Succinate Dehydrogenase Subunit C Contributes to Mycelial Growth and Development, Stress Response, and Virulence in the Insect Parasitic Fungus Beauveria bassiana

被引:22
作者
Ding, Jin-Li [1 ]
Li, Xiu-Hui [1 ]
Lei, Jia-Hui [1 ]
Feng, Ming-Guang [1 ]
Ying, Sheng-Hua [1 ]
机构
[1] Zhejiang Univ, Inst Microbiol, Coll Life Sci, Hangzhou, Peoples R China
基金
中国国家自然科学基金;
关键词
succinate dehydrogenase; entomopathogenic fungus; oxidative stress; development; virulence; ENTOMOPATHOGENIC FUNGI; HOST; TRANSCRIPTION; SUPEROXIDE; COMPLEX; BBSNF1;
D O I
10.1128/spectrum.02891-22
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
The electron transport chain (ETC) is critical for energy supply by mediating the electron flow along the mitochondrial membrane. Succinate dehydrogenase (SDH) is also known as complex II in the ETC, in which SdhC is a subunit anchored in mitochondrial membrane. However, the physiological roles of SdhC remain enigmatic in filamentous fungi. Succinate dehydrogenase (SDH), also known as respiratory chain complex II, plays a crucial role in energy production in which SdhC functions as an anchored subunit in the inner membrane of mitochondria. In this study, domain annotation analyses revealed that two SdhC domain-containing proteins were present in the filamentous insect-pathogenic fungus Beauveria bassiana, and they were named BbSdhC1 and BbSdhC2, respectively. Only BbSdhC1 localized to mitochondria; hence, this protein is considered the ortholog of SdhC in B. bassiana. Ablation of BbSdhC1 led to significantly reduced vegetative growth on various nutrients. The Delta Bbsdhc1 mutant displayed the significantly reduced ATP synthesis and abnormal differentiation under aerial and submerged conditions. Notably, the BbSdhC1 loss resulted in enhanced intracellular levels of reactive oxygen species (ROS) and impaired growth of mycelia under oxidative stress. Finally, insect bioassays (via cuticle and intrahemocoel injection infection) revealed that disruption of BbSdhC1 significantly attenuated fungal virulence against the insect hosts. These findings indicate that BbSdhC1 contributes to vegetative growth, resistance to oxidative stress, differentiation, and virulence of B. bassiana due to its roles in energy generation and maintaining the homeostasis of the intracellular ROS levels. IMPORTANCE The electron transport chain (ETC) is critical for energy supply by mediating the electron flow along the mitochondrial membrane. Succinate dehydrogenase (SDH) is also known as complex II in the ETC, in which SdhC is a subunit anchored in mitochondrial membrane. However, the physiological roles of SdhC remain enigmatic in filamentous fungi. In filamentous insect-pathogenic fungus B. bassiana, SdhC is required for maintaining mitochondrial functionality, which is critical for fungal stress response, development, and pathogenicity. These findings improve our understanding of physiological mechanisms of ETC components involved in pathogenicity of the entomopathogenic fungi.
引用
收藏
页数:13
相关论文
共 36 条
[1]   Mutations in the Membrane-Anchored SdhC Subunit Affect Fitness and Sensitivity to Succinate Dehydrogenase Inhibitors in Botrytis cinerea Populations from Multiple Hosts [J].
Amiri, Achour ;
Zuniga, Adrian, I ;
Peres, Natalia A. .
PHYTOPATHOLOGY, 2020, 110 (02) :327-335
[2]   Superoxide production in Galleria mellonella hemocytes:: Identification of proteins homologous to the NADPH oxidase complex of human neutrophils [J].
Bergin, D ;
Reeves, EP ;
Renwick, J ;
Wientjes, FB ;
Kavanagh, K .
INFECTION AND IMMUNITY, 2005, 73 (07) :4161-4170
[3]   Entomopathogenic Fungi: New Insights into Host-Pathogen Interactions [J].
Butt, T. M. ;
Coates, C. J. ;
Dubovskiy, I. M. ;
Ratcliffe, N. A. .
GENETICS AND MOLECULAR BIOLOGY OF ENTOMOPATHOGENIC FUNGI, 2016, 94 :307-364
[4]   Microbial virulence results from the interaction between host and microorganism [J].
Casadevall, A ;
Pirofski, LA .
TRENDS IN MICROBIOLOGY, 2003, 11 (04) :157-158
[5]   Respiratory complex II: Role in cellular physiology and disease Preface [J].
Cecchini, Gary .
BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS, 2013, 1827 (05) :541-542
[6]   Interactome analysis of transcriptional coactivator multiprotein bridging factor 1 unveils a yeast AP-1-like transcription factor involved in oxidation tolerance of mycopathogen Beauveria bassiana [J].
Chu, Xin-Ling ;
Dong, Wei-Xia ;
Ding, Jin-Li ;
Feng, Ming-Guang ;
Ying, Sheng-Hua .
CURRENT GENETICS, 2018, 64 (01) :275-284
[7]   Evolution of host resistance to insect pathogens [J].
Cory, Jenny S. .
CURRENT OPINION IN INSECT SCIENCE, 2017, 21 :54-59
[8]   Challenges and opportunities of the bio-pesticides production by solid-state fermentation: filamentous fungi as a model [J].
De la Cruz Quiroz, Reynaldo ;
Roussos, Sevastianos ;
Hernandez, Daniel ;
Rodriguez, Raul ;
Castillo, Francisco ;
Aguilar, Cristobal N. .
CRITICAL REVIEWS IN BIOTECHNOLOGY, 2015, 35 (03) :326-333
[9]   Mbp1, a component of the MluI cell cycle box-binding complex, contributes to morphological transition and virulence in the filamentous entomopathogenic fungus Beauveria bassiana [J].
Ding, Jin-Li ;
Lin, Hai-Yan ;
Feng, Ming-Guang ;
Ying, Sheng-Hua .
ENVIRONMENTAL MICROBIOLOGY, 2020, 22 (02) :584-597
[10]   Autophagy-related gene BbATG11 is indispensable for pexophagy and mitophagy, and contributes to stress response, conidiation and virulence in the insect mycopathogen Beauveria bassiana [J].
Ding, Jin-Li ;
Peng, Yue-Jin ;
Chu, Xin-Ling ;
Feng, Ming-Guang ;
Ying, Sheng-Hua .
ENVIRONMENTAL MICROBIOLOGY, 2018, 20 (09) :3309-3324