesi, S., Maniania, N. K., & Ampong-Nyarko, K. (1999). Effect of temperature on germination, radial growth and virulence of Metarhizium anisopliae and Beauveria bassiana on Megalurothrips sjostedti. Biocontrol Science and Technology, 9, 177-185. doi:10.1080/09583159929767
16. Elliot, S. L., Blanford, S., & Thomas, M. B. (2002). Host-pathogen interactions in a varying environment: Temperature, behavioural fever and fitness. Proceedings of the Royal Society B-Biological Sciences, 269, 1599-1607. doi:10.1098/rspb.2002.2067
17. Faria, M., & Wraight, S. P. (2001). Biological control of Bemisia tabaci with fungi. Crop Protection, 20, 767-778. doi:10.1016/S0261-2194(01)00110-7
18. Faria, M. R., & Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43, 237-256. doi:10.1016/j.biocontrol.2007.08.001
19. Fernandes, E. K. K., Angelo, I. C., Rangel, D. E. N., Bahiense, T. C., Moraes, A. M., Roberts, D. W., & Bittencourt, V. R. (2011). An intensive search for promising fungal biological control agents of ticks, particularly Rhipicephalus microplus. Veterinary Parasitology, 182, 307-318. doi:10.1016/j.vetpar.2011.05.046
20. Fernandes, E. K. K., Keyser, C. A., Chong, J. P., Rangel, D. E. N., Miller, M. P., & Roberts, D. W. (2010). Characterization of Metarhizium species and varieties based on molecular analysis, heat tolerance and cold activity. Journal of Applied Microbiology, 108, 115-128. doi:10.1111/j.1365-2672.2009.04422.x
21. Fernandes, E. K. K., Rangel, D. E. N., Moraes, A. M. L., Bittencourt, V. R. E. P., & Roberts, D. W. (2008). Cold activity of Beauveria e Metarhizium, and thermotolerance of Beauveria. Journal of Invertebrate Pathology, 98, 69-78. doi:10.1016/j.jip.2007.10.011
22. Foster, R. N., Jaronski, S., Reuter, K. C., Black, L. R., Schlothauer, R., Harper, J., & Jech, L. E. (2011). Simulated aerial sprays for field cage evaluation of Beauveria bassiana and Metarhizium brunneum (Ascomycetes: Hypocreales) against Anabrus simplex (Orthoptera: Tettigoniidae) in Montana. Biocontrol Science and Technology, 21, 1331-1350. doi:10.1080/09583157.2011.620080
23. Girardin, H., Paris, S., Rault, J., Bellon-Fontaine, M. N., & Latge, J. P. (1999). The role of the rodlet structure on the physicochemical properties of Aspergillus conidia. Letters in Applied Microbiology, 29, 364-369. doi:10.1046/j.1472-765X.1999.00643.x
24. Heddergott, C., Bruns, S., Nietzsche, S., Leonhardt, I., Kurzai, O., Kniemeyer, O., & Brakhage, A. A. (2012). The Arthroderma benhamiae hydrophobin HypA mediates hydrophobicity and influences recognition by human immune effector cells. Eukaryotic Cell, 11, 673-682. doi:10.1128/EC.00037-12
25. Holder, D. J., & Keyhani, N. O. (2005). Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Applied and Environmental Microbiology, 71, 5260-5266. doi:10.1128/AEM.71.9.5260-5266.2005
26. Hywel-Jones, N. L., & Gillespie, A. T. (1990). Effect of temperature on spore germination in Metarhizium anisopliae and Beauveria bassiana. Mycological Research, 94, 389-392. doi:10.1016/S0953-7562(09)80363-8
27. Kim, S., Ahn, I. P., Rho, H. S., & Lee, Y. H. (2005). MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Molecular Microbiology, 57, 1224-1237.
