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Antioxidant activities of four superoxide dismutases in Metarhizium robertsii and their contributions to pest control potential

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Abstract

The superoxide dismutase (SOD) family of Metarhizium robertsii, a fungal insect pathogen, comprises six members functionally unknown yet, including Cu/ZnSODs (Sod1/5/6), MnSODs (Sod2/3), and FeSOD (Sod4). Here, we show a mitochondrial localization of Sod3 and Sod4 and a requirement of either sod4 or sod6 for the fungal life as suggested by an inability to be deleted. We found remarked roles of Sod1, Sod2, and Sod3 in sustaining antioxidant activity and the fungal potential against insect pests but no role of Sod5 in all examined phenotypes. Intracellular SOD activity decreased by 49% in Δsod1 and 22% in either Δsod2 or Δsod3. The decreased SOD activities concurred with altered enzymographs, in which one of two SOD-active bands in wild-type and rescued strains disappeared in Δsod1 rather than in Δsod2 and another band disappeared in Δsod3. Consequently, maximal cell sensitivity to superoxide anions generated by oxidant menadione occurred in Δsod1, followed sequentially by Δsod3 and Δsod2. The latter two mutants were more sensitive than Δsod1 to oxidant H2O2. Transcriptional analysis revealed partial compensation of one or two partner genes upregulated for the absence of sod1, sod2, or sod3 and full compensation of three partners largely upregulated for the absence of sod5, as well as differential expression of most catalase genes in each Δsod mutant. The three mutants also suffered defects in conidial thermotolerance, UVB resistance, and virulence. These findings unveil that, to adapt to different host spectra and habitats, some major SODs in M. roberstii are functionally differentiated from those known previously in Beauveria bassiana, a classic insect mycopathogen lacking Sod6.

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Funding

This work was financially supported by the Ministry of Science and Technology of the People’s Republic of China (Grant No.: 2017YFD0201202), the National Natural Science Foundation of China (Grant No.: 31772218), and the Fundamental Research Funds for the Central Universities (Grant No.: 2018FZA6003).

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Authors and Affiliations

  1. Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, 310058, Zhejiang, China

    Xiao-Guan Zhu, Sen-Miao Tong, Sheng-Hua Ying & Ming-Guang Feng

  2. College of Agricultural and Food Science, Zhejiang A&F University, Lin’an, 311300, Zhejiang, China

    Sen-Miao Tong

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  1. Xiao-Guan Zhu
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  2. Sen-Miao Tong
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  3. Sheng-Hua Ying
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  4. Ming-Guang Feng
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Correspondence to Sen-Miao Tong or Ming-Guang Feng.

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The authors declare that they have no competing interests.

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This article does not contain any studies with human participants or animals other than Galleria mellonella moth larvae performed by any of the authors.

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Zhu, XG., Tong, SM., Ying, SH. et al. Antioxidant activities of four superoxide dismutases in Metarhizium robertsii and their contributions to pest control potential. Appl Microbiol Biotechnol 102, 9221–9230 (2018). https://doi.org/10.1007/s00253-018-9302-0

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  • DOI: https://doi.org/10.1007/s00253-018-9302-0

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