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The cysteine-rich virulence factor NipA of Arthrobotrys flagrans interferes with cuticle integrity of Caenorhabditis elegans

Author

Listed:
  • Jennifer Emser

    (Karlsruhe Institute of Technology (KIT) - South Campus)

  • Nicole Wernet

    (Karlsruhe Institute of Technology (KIT) - South Campus)

  • Birgit Hetzer

    (Max Rubner-Institut (MRI) - Federal Research Institute of Nutrition and Food)

  • Elke Wohlmann

    (Karlsruhe Institute of Technology (KIT) - South Campus)

  • Reinhard Fischer

    (Karlsruhe Institute of Technology (KIT) - South Campus)

Abstract

Animals protect themself from microbial attacks by robust skins or a cuticle as in Caenorhabditis elegans. Nematode-trapping fungi, like Arthrobotrys flagrans, overcome the cuticle barrier and colonize the nematode body. While lytic enzymes are important for infection, small-secreted proteins (SSPs) without enzymatic activity, emerge as crucial virulence factors. Here, we characterized NipA (nematode induced protein) which A. flagrans secretes at the penetration site. In the absence of NipA, A. flagrans required more time to penetrate C. elegans. Heterologous expression of the fungal protein in the epidermis of C. elegans led to blister formation. NipA contains 13 cysteines, 12 of which are likely to form disulfide bridges, and the remaining cysteine was crucial for blister formation. We hypothesize that NipA interferes with cuticle integrity to facilitate fungal entry. Genome-wide expression analyses of C. elegans expressing NipA revealed mis-regulation of genes associated with extracellular matrix (ECM) maintenance and innate immunity.

Suggested Citation

  • Jennifer Emser & Nicole Wernet & Birgit Hetzer & Elke Wohlmann & Reinhard Fischer, 2024. "The cysteine-rich virulence factor NipA of Arthrobotrys flagrans interferes with cuticle integrity of Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50096-4
    DOI: 10.1038/s41467-024-50096-4
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    3. Xi Yu & Xiaodi Hu & Maria Pop & Nicole Wernet & Frank Kirschhöfer & Gerald Brenner-Weiß & Julia Keller & Mirko Bunzel & Reinhard Fischer, 2021. "Fatal attraction of Caenorhabditis elegans to predatory fungi through 6-methyl-salicylic acid," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Lay-Sun Ma & Lei Wang & Christine Trippel & Artemio Mendoza-Mendoza & Steffen Ullmann & Marino Moretti & Alexander Carsten & Jörg Kahnt & Stefanie Reissmann & Bernd Zechmann & Gert Bange & Regine Kahm, 2018. "The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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