28. Kim, J. S., Je, Y. H., & Roh, J. Y. (2010). Production of thermotolerant entomopathogenic Isaria fumosorosea SFP-198 conidia in corn-corn oil mixture. Journal of Industrial Microbiology & Biotechnology, 37, 419-423. doi:10.1007/s10295-010-0692-y
29. Kim, J. S., Kassa, A., Skinner, M., Hata, T., & Parker, B. L. (2011). Production of thermotolerant entomopathogenic fungal conidia on millet grain. Journal of Industrial Microbiology & Biotechnology, 38, 697-704. doi:10.1007/s10295-010-0850-2
30. Kim, J. S., Skinner, M., Hata, T., & Parker, B. L. (2010). Effects of culture media on hydrophobicity and thermotolerance of Bb and Ma conidia, with description of a novel surfactant based hydrophobicity assay. Journal of Invertebrate Pathology, 105, 322-328. doi:10.1016/j.jip.2010.08.008
31. Li, Z., Alves, S. B., Roberts, D. W., Fan, M., Delalibera, I., Tang, J., Rangel, D. E. N. (2010). Biological control of insects in Brazil and China: History, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Science and Technology, 20, 117-136. doi:10.1080/09583150903431665
32. Li, J., & Feng, M.-G. (2009). Intraspecific tolerance of Metarhizium anisopliae conidia to the upper thermal limits of summer with a description of a quantitative assay system. Mycological Research, 113, 93-99. doi:10.1016/j.mycres.2008.08.006
33. Linder, M. B., Szilvay, G. R., Nakari-Setala, T., & Penttila, M. E. (2005). Hydrophobins: The protein-amphiphiles of filamentous fungi. FEMS Microbiology Reviews, 29, 877-896. doi:10.1016/j.femsre.2005.01.004
34. Liu, H., Skinner, M., Brownbridge, M., & Parker, B. L. (2003). Characterization of Beauveria bassiana and Metarhizium anisopliae isolates for management of tarnished plant bug, Lygus lineolaris (Hemiptera: Miridae). Journal of Invertebrate Pathology, 82, 139-147. doi:10.1016/S0022-2011(03)00018-1
35. Lomer, C. J., Bateman, R. P., Johnson, D. L., Langewald, J., & Thomas, M. B. (2001). Biological control of locusts and grasshoppers. Annual Review of Entomology, 46, 667-702. doi:10.1146/annurev.ento.46.1.667
36. Luz, C., & Fargues, J. (1997). Temperature and moisture requirements for conidial germination of an isolate of Beauveria bassiana, pathogenic to Rhodnius prolixus. Mycopathologia, 138, 117-125. doi:10.1023/A:1006803812504
37. Ouedraogo, A., Fargues, J., Goettel, M. S., & Lomer, C. J. (1997). Effect of temperature on vegetative growth among isolates of Metarhizium anisopliae and M. flavoviride. Mycopathologia, 137, 37-43. doi:10.1023/A:1006882621776
38. Paris, S., Debeaupuis, J.-P., Crameri, R., Carey, M., Charles, F., Prevost, M.C., Latge, J. P. (2003). Conidial hydrophobins of Aspergillus fumigatus. Applied and Environmental Microbiology, 69, 1581-1588. doi:10.1128/AEM.69.3.1581-1588.2003
39. Rangel, D. E. N. (2011). Stress induced cross-protection against environmental challenges on prokaryotic and eukaryotic microbes. World Journal of Microbiology & Biotechnology, 27, 1281-1296. doi:10.1007/s11274-010-0584-3
40. Rangel, D. E. N., Anderson, A. J., & Roberts, D. W. (2006). Growth of Metarhizium anisopliae on non-preferred carbon sources yields conidia with increased UV-B tolerance. Journal of Invertebrate Pathology, 93, 127-134. doi:10.1016/j.jip.2006.05.011
41. Rangel, D. E. N., Anderson, A. J., & Roberts, D. W. (2008). Evaluating physical and nutritional stress during mycelial growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycological Research, 112, 1362-1372. doi:10.1016/j.mycres.2008.04.013
42. Rangel, D. E. N., Braga, G. U. L., Anderson, A. J., & Roberts, D. W. (2005). Variability in conidial thermotolerance of Metarhizium anisopliae isolates from different geographic origins. Journal of Invertebrate Pathology, 88, 116-125. doi:10.1016/j.jip.2004.11.007
43. Rangel, D. E. N., Butler, M. J., Torabinejad, J., Anderson, A. J., Braga, G. U. L., Day, A. W., & Roberts, D. W. (2006). Mutants and isolates of Metarhizium anisopliae are diverse in their relationships between conidial pigmentation and stress tolerance. Journal of Invertebrate Pathology, 93, 170-182. doi:10.1016/j.jip.2006.06.008
44. Rangel, D. E. N., & Correia, A. d. C. B. (2003). Virulencia de Aphanocladium album (Preuss) Gams e Verticillium lecanii (Zimm.) Viégas (Deuteromycotina: Hyphomycetes) para o percevejo-de-renda da seringueira, Leptopharsa heveae (Drake & Poor) (Hemiptera: Tingidae). Ciência e Agrotecnologia Edicao Especial, 1636-1642.
