-bees: A dynamic symbiotic association.

Andrea Becchimanzi, Rosario Nicoletti
Author Information
  1. Andrea Becchimanzi: Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy.
  2. Rosario Nicoletti: Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy.

Abstract

Besides representing one of the most relevant threats of fungal origin to human and animal health, the genus includes opportunistic pathogens which may infect bees (Hymenoptera, Apoidea) in all developmental stages. At least 30 different species of have been isolated from managed and wild bees. Some efficient behavioral responses (e.g., diseased brood removal) exerted by bees negatively affect the chance to diagnose the pathology, and may contribute to the underestimation of aspergillosis importance in beekeeping. On the other hand, bee immune responses may be affected by biotic and abiotic stresses and suffer from the loose co-evolutionary relationships with pathogenic strains. However, if not pathogenic, these hive mycobiota components can prove to be beneficial to bees, by affecting the interaction with other pathogens and parasites and by detoxifying xenobiotics. The pathogenic aptitude of spp. likely derives from the combined action of toxins and hydrolytic enzymes, whose effects on bees have been largely overlooked until recently. Variation in the production of these virulence factors has been observed among strains, even belonging to the same species. Toxigenic and non-toxigenic strains/species may co-exist in a homeostatic equilibrium which is susceptible to be perturbed by several external factors, leading to mutualistic/antagonistic switch in the relationships between and bees.

