Non-thermal atmospheric pressure plasma inactivation of Paenibacillus larvae, the causative agent of American foulbrood in honeybees (Apis mellifera)

non-thermal-atmospheric-pressure-plasma-inactivation-of-paenibacillus-larvae,-the-causative-agent-of-american-foulbrood-in-honeybees-(apis-mellifera)
Non-thermal atmospheric pressure plasma inactivation of Paenibacillus larvae, the causative agent of American foulbrood in honeybees (Apis mellifera)

References

  1. Genersch, E. et al. Reclassification of Paenibacillus larvae subsp. Pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Microbiol. 56, 501–511 (2006).

    Google Scholar 

  2. Yue, D., Nordhoff, M., Wieler, L. H. & Genersch, E. Fluorescence in situ hybridization (FISH) analysis of interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ. Microbiol. 10, 1612–1620 (2008).

    Google Scholar 

  3. Dancer, B. N. & Chantawannakul, P. The protease of American foulbrood scales. J. Invertebr Pathol. 70, 79–87 (1997).

    Google Scholar 

  4. Hrabak, J. & Martinek, K. Screening of secreted proteases of Paenibacillus larvae by using substrate-SDS-polyacrylamide gel electrophoresis. J. Apic. Res. 46, 160–164 (2007).

    Google Scholar 

  5. Antúnez, K., Anido, M., Arredondo, D., Evans, J. D. & Zunino, P. Paenibacillus larvae enolase as a virulence factor in honeybee larvae infection. Vet. Microbiol. 147, 83–89 (2011).

    Google Scholar 

  6. Poppinga, L. et al. Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American foulbrood of honey bees. PLoS Pathog. 8, e1002716 (2012).

    Google Scholar 

  7. Erban, T. et al. Comprehensive proteomic analysis of exoproteins expressed by ERIC I, II, III and IV Paenibacillus larvae genotypes reveals a wide range of virulence factors. Virulence 10, 363–375 (2019).

    Google Scholar 

  8. Bailey, L. & Ball, B. V. Honey Bee Pathology (Academic Press Limited, 1991).

  9. Gregorc, A. & Bowen, I. D. Histopathological and histochemical changes in honeybee larvae (Apis mellifera L.) after infection with Bacillus larvae, the causative agent of American foulbrood disease. Cell. Biol. 22, 137–144 (1998).

    Google Scholar 

  10. Lindström, A., Korpela, S. & Fries, I. The distribution of Paenibacillus larvae spores in adult bees and honey and larval mortality, following the addition of American foulbrood diseased brood or spore-contaminated honey in honey bee (Apis mellifera) colonies. J. Invertebr Pathol. 99, 82–86 (2008).

    Google Scholar 

  11. Alonso-Salces, R. M. et al. Natural strategies for the control of Paenibacillus larvae, the causative agent of American foulbrood in honey bees: a review. Apidologie 48, 387–400 (2017).

    Google Scholar 

  12. Hasemann, L. How long can spores of American foulbrood live? Am. Bee J. 101, 298–299 (1961).

    Google Scholar 

  13. Miyagi, T. et al. Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. J. Invertebr Pathol. 75, 95–96 (2000).

    Google Scholar 

  14. Mussen, E. C. Antibiotic-resistant American foulbrood. Am. Bee J. 140, 300–301 (2000).

    Google Scholar 

  15. Evans, J. D. Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J. Invertebr Pathol. 83, 46–50 (2003).

    Google Scholar 

  16. Alippi, A. M. & Reynaldi, F. J. Inhibition of the growth of Paenibacillus larvae, the causal agent of American foulbrood of honeybees, by selected strains of aerobic spore-forming bacteria isolated from apiarian sources. J. Invertebr Pathol. 91, 141–146 (2006).

    Google Scholar 

  17. Evans, J. D. & Armstrong, T. N. Inhibition of the American foulbrood bacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. J. Apic. Res. 44, 168–171 (2005).