45. Rangel, D. E. N., Fernandes, É. K. K., Anderson, A. J., & Roberts, D. W. (2012). Culture of Metarhizium robertsii on salicylic-acid supplemented medium induces increased conidial thermotolerance. Fungal Biology, 116, 438-442. doi:10.1016/j.funbio.2012.01.003
46. Rangel, D. E. N., Fernandes, E. K. K., Braga, G. U. L., & Roberts, D. W. (2011). Visible light during mycelial growth and conidiation of Metarhizium robertsii produces conidia with increased stress tolerance. FEMS Microbiology Letters, 315, 81-86. doi:10.1111/j.1574-6968.2010.02168.x
47. Rangel, D. E. N., Fernandes, E. K. K., Dettenmaier, S. J., & Roberts, D. W. (2010). Thermotolerance of germlings and mycelium of the insect-pathogenic fungus Metarhizium spp. and mycelial recovery after heat stress. Journal of Basic Microbiology, 50, 344-350. doi:10.1002/jobm.200900430
48. Santi, L., Silva, L. A. D. E., da Silva, W. O. B., Correa, A. P. F., Rangel, D. E. N., Carlini, C.R., Vainstein, M. H. (2011). Virulence of the entomopathogenic fungus Metarhizium anisopliae using soybean oil formulation for control of the cotton stainer bug, Dysdercus peruvianus. World Journal of Microbiology & Biotechnology, 27, 2297-2303. doi:10.1007/s11274-011-0695-5
49. Santos, M. P., Dias, L. P., Ferreira, P. C., Pasin, L. A. A. P., & Rangel, D. E. N. (2011). Cold activity and tolerance of the entomopathogenic fungus Tolypocladium spp. to UV-B irradiation and heat. Journal of Invertebrate Pathology, 108, 209-213. doi:10.1016/j.jip.2011.09.001
50. Sevim, A., Donzelli, B. G. G., Wu, D., Demirbag, Z., Gibson, D. M., & Turgeon, B. G. (2012). Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are differentially expressed and corresponding mutants are decreased in virulence. Current Genetics, 58, 79-92. doi:10.1007/s00294-012-0366-6
51. Shan, L.-T., Wang, Z.-L., Ying, S.-H., & Feng, M.-G. (2010). Hydrophobicity-related protein contents and surface areas of aerial conidia are useful traits for formulation design of fungal biocontrol agents. Mycopathologia, 169, 483-494. doi:10.1007/s11046-010-9283-8
52. Sun, J., Fuxa, J. R., & Henderson, G. (2003). Effects of virulence, sporulation, and temperature on Metarhizium anisopliae and Beauveria bassiana laboratory transmission in Coptotermes formosanus. Journal of Invertebrate Pathology, 84, 38-46. doi:10.1016/S0022-2011(03)00122-8
53. Wessels, J. G. (1997). Hydrophobins: Proteins that change the nature of the fungal surface. Advances in Microbial Physiology, 38, 1-45.
54. Wösten, H. A. (2001). Hydrophobins: Multipurpose proteins. Annual Review of Microbiology, 55, 625-646. doi:10.1146/annurev.micro.55.1.625
55. Ying, S.-H., & Feng, M.-G. (2004). Relationship between thermotolerance and hydrophobin-like proteins in aerial conidia of Beauveria bassiana and Paecilomyces fumosoroseus as fungal biocontrol agents. Journal of Applied Microbiology, 97, 323-331. doi:10.1111/j.1365-2672.2004.02311.x
56. Ying, S.-H., & Feng, M.-G. (2006). Medium components and culture conditions affect the thermotolerance of aerial conidia of fungal biocontrol agent Beauveria bassiana. Letters in Applied Microbiology, 43, 331-335. doi:10.1111/j.1472-765X.2006.01947.x
57. Zhang, H., Liu, K., Zhang, X., Tang, W., Wang, J., Guo, M., Zhang, Z. (2011). Two phosphodiesterase genes, PDEL and PDEH, regulate development and pathogenicity by modulating intracellular cyclic AMP levels in Magnaporthe oryzae. PLoS One, 6, 1-15.
58. Zhang, S., Xia, Y. X., Kim, B., & Keyhani, N. O. (2011). Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Molecular Microbiology, 80, 811-826. doi:10.1111/j.1365-2958.2011.07613.x
59. Zimmermann, G. (1982). Effect of high temperatures and artificial sunlight on the viability of conidia of Metarhizium anisopliae. Journal of Invertebrate Pathology, 40, 36-40. doi:10.1016/0022-2011(82)90034-9