Keywords

References

  1. J Clin Microbiol. 2004 Sep;42(9):4335-7 [PMID: 15365039]
  2. Mycopathologia. 2006 Sep;162(3):167-77 [PMID: 16944284]
  3. J Agric Food Chem. 2010 Jan 13;58(1):194-201 [PMID: 19916546]
  4. Appl Environ Microbiol. 2000 Jan;66(1):320-4 [PMID: 10618242]
  5. Microorganisms. 2020 Feb 15;8(2): [PMID: 32075309]
  6. Int J Food Microbiol. 2005 Oct 15;104(2):207-14 [PMID: 15967531]
  7. Microbes Environ. 2015;30(3):273-5 [PMID: 26063353]
  8. Front Microbiol. 2020 Jan 09;10:2908 [PMID: 31998250]
  9. Toxins (Basel). 2019 Dec 20;12(1): [PMID: 31861936]
  10. Res Vet Sci. 2021 Mar;135:85-95 [PMID: 33454582]
  11. Pak J Biol Sci. 2018 Jan;21(5):232-238 [PMID: 30311486]
  12. Nature. 2015 May 21;521(7552):S62-3 [PMID: 25992676]
  13. Vet Sci. 2022 May 02;9(5): [PMID: 35622749]
  14. Vet Microbiol. 2011 Apr 21;149(1-2):200-5 [PMID: 21050682]
  15. Lancet. 2007 Aug 25;370(9588):639 [PMID: 17720000]
  16. J Fungi (Basel). 2021 Jun 25;7(7): [PMID: 34202244]
  17. Microb Ecol. 2020 Nov;80(4):897-907 [PMID: 32572535]
  18. Microb Ecol. 2023 Jan;85(1):330-334 [PMID: 34997310]
  19. Curr Biol. 2007 Aug 21;17(16):R693-702 [PMID: 17714663]
  20. Antonie Van Leeuwenhoek. 1987;53(3):147-58 [PMID: 3116923]
  21. Vet Sci. 2022 Mar 21;9(3): [PMID: 35324875]
  22. Evolution. 2009 Nov;63(11):3016-22 [PMID: 19619221]
  23. R Soc Open Sci. 2021 Jan 13;8(1):201805 [PMID: 33614099]
  24. J Food Sci. 2013 Sep;78(9):M1421-9 [PMID: 23915150]
  25. Annu Rev Entomol. 2009;54:405-23 [PMID: 18793100]
  26. Science. 2015 Mar 27;347(6229):1255957 [PMID: 25721506]
  27. Biol Lett. 2010 Aug 23;6(4):562-5 [PMID: 20089536]
  28. Molecules. 2021 Aug 22;26(16): [PMID: 34443668]
  29. Annu Rev Entomol. 2018 Jan 7;63:105-123 [PMID: 28945976]
  30. Peptides. 2015 Jun;68:190-6 [PMID: 25784287]
  31. J Invertebr Pathol. 1974 Sep;24(2):213-7 [PMID: 4413522]
  32. Vet Clin North Am Food Anim Pract. 2021 Nov;37(3):521-533 [PMID: 34689918]
  33. J Invertebr Pathol. 2008 Mar;97(3):273-81 [PMID: 18054037]
  34. Insect Mol Biol. 2006 Oct;15(5):645-56 [PMID: 17069638]
  35. Braz J Microbiol. 2015 Oct-Dec;46(4):1171-6 [PMID: 26691478]
  36. Curr Opin Immunol. 1995 Feb;7(1):4-10 [PMID: 7772280]
  37. Curr Opin Insect Sci. 2018 Apr;26:105-113 [PMID: 29764649]
  38. Zentralbl Mikrobiol. 1984;139(4):249-55 [PMID: 6475343]
  39. Mycopathologia. 2004 Jul;158(1):73-9 [PMID: 15487324]
  40. Trends Microbiol. 2020 Dec;28(12):1010-1021 [PMID: 32680791]
  41. Molecules. 2019 May 02;24(9): [PMID: 31052538]
  42. Probiotics Antimicrob Proteins. 2018 Dec;10(4):638-646 [PMID: 29297160]
  43. Insects. 2021 Mar 25;12(4): [PMID: 33806001]
  44. J Invertebr Pathol. 2010 Jan;103 Suppl 1:S20-9 [PMID: 19909969]
  45. Microb Ecol. 1993 Sep;26(2):125-43 [PMID: 24190009]
  46. Science. 2021 Mar 5;371(6533): [PMID: 33674468]
  47. Proc Biol Sci. 2004 Feb 7;271 Suppl 3:S104-6 [PMID: 15101433]
  48. Viruses. 2018 Mar 30;10(4): [PMID: 29601473]
  49. Curr Opin Insect Sci. 2015 Aug;10:51-58 [PMID: 29588014]
  50. J Invertebr Pathol. 2012 Sep 15;111(1):68-73 [PMID: 22750047]
  51. Science. 2018 Jan 26;359(6374):392-393 [PMID: 29371456]
  52. Int J Food Microbiol. 2005 Nov 15;105(1):1-9 [PMID: 16009441]
  53. Curr Opin Insect Sci. 2015 Aug 1;10:71-82 [PMID: 26273564]
  54. Syst Appl Microbiol. 2004 Mar;27(2):261-7 [PMID: 15046315]
  55. Ecol Evol. 2013 Jul;3(7):2214-22 [PMID: 23919163]
  56. EFSA J. 2022 Mar 31;20(3):e07202 [PMID: 35386571]
  57. Mycoses. 2008 Nov;51(6):520-2 [PMID: 18331445]
  58. Fungal Genet Biol. 2015 Aug;81:88-97 [PMID: 26051490]
  59. J Insect Sci. 2006;6:1-12 [PMID: 19537988]
  60. Proc Biol Sci. 2007 Feb 7;274(1608):303-13 [PMID: 17164193]
  61. Sci Total Environ. 2020 Feb 20;704:135931 [PMID: 31830656]
  62. Phytother Res. 2015 Jan;29(1):48-58 [PMID: 25230727]
  63. Stud Mycol. 2019 Jun;93:1-63 [PMID: 30108412]
  64. Microbiology (Reading). 2011 May;157(Pt 5):1481-1488 [PMID: 21349977]
  65. Food Chem Toxicol. 2012 May;50(5):1790-5 [PMID: 22425940]
  66. J Fungi (Basel). 2021 May 12;7(5): [PMID: 34066127]
  67. Folia Microbiol (Praha). 1998;43(2):156-60 [PMID: 9721607]
  68. Food Chem Toxicol. 2011 Sep;49(9):1970-8 [PMID: 21600954]
  69. Curr Opin Insect Sci. 2015 Aug;10:1-