Skip to main content
Log in

The effects of fluctuating culture temperature on stress tolerance and antioxidase expression in Esteya vermicola

  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

The endoparasitic nematophagous fungus, Esteya vermicola, has shown great potential as a biological control agent against the pine wood nematode, Bursaphelenchus xylophilus. Fluctuating culture temperatures can affect fungal yields and fungal tolerance to desiccation, UV radiation, H2O2, and heat stress, as well as antioxidase expression. To explore these effects, E. vermicola cultured under five temperature ranges, 26°C, 15–26°C, 26–35°C, 20–30°C, and 15–35°C, were compared. The cultures grown at lower temperatures showed better growth, stronger tolerance to desiccation, UV, and H2O2 stresses, and increased catalase expression, However, these cultures also showed weaker heat stress tolerance and lower superoxide dismutase expression than the higher-temperature cultures. In particular, the E. vermicola cultured at 20–30°C, i.e., fluctuating in a narrow range around the optimal temperature, showed the best performance. Therefore, for production in practical applications, this narrowly fluctuating, moderate temperature appears to be optimal for yield and stress tolerance in E. vermicola.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abedi, T. and Pakniyat, H. 2010. Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech. J. Genet. Plant Breed 46, 27–34.

    CAS  Google Scholar 

  • Almeselmani, M., Deshmukh, P.S., Sairam, R.K., Kushwaha, S.R., and Singh, T.P. 2006. Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 171, 382–388.

    Article  CAS  PubMed  Google Scholar 

  • Avilla, J. and Copland, M.J.W. 1988. Development rate, number of mature oocytes at emergence and adult size of Encarsia tricolor at constant and variable temperatures. Entom. 33, 289–298.

    Article  Google Scholar 

  • Becker, D., Brinkmann, B.F., Zeis, B., and Paul, R.J. 2011. Acute changes in temperature or oxygen availability induce ROS fluctuations in Daphnia magna linked with fluctuations of reduced and oxidized glutathione, catalase activity and gene (haemoglobin) expression. Biol. Cell. 103, 351–363.

    Article  CAS  PubMed  Google Scholar 

  • Bowler, C., Montagu, M.V., and Inze, D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Biol. 43, 83–116.

    Article  CAS  Google Scholar 

  • Burgess, L.W. and Griffin, D.M. 1968. The influence of diurnal temperature fluctuations on the growth of fungi. New Phytol. 67, 131–137.

    Article  Google Scholar 

  • Dat, J.F., Lopez-Delgado, H., Foyer, C.H., and Scott, I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116, 1351–1357.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Di Capua, C., Bortolotti, A., Farías, M.E., and Cortez, N. 2011. UV resistant Acinetobacter sp. isolates from Andean wetlands display high catalase activity. FEMS Microbiol. Lett. 317, 181–189.

    Article  PubMed  Google Scholar 

  • Fangue, N.A., Hofmeister, M., and Schulte, P.M. 2006. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J. Exp. Biol. 209, 2859–2872.

    Article  CAS  PubMed  Google Scholar 

  • Gill, T., Sreenivasulu, Y., Kumar, S., and Ahuja, P.S. 2010. Overexpression of Potentilla superoxide dismutase improves salt stress tolerance during germination and growth in Arabidopsis thaliana. J. Plant Genet. Transgenics 1, 1–10.

    Google Scholar 

  • Gupta, A.S., Webb, R.P., Holaday, A.S., and Allen, R.D. 1993. Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol. 103, 1067–1073.

    PubMed Central  PubMed  Google Scholar 

  • Heise, K., Puntarulo, S., Nikinmaa, M., Abele, D., and Pörtner, H.O. 2006. Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L. J. Exp. Biol. 209, 353–363.

    Article  CAS  PubMed  Google Scholar 

  • Jalali-e-Emam, S.M.S., Alizadeh, B., Zaefizadeh, M., Zakarya, R.A., and Khayatnezhad, M. 2011. Superoxide dismutase (SOD) activity in NaCl stress in salt-sensitive and salt-tolerance genotypes of colza (Brassica napus L.). Middle East J. Sci. Res. 7, 7–11.

    CAS  Google Scholar 

  • Kubátová, A., Novotný, D., Prášil, K., and Mráček, Z. 2000. The nematophagous hyphomycete Esteya vermicola found in the Czech Republic. Czech Mycol. 52, 227–235.

    Google Scholar 

  • Liou, J.Y., Shih, J.Y., and Tzean, S.S. 1999. Esteya, a new nematophagous genus from Taiwan, attacking the pinewood nematode (Bursaphelenchus xylophilus). Mycol. Res. 103, 242–248.

    Article  Google Scholar 

  • Mohamed, E.A., Iwaki, T., Munir, I., Tamoi, M., Shigeoka, S., and Wadano, A. 2003. Overexpression of bacterial catalase in tomato leaf chloroplasts enhances photo-oxidative stress tolerance. Plant Cell Environ. 26, 2037–2046.

