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Comparative Transcriptomics of the Entomopathogenic Fungus Beauveria bassiana Grown on Aerial Surface and in Liquid Environment

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Abstract

Beauveria bassiana, the causative agent of arthropod, proliferates in the host hemolymph (liquid environment) and shits to saprotrophic growth on the host cadaver (aerial surface). In this study, we used transcriptomic analysis to compare the gene expression modes between these two growth phases. Of 10,366 total predicted genes in B. bassiana, 10,026 and 9985 genes were expressed in aerial (AM) and submerged (SM) mycelia, respectively, with 9853 genes overlapped. Comparative analysis between two transcriptomes indicated that there were 1041 up-regulated genes in AM library when compared with SM library, and 1995 genes were down-regulated, in particular, there were 7085 genes without significant change in expression between two transcriptomes. Furthermore, of 25 amidase genes (AMD), BbAMD5 has high expression level in both transcriptomes, and its protein product was associated with cell wall in aerial and submerged mycelia. Disruption of BbAMD5 significantly reduced mycelial hydrophobicity, hydrophobin translocation, and conidiation on aerial plate. Functional analysis also indicated that BbAmd5 was involved in B. bassiana blastospore formation in broth, but dispensable for fungal virulence. This study revealed the high similarity in global expression mode between mycelia grown under two cultivation conditions.

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References

  1. Lopez-Perez M, Rodriguez-Gomez D, Loera O (2015) Production of conidia of Beauveria bassiana in solid-state culture: current status and future perspectives. Crit Rev Biotechnol 35(3):334–341

    Article  CAS  PubMed  Google Scholar 

  2. Ortiz-Urquiza A, Keyhani NO (2016) Molecular genetics of Beauveria bassiana infection of insects. Adv Genet 94:165–249

    Article  CAS  PubMed  Google Scholar 

  3. Ding JL, Hou J, Feng MG et al (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(1):1352–1365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Peng YJ, Zhang H, Wang G et al (2024) MARVEL family proteins contribute to vegetative growth, development, and virulence of the insect fungal pathogen Beauveria bassiana. J Invertebr Pathol 203:108076

    Article  CAS  PubMed  Google Scholar 

  5. Ying SH (2024) Subcellular biochemistry and biology of filamentous entomopathogenic fungi. Adv Appl Microbiol. https://doi.org/10.1016/bs.aambs.2024.04.002

    Article  Google Scholar 

  6. Li C, **a Y, ** K (2022) The C2H2 zinc finger protein MaNCP1 contributes to conidiation through governing the nitrate assimilation pathway in the entomopathogenic fungus Metarhizium acridum. J Fungi (Basel) 8(9):942

    Article  CAS  PubMed  Google Scholar 

  7. He PH, Wang XX, Chu XL et al (2015) RNA sequencing analysis identifies the metabolic and developmental genes regulated by BbSNF1 during conidiation of the entomopathogenic fungus Beauveria bassiana. Curr Genet 61(2):143–152

    Article  PubMed  Google Scholar 

  8. Labahn J, Neumann S, Büldt G et al (2002) An alternative mechanism for amidase signature enzymes. J Mol Biol 322(5):1053–1064

    Article  CAS  PubMed  Google Scholar 

  9. Mantilla JG, Galeano NF, Gaitan AL et al (2012) Transcriptome analysis of the entomopathogenic fungus Beauveria bassiana grown on cuticular extracts of the coffee berry borer (Hypothenemus hampei). Microbiology-SGM 158(7):1826–1842

    Article  CAS  Google Scholar 

  10. **ao G, Ying SH, Zheng P et al (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hou C, Qin G, Liu T et al (2014) Transcriptome analysis of silkworm, Bombyx mori, during early response to Beauveria bassiana challenges. PLoS ONE 9(3):e91189

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Trapnell C, Williams BA, Pertea G et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Trapnell C, Hendrickson DG, Sauvageau M et al (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31(1):46–53

    Article  CAS  PubMed  Google Scholar 

  15. Priebe S, Kreisel C, Horn F et al (2015) FungiFun2: a comprehensive online resource for systematic analysis of gene lists from fungal species. Bioinformatics 31(3):445–446

    Article  CAS  PubMed  Google Scholar 

  16. Letunic I, Khedkar S, Bork P (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Res 49:D458–D460

    Article  CAS  PubMed  Google Scholar 

  17. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  18. Ding JL, Hou J, Li XH et al (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(6):411

    Article  CAS  PubMed  Google Scholar 

  19. He PH, Dong WX, Chu XL et al (2016) The cellular proteome is affected by a gelsolin (BbGEL1) during morphological transitions in aerobic surface versus liquid growth in the entomopathogenic fungus Beauveria bassiana. Environ Microbiol 18(11):4153–4169