    Google Scholar 

  18. Forsgren, E., Olofsson, T. C., Váasquez, A. & Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108 (2010).

    Google Scholar 

  19. Fuselli, S. R., de la García, S. B., Eguaras, M. J. & Fritz, R. Susceptibility of the honeybee bacterial pathogen Paenibacillus larvae to essential oils distilled from exotic and indigenous Argentinean plants. J. Essent. Oil Res. 20, 464–470 (2011).

    Google Scholar 

  20. Gende, L. B., Floris, I., Fritz, R. & Eguaras, M. J. Antimicrobial activity of cinnamon (Cinnamomum zeylanicum) essential oil and its main components against Paenibacillus larvae from Argentine. Bull. insectology. 61, 1–4 (2008).

    Google Scholar 

  21. Flesar, J. et al. In vitro growth-inhibitory effect of plant-derived extracts and compounds against Paenibacillus larvae and their acute oral toxicity to adult honey bees. Vet. Microbiol. 145, 129–133 (2010).

    Google Scholar 

  22. Damiani, N. et al. Laurel leaf extracts for honeybee pest and disease management: antimicrobial, microsporicidal, and acaricidal activity. Parasitol. Res. 113, 701–709 (2014).

    Google Scholar 

  23. 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. J. Appl. Microbiol. 123, 1160–1167 (2017).

    Google Scholar 

  24. Antúnez, K. et al. Efficacy of natural propolis extract in the control of American foulbrood. Vet. Microbiol. 131, 324–331 (2008).

    Google Scholar 

  25. Spivak, M. & Reuter, G. S. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32, 555–565 (2001).

    Google Scholar 

  26. Fridman, G. et al. Applied plasma medicine. Plasma Process. Polym. 5, 503–533 (2008).

    Google Scholar 

  27. Tendero, C., Tixier, C., Tristant, P., Desmaison, J. & Leprince, P. Atmospheric pressure plasmas: A review. Spectrochim Acta B Spectrosc. 61, 2–30 (2006).

    Google Scholar 

  28. Thirumdas, R., Sarangapani, C. & Annapure, U. S. Cold plasma: A novel non-thermal technology for food processing. Food Biophys. 10, 1–11 (2015).

    Google Scholar 

  29. Pankaj, S. K. & Keener, K. M. Cold plasma: background, apllications and current trends. Curr. Opin. Food Sci. 16, 49–52 (2017).

    Google Scholar 

  30. Moisan, M. et al. Plasma sterilization. Methods and mechanisms. Pure Appl. Chem. 74, 349–358 (2002).

    Google Scholar 

  31. Cullen, P. J. & Milosavljević, V. Spectroscopic charcaterization of a radio-frequency argon plasma jet discharge in ambient air. Prog. Theor. Exp. Phys. 2015, 063J01 (2015).

  32. 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).

    Google Scholar 

  33. Casciola, M. & Tarek, M. A. A molecular insight into the electro-transfer of small molecules through electropores driven by electric fields. Biochim. Biophys. Acta (Bba)-Biomembranes. 1858, 22782–22289 (2016).

    Google Scholar 

  34. Kotnik, T., Rems, L., Tarek, M. & Miklavcic, D. Membrane electroporation and electropermeabilization: mechanisms and models. Annu. Rev. Biophys. 48, 63–91 (2019).

    Google Scholar 

  35. Mentheour, R. & Machala, Z. Coupled antibacterial effects of plasma-activated water and pulsed electric field. Front. Phys. 10, 895813 (2022).

    Google Scholar 

  36. Hu, X. et al. Potential use of atmospheric cold plasma for postharvest preservation of blueberries. Postharvest Biol. Technol. 179, 111564 (2021).

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

    Google Scholar 

  38. Boonmee, T. et al. Antifungal activity of non-thermal atmospheric pressure plasma against postharvest mango anthracnose, Colletotrichum siamense. Postharvest Biol. Technol. 232, 113994 (2026).

    Google Scholar 

  39. Wang, Y. et al. Effective inhibition of fungal growth, deoxynivalenol biosynthesis and pathogenicity in cereal pathogen Fusarium spp. by cold atmospheric plasma. Chem. Eng. J. 437, 135307 (2022).

    Google Scholar 

  40. Liu, Y. et al. Inactivation mechanisms of atmospheric pressure plasma jet on Bacillus cereus spores and its application on low-water activity foods. Food Res. Int. 169, 112867 (2023).

    Google Scholar 

  41. Boonmee, T. et al. Atmospheric non-thermal plasma inactivation of Ascosphaera apis, the causative agent of chalkbrood disease in honeybee. Sci. Rep. 14, 1831 (2024).

    Google Scholar 

  42. Boonmee, T. et al. The in vitro potential of non-thermal atmospheric pressure plasma against Nosema ceranae infection in honeybees (Apis mellifera). Sci. Rep. 15, 26975 (2025).

    Google Scholar 

  43. Nicol, M. J. et al. Antibacterial effects of low-temperature plasma generated by atmospheric-pressure plasma jet are mediated by reactive oxygen species. Sci. Rep. 10, 3066 (2020).

    Google Scholar 

  44. Scholtz, V., Jirešová, J., Šerá, B. & Julák, J. A review of microbial decontamination of cereals by non-thermal plasma. Foods 10, 2927 (2021).

    Google Scholar 

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

    Google Scholar 

  46. Bourke, P., Ziuzina, D., Boehm, D., Cullen, P. J. & Keener, K. The potential of cold plasma for safe and sustainable food production. Trends Biotechnol. 36, 615–626 (2018).

    Google Scholar 

  47. Bruggeman, P. J. et al. Plasma-liquid interactions: A review and roadmap. PSST 25, 053002 (2016).

    Google Scholar 

  48. Zhang, Q. et al. A study of oxidative stress induced by non-thermal plasma-activated water for bacterial damage. Appl. Phys. Lett. 102, 203701 (2013).

    Google Scholar 

  49. Maisch, T. Resistance in antimicrobial photodynamic inactivation of bacteria. Photochem. Photobiol Sci. 14, 1518–1526 (2015).

    Google Scholar 

  50. Zhang, H., Zhang, C. & Han, Q. Mechanisms of bacterial inhibition and tolerance around cold atmospheric plasma. Appl. Microbiol. Biotechnol. 107, 5301–5316 (2023).

    Google Scholar 

  51. Hu, J. et al. Antibacterial mechanism of atmospheric cold plasma against Pseudomonas fluorescens and Pseudomonas putida and its preservation application on in-packaged red shrimp paste. Food Chem. 464, 141590 (2025).

    Google Scholar 

  52. Genersch, E., Ashiralieva, A. & Fries, I. Strain- and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, a bacterial pathogen causing American foulbrood disease in honeybees. Appl. Environ. Microbiol. 71, 7551–7555 (2005).

    Google Scholar 

  53. Antúnez, K., Anido, M., Schlapp, G., Evans, J. D. & Zunino, P. Characterization of secreted protease of Paenibacillus larvae, potential virulence factors involved in honeybee larval infection. J. Invertebr Pathol. 102, 129–132 (2009).

    Google Scholar 

  54. Genersch, E. American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr Pathol. 103(Suppl 1), S10–S19 (2010).

    Google Scholar 

  55. Calderón-Franco, D., Lin, Q., van Loosdrecht, M. C. M., Abbas, B. & Weissbrodt, D. G. Anticipating xenogenic pollution at the source: impact of sterilizations on DNA release from microbial cultures. Front. Bioeng. Biotechnol. 8, 171 (2020).

    Google Scholar 

  56. Shi, X. et al. Development and characterization of touchable air plasma jet device for inactivation of oral bacteria. Results Phys. 36, 105405 (2020).

    Google Scholar 

  57. Daisley, B. A. et al. Novel probiotic approach to counter Paenibacillus larvae infection in honey bees. ISME J. 14, 476–491 (2020).

    Google Scholar 

  58. Ory, F. et al. Ecology and pathogenicity for honey bee brood of recently described Paenibacillus melissococcoides and comparison with Paenibacillus dendritiformis, Paenibacillus thiaminolyticus. Environ. Microbiol. Rep. 17, e70089 (2025).

    Google Scholar 

Download references