    Article  CAS  Google Scholar 

  • Montagnes, D.J. and Weisse, T. 2000. Fluctuating temperatures affect growth and production rates. Aquat. Microb. Ecol. 21, 97–102.

    Article  Google Scholar 

  • Nakano, K. and Iwama, G.K. 2002. The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: relationship of hsp70 and thermal tolerance. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 133, 79–94.

    Article  PubMed  Google Scholar 

  • Podrabsky, J.E. and Somero, G.N. 2004. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J. Exp. Biol. 207, 2237–2254.

    Article  CAS  PubMed  Google Scholar 

  • Prasad, T.K. 1996. Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J. 10, 1017–1026.

    Article  CAS  Google Scholar 

  • Prasad, T.K. 1997. Role of catalase in inducing chilling tolerance in pre-emergence maize seedlings. Plant Physiol. 114, 1369–1376.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Slade, D. and Radman, M. 2011. Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. R. 75, 133–191.

    Article  CAS  Google Scholar 

  • Tang, L., Kwon, S.Y., Kim, S.H., Kim, J.S., Choi, J.S., Cho, K.Y., and Lee, H.S. 2006. Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep. 25, 1380–1386.

    Article  CAS  PubMed  Google Scholar 

  • Terblanche, J.S., Nyamukondiwa, C., and Kleynhans, E. 2010. Thermal variability alters climatic stress resistance and plastic responses in a globally invasive pest, the Mediterranean fruit fly (Ceratitis capitata). Entomol. Exp. Appl. 137, 304–315.

    Article  Google Scholar 

  • Wang, Q., Dong, S., Tian, X., and Wang, F. 2007. Effects of circadian rhythms of fluctuating temperature on growth and biochemical composition of Ulva pertusa. Hydrobiologia 586, 313–319.

    Article  CAS  Google Scholar 

  • Wang, C.Y., Fang, Z.M., Sun, B.S., Gu, L.J., Zhang, K.Q., and Sung, C.K. 2008. High infectivity of an endoparasitic fungus strain, Esteya vermicola, against nematodes. J. Microbiol. 46, 380–389.

    Article  PubMed  Google Scholar 

  • Wang, C.Y., Fang, Z.M., Wang, Z., Gu, L.J., Sun, B.S., Zhang, D.L., and Sung, C.K. 2009. High infection activities of two Esteya vermicola isolates against pinewood nematode. Afr. J. Microbiol. Res. 3, 581–584.

    Google Scholar 

  • Wang, C.Y., Fang, Z.M., Wang, Z., Zhang, D.L., Gu, L.J., Lee, M.L., Liu, L., and Sung, C.K. 2011a. Biological control of the pinewood nematode Bursaphenlenchus xylophilus by application of the endoparasitic fungi Esteya vermicola. Biol. Control. 56, 91–100.

    Article  Google Scholar 

  • Wang, Y.B., Wang, C.Y., Wang, Z., Xue, J.J., Li, Z., Li, J.J., and Sung, C.K. 2012. Laboratory studies on the development of a conidial formulation of Esteya vermicola. Biocontrol Sci. Technol. 22, 1362–1372.

    Article  Google Scholar 

  • Wang, Z., Wang, C.Y., Yang, Z.H., Fang, Z.M., Moon, Y.J., Sun, B.S., and Sung, C.K. 2011b. Viability and pathogenicity of Esteya vermicola in pine trees. Biocontrol Sci. Technol. 21, 387–393.

    Article  Google Scholar 

  • Weydert, C.J. and Cullen, J.J. 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat. Protoc. 5, 51–66.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Van, M.M., and Van, C.W. 1997. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 16, 4806–4816.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xue, J., Zhang, Y., Wang, C., Wang, Y., Hou, J., Wang, Z., and Sung, C. 2013. Effect of nutrition and environmental factors on the endoparasitic fungus Esteya vermicola, a biocontrol agent against pine wilt disease. Curr. Microbiol. 67, 306–312.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Ervin, E.H., and Schmidt, R.E. 2005. The role of leaf pigment and antioxidant levels in UV-B resistance of dark-and light-green Kentucky bluegrass cultivars. J. Am. Soc. Hortic. Sci. 130, 836–841.

    CAS  Google Scholar 

  • Zhang, J. and Kirkham, M.B. 1994. Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol. 35, 785–791.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chang-keun Sung.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Yb., Pang, Wx., Yv, Xn. et al. The effects of fluctuating culture temperature on stress tolerance and antioxidase expression in Esteya vermicola . J Microbiol. 53, 122–126 (2015). https://doi.org/10.1007/s12275-015-4529-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-015-4529-2

Keywords

Navigation