    Article  CAS  PubMed  Google Scholar 

  20. Wang JJ, Peng YJ, Ding JL et al (2020) Mitochondrial fission is necessary for mitophagy, development and virulence of the insect pathogenic fungus Beauveria bassiana. J Appl Microbiol 129(2):411–421

    Article  CAS  PubMed  Google Scholar 

  21. Michielse CB, Hooykaas PJJ, van den Hondel CAMJJ et al (2008) Agrobacterium-mediated transformation of the filamentous fungus Aspergillus awamori. Nat Protoc 3:1671–1678

    Article  PubMed  Google Scholar 

  22. Li XH, Peng YJ, Ding JL et al (2022) A homologue of yeast acyl-CoA synthetase Faa1 contributes to cytomembrane functionality involved in development and virulence in the insect pathogenic fungus Beauveria bassiana. Microb Pathog 164:105419

    Article  CAS  PubMed  Google Scholar 

  23. Ding JL, Wei K, Feng MG et al (2024) Two aminopeptidase I homologs convergently contribute to pathobiology of fungal entomopathogen Beauveria bassiana via divergent physiology-dependent autophagy pathways for vacuolar targeting. J Adv Res 59:1–17

    Article  CAS  PubMed  Google Scholar 

  24. Ding JL, Lin HY, Feng MG et al (2020) Mbp1, a component of the MluI cell cycle box-binding complex, contributes to morphological transition and virulence in the filamentous entomopathogenic fungus Beauveria bassiana. Environ Microbiol 22(2):584–597

    Article  CAS  PubMed  Google Scholar 

  25. Gasch AP, Spellman PT, Kao CM et al (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11(12):4241–4257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bonaccorsi ED, Ferreira AJ, Chambergo FS et al (2006) Transcriptional response of the obligatory aerobe Trichoderma reesei to hypoxia and transient anoxia: implications for energy production and survival in the absence of oxygen. Biochemistry 45(12):3912–3924

    Article  CAS  PubMed  Google Scholar 

  27. Masuo S, Terabayashi Y, Shimizu M et al (2010) Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia. Mol Genet Genomics 284(6):415–424

    Article  CAS  PubMed  Google Scholar 

  28. Garrigues S, Kun RS, Peng M et al (2021) The cultivation method affects the transcriptomic response of Aspergillus niger to growth on sugar beet pulp. Microbiol Spectr 9(1):e0106421

    Article  PubMed  Google Scholar 

  29. López-Calleja AC, Cuadra T, Barrios-González J et al (2012) Solid-state and submerged fermentations show different gene expression profiles in cephalosporin c production by Acremonium chrysogenum. J Mol Microbiol Biotechnol 22(2):126–134

    PubMed  Google Scholar 

  30. Yakhnina AA, McManus HR, Bernhardt TG (2015) The cell wall amidase AmiB is essential for Pseudomonas aeruginosa cell division, drug resistance and viability. Mol Microbiol 97(5):957–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Modi M, Thambiraja M, Cherukat A et al (2024) Structure predictions and functional insights into Amidase_3 domain containing N-acetylmuramyl-L-alanine amidases from Deinococcus indicus DR1. BMC Microbiol 24(1):101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gauthier GM (2015) Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog 11(2):e1004608

    Article  PubMed  PubMed Central  Google Scholar 

  33. Li W, Lu J, Yang C et al (2022) An amidase contributes to full virulence of Sclerotinia sclerotiorum. Int J Mol Sci 23(19):11207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hou J, Lin H, Ding J et al (2022) Peroxins in peroxisomal receptor export system contribute to development, stress response, and virulence of insect pathogenic fungus Beauveria bassiana. J Fungi (Basel) 8(6):622

    Article  CAS  PubMed  Google Scholar 

  35. Dietsch R, Jakobs-Schönwandt D, Grünberger A et al (2021) Desiccation-tolerant fungal blastospores: from production to application. Curr Res Biotechnol 3:323–339

    Article  CAS  Google Scholar 

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Funding

This study was supported by National Natural Science Foundation of China (32170027).

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KW wrote the original manuscript. KW and JD performed the experiments. MF and SY reviewed and edited the manuscript. SY acquired the funding and supervised the study. All authors read and approved the final manuscript.

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Correspondence to Sheng-Hua Ying.

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Wei, K., Ding, JL., Feng, MG. et al. Comparative Transcriptomics of the Entomopathogenic Fungus Beauveria bassiana Grown on Aerial Surface and in Liquid Environment. Curr Microbiol 81, 249 (2024). https://doi.org/10.1007/s00284-024-03783-w

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