Abstract
Acetyl-coenzyme A (CoA) synthetase (Acs) links cellular metabolism and physiology by catalyzing acetate and CoA into acetyl-CoA. However, the biological roles of Acs are not well studied in entomopathogenic fungi. In this study, two Acs proteins (BbAcs1 and BbAcs2) was functionally characterized in the filamentous insect pathogenic fungus Beauveria bassiana. BbAcs1 and BbAcs2 localize in cytoplasm and peroxisome, respectively. BbAcs1 contributes to vegetative growth on fatty acids as carbon source, and BbAcs2 did not. Both genes did not contribute to fungal response to stresses. The BbAcs1 loss conferred a slight influence on conidiation, and did not result in the defects in blastospore formation. On the contrary, BbAcs2 significantly contributes to lipid metabolism in germlings, blastospore formation, and virulence. The results indicated that Acs2 played a more predominant role than Acs1 in B. bassiana, which links the acetyl-CoA metabolism with the lifestyle of entomopathogenic fungi.
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References
Chen Y, Siewers V, Nielsen J (2012) Profiling of cytosolic and peroxisomal acetyl-CoA metabolism in Saccharomyces cerevisiae. PLoS ONE 7:e42475
De Cima S, Rúa J, Perdiguero E, del Valle P, Busto F, Baroja-Mazo A, de Arriaga D (2005) An acetyl-CoA synthetase not encoded by the facA gene is expressed under carbon starvation in Phycomyces blakesleeanus. Res Microbiol 156:663–669
Ding JL, Hou J, Feng MG, Ying SH (2020) Transcriptomic analyses reveal comprehensive responses of insect hemocytes to mycopathogen Beauveria bassiana, and fungal virulence-related cell wall protein assists pathogen to evade host cellular defense. Virulence 11:1352–1365
Ding JL, Hou J, Li XH, Feng MG, Ying SH (2021) Transcription activator Swi6 interacts with Mbp1 in MluI cell cycle box-binding complex and regulates hyphal differentiation and virulence in Beauveria bassiana. J Fungi (basel) 7:411
Ding JL, Peng YJ, Chu XL, Feng MG, Ying SH (2018) Autophagy-related gene BbATG11 is indispensable for pexophagy and mitophagy, and contributes to stress response, conidiation and virulence in the insect mycopathogen Beauveria bassiana. Environ Microbiol 20:3309–3324
Falcón AA, Chen S, Wood MS, Aris JP (2010) Acetyl-coenzyme A synthetase 2 is a nuclear protein required for replicative longevity in Saccharomyces cerevisiae. Mol Cell Biochem 333:99–108
Galdieri L, Zhang T, Rogerson D, Lleshi R, Vancura A (2014) Protein acetylation and acetyl coenzyme a metabolism in budding yeast. Eukaryot Cell 13:1472–1483
Gauthier GM (2015) Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog 11:e1004608
Gu Q, Yuan Q, Zhao D, Huang J, Hsiang T, Wei Y, Zheng L (2019) Acetyl-coenzyme A synthetase gene ChAcs1 is essential for lipid metabolism, carbon utilization and virulence of the hemibiotrophic fungus Colletotrichum higginsianum. Mol Plant Pathol 20:107–123
Karan D, David JR, Capy P (2001) Molecular evolution of the AMP-forming Acetyl-CoA synthetase. Gene 265:95–101
Klein HP, Jahnke L (1979) Effects of aeration on formation and localization of the acetyl coenzyme A synthetase of Saccharomyces cerevisiae. J Bacteriol 137:179–184
Lee S, Son H, Lee J, Min K, Choi GJ, Kim JC, Lee YW (2011) Functional analyses of two acetyl coenzyme A synthetases in the ascomycete Gibberella zeae. Eukaryot Cell 10:1043–1052
Lin HY, Pang MY, Feng MG, Ying SH (2022) A peroxisomal sterol carrier protein 2 Scp2 contributes to lipid trafficking in differentiation and virulence of the insect pathogenic fungus Beauveria bassiana. Fungal Genet Biol 158:103651
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 4:357–374
Ortiz-Urquiza A, Keyhani NO (2016) Molecular genetics of Beauveria bassiana infection of insects. Adv Genet 94:165–249
Peng YJ, Wang JJ, Lin HY, Ding JL, Feng MG, Ying SH (2020) HapX, an indispensable bZIP transcription factor for iron acquisition, regulates infection initiation by orchestrating conidial oleic acid homeostasis and cytomembrane functionality in mycopathogen Beauveria bassiana. mSystems 5:e00695-20
Peng YJ, Zhang H, Feng MG, Ying SH (2022) Steryl acetyl hydrolase 1 (BbSay1) links lipid homeostasis to conidiogenesis and virulence in the entomopathogenic fungus Beauveria bassiana. J Fungi (basel) 8:292
Pieuchot L, Jedd G (2012) Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu Rev Microbiol 66:237–263
Starai VJ, Escalante-Semerena JC (2004) Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci 61:2020–2030
Takahashi H, McCaffery JM, Irizarry RA, Boeke JD (2006) Nucleocytosolic acetyl-coenzyme A synthetase is required for histone acetylation and global transcription. Mol Cell 23:207–217
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
van den Berg MA, de Jong-Gubbels P, Kortland CJ, van Dijken JP, Pronk JT, Steensma HY (1996) The two acetylcoenzymeA synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptionalregulation. J Biol Chem 271:28953–28959
van den Berg MA, de Jong-Gubbels P, Kortland CJ, van Dijken JP, Pronk JT, Steensma HY (2004) The two acetyl-coenzyme A synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptional regulation. J Biol Chem 271:28953–28959
van den Berg MA, Steensma HY (1995) ACS2, a Saccharomyces cerevisiae gene encoding acetyl-coenzyme A synthetase, essential for growth on glucose. Eur J Biochem 231:704–713
Wang CS, Feng MG (2014) Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control 68:129–135
Wang JJ, Peng YJ, Ding JL, Feng MG, Ying SH (2020) Mitochondrial fission is necessary for mitophagy, development and virulence of the insect pathogenic fungus Beauveria bassiana. J Appl Microbiol 129:411–421
Ying SH, Liu J, Chu XL, Xie XQ, Feng MG (2016) The autophagy-related genes BbATG1 and BbATG8 have different functions in differentiation, stress resistance and virulence of mycopathogen Beauveria bassiana. Sci Rep 6:26376
Acknowledgements
The author thanks Dr. She-Long Zhang (Equipment and Technology Service Platform, College of Life Sciences, Zhejiang University) for his help with fluorescence microscopy.
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This research was supported by the National Natural Science Foundation of China (32170027 and 31972331) (S.Y.).
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jia-Hui Lei, Hai-Yan Lin, and Jin-Li Ding. The first draft of the manuscript was written by Jia-Hui Lei and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Lei, JH., Lin, HY., Ding, JL. et al. Functional characterization of two homologs of yeast acetyl-coenzyme A synthetase in the entomopathogenic fungus Beauveria bassiana. Arch Microbiol 204, 653 (2022). https://doi.org/10.1007/s00203-022-03269-y
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DOI: https://doi.org/10.1007/s00203-022-03269-y