Atmospheric non-thermal plasma inactivation of Ascosphaera apis, the causative agent of chalkbrood disease in honeybee – Scientific Reports

  • Spiltoir, C. F. Life cycle of Ascosphaera apis (Pericystis apis). Am. J. Bot. 42, 501–508 (1955).

    Article 

    Google Scholar
     

  • Spiltoir, C. F. & Olive, L. S. A reclassification of the genus Pericystis betts. Mycologia 47(2), 238–244 (1955).

    Article 

    Google Scholar
     

  • Kluser, S. & Peduzzi, P. Global Pollinator Decline: A Literature Review—A Scientific Report About the Current Situation, Recent Findings and Potential Solution to Shed Light on the Global Pollinator Crisis (2007).

  • Bailey, L. Infectious Diseases of the Honeybee (ed. Bailey, L.). Vol. 176 (Land Books Ltd, 1963).

  • De Jong, D. Experimental enhancement of chalk brood infections. Bee World 57, 114–115 (1976).

    Article 

    Google Scholar
     

  • Gilliam, M., Iii, S. T. & Rose, J. B. Chalkbrood disease of honeybees, Apis mellifera L: A progress report. Apidologie 9, 75–89 (1978).

    Article 

    Google Scholar
     

  • Gilliam, M. & Vanderleyden, J. Honeybee Pests, Predators, and Diseases. 3rd ed. (AI Root, 1997).

  • Bailey, L. & Ball, B. V. Honeybee Pathology (Academic Press, 1991).


    Google Scholar
     

  • Nelson, D. & Ta, G. Field and laboratory studies on chalkbrood disease of honeybees. In Field and Laboratory Studies on Chalkbrood Disease of Honeybees (1982).

  • Aronstein, K. A. & Murray, K. D. Chalkbrood disease in honeybees. J. Invertebr. Pathol. 103, S20–S29 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Chantawannakul, P., Puchanichanthranon, T. & Wongsiri, S. Inhibitory effects of some medicinal plant extracts on the growth of Ascosphaera apis. Acta Hortic. https://doi.org/10.17660/ActaHortic.2005.678.26 (2005).

    Article 

    Google Scholar
     

  • Gilliam, M., Iii, S. T. & Richardson, G. V. Hygienic behavior of honeybees in relation to chalkbrood disease. Apidologie 14, 29–39 (1983).

    Article 

    Google Scholar
     

  • Liu, T. P. Ultrastructural changes in the spore and mycelia of Ascosphaera apis after treatment with benomyl (Benlate 50 W). Mycopathologia 116, 23–28 (1991).

    Article 

    Google Scholar
     

  • Calderone, N. W., Shimanuki, H. & Allen-Wardell, G. An in vitro evaluation of botanical compounds for the control of the honeybee pathogens Bacillus larvae and Ascosphaera apis, and the secondary invader B. alvei. J. Essent. Oil Res. 6, 279–287 (1994).

    Article 
    CAS 

    Google Scholar
     

  • Mourad, A. K., Zaghloul, O. A., El Kady, M. B., Nemat, F. M. & Morsy, M. E. A novel approach for the management of the chalkbrood disease infesting honeybee Apis mellifera L. (Hymenoptera: Apidae) colonies in Egypt. Commun. Agric. Appl. Biol. Sci. 70, 601–611 (2005).

    CAS 
    PubMed 

    Google Scholar
     

  • Chaimanee, V., Thongtue, U., Sornmai, N., Songsri, S. & Pettis, J. S. Antimicrobial activity of plant extracts against the honeybee pathogens, Paenibacillus larvae and Ascosphaera apis and their topical toxicity to Apis mellifera adults. JAM 123, 1160–1167 (2017).

    CAS 

    Google Scholar
     

  • Ansari, M. J. et al. In vitro evaluation of the effects of some plant essential oils on Ascosphaera apis, the causative agent of Chalkbrood disease. Saudi J. Biol. Sci. 24, 1001–1006 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Park, S. Y. & Ha, S.-D. Application of cold oxygen plasma for the reduction of Cladosporium cladosporioides and Penicillium citrinum on the surface of dried filefish (Stephanolepis cirrhifer) fillets. Int. J. Food Sci. Tech. 50, 966–973 (2015).

    Article 
    CAS 

    Google Scholar
     

  • Thirumdas, R. et al. Plasma activated water (PAW): Chemistry, physico-chemical properties, applications in food and agriculture. Trends Food Sci. Tech. 77, 21–31 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Guo, L. et al. Plasma-activated water: An alternative disinfectant for S protein inactivation to prevent SARS-CoV-2 infection. Chem. Eng. J. 421, 127742 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ott, L. C., Appleton, H. J., Shi, H., Keener, K. & Mellata, M. High voltage atmospheric cold plasma treatment inactivates Aspergillus flavus spores and deoxynivalenol toxin. Food Microbiol. 95, 103669 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cullen, P. J. & Milosavljević, V. Spectroscopic characterization of a radio-frequency argon plasma jet discharge in ambient air. PTEP 2015, 063J01 (2015).

  • Kang, M. H. et al. Differential inactivation of fungal spores in water and on seeds by ozone and arc discharge plasma. PLOS ONE 10, e0139263 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shen, J. et al. Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci. Rep. 6, 28505 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shaw, P. et al. Bacterial inactivation by plasma treated water enhanced by reactive nitrogen species. Sci. Rep. 8, 11268 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ki, S. H. et al. Influence of nonthermal atmospheric plasma-activated water on the structural, optical, and biological properties of Aspergillus brasiliensis spores. Appl. Sci. 10, 6378 (2020).

    Article 
    CAS 

    Google Scholar
     

  • Guo, D., Liu, H., Zhou, L., Xie, J. & He, C. Plasma-activated water production and its application in agriculture. J. Sci. Food Agric. 101, 4891–4899 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu, Y., Cheng, J.-H. & Sun, D.-W. Subcellular damages of Colletotrichum asianum and inhibition of mango anthracnose by dielectric barrier discharge plasma. Food Chem. 381, 132197 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lu, H., Patil, S., Keener, K. M., Cullen, P. J. & Bourke, P. Bacterial inactivation by high-voltage atmospheric cold plasma: Influence of process parameters and effects on cell leakage and DNA. J. Appl. Microbiol. 116, 784–794 (2014).

    Article 
    CAS 

    Google Scholar
     

  • Das, S., Gajula, V. P., Mohapatra, S., Singh, G. & Kar, S. Role of cold atmospheric plasma in microbial inactivation and the factors affecting its efficacy. Health Sci. Rev. 4, 100037 (2022).

    Article 

    Google Scholar
     

  • Dobrynin, D., Fridman, G., Friedman, G. & Fridman, A. Physical and biological mechanisms of direct plasma interaction with living tissue. New J. Phys. 11, 115020 (2009).

    Article 
    ADS 

    Google Scholar
     

  • Davies, B. W. et al. Dna damage and reactive nitrogen species are barriers to Vibrio cholerae colonization of the infant mouse intestine. PLOS Pathog. 7, e1001295 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Joshi, S. G. et al. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob. Agents Chem. 55, 1053–1062 (2011).

    Article 
    CAS 

    Google Scholar
     

  • Han, L. et al. Mechanisms of inactivation by high-voltage atmospheric cold plasma differ for Escherichia coli and Staphylococcus aureus. Appl. Environ. Microb. 82, 450–458 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Los, A., Ziuzina, D., Boehm, D., Cullen, P. J. & Bourke, P. Inactivation efficacies and mechanisms of gas plasma and plasma-activated water against Aspergillus flavus spores and biofilms: A comparative study. Appl. Environ. Microb. 86, e02619-e2719 (2020).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Phan, K. T. K. et al. Gliding arc discharge non-thermal plasma for retardation of mango anthracnose. LWT 105, 142–148 (2019).

    Article 
    CAS 

    Google Scholar
     

  • López, M. et al. A review on non-thermal atmospheric plasma for food preservation: Mode of action, determinants of effectiveness, and applications. Front. Microb. 10, 4 (2019).

    Article 

    Google Scholar
     

  • Wang, Z. et al. Inactivation of Alicyclobacillus contaminans in apple juice by dielectric barrier discharge plasma. Food Control 146, 109475 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Liao, X. et al. Inactivation mechanisms of non-thermal plasma on microbes: A review. Food Control 75, 83–91 (2017).

    Article 
    CAS 

    Google Scholar
     

  • Puligundla, P. & Mok, C. Inactivation of spores by nonthermal plasmas. World J. Microbiol. Biotechnol. 34, 143 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Lin, L. et al. Plasma activated Ezhangfeng cuji as innovative antifungal agent and its inactivation mechanism. AMB Expr. 13, 65 (2023).

    Article 
    CAS 

    Google Scholar
     

  • Weitz, H. J., Ballard, A. L., Campbell, C. D. & Killham, K. The effect of culture conditions on the mycelial growth and luminescence of naturally bioluminescent fungi. FEMS Microb. Lett. 202, 165–170 (2001).

    Article 
    CAS 

    Google Scholar
     

  • Veerana, M., Lim, J.-S., Choi, E.-H. & Park, G. Aspergillus oryzae spore germination is enhanced by non-thermal atmospheric pressure plasma. Sci. Rep. 9, 11184 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaftanoglu, O., Linksvayer, T. A. & Page, R. E. Rearing honeybees, Apis mellifera, in vitro I: Effects of sugar concentrations on survival and development. J. Insect Sci. 19, 96 (2011).


    Google Scholar
     

  • Zygaflo, J., Guzman, C. & Grosso, N. Antifungal properties of the leaf oils of Tagets minuta L. and T. fifolia lag. J. Essent. Oil Res. 6, 617–621 (1994).

    Article 

    Google Scholar
     

  • Ebadzadsahrai, G., Keppler, E. A. H., Soby, S. D. & Bean, H. D. Inhibition of fungal growth and induction od a novel volatilome in response to Chromobacterium vaccinii volatile organic compounds. Front. Microb. 11, 1035 (2020).

    Article 

    Google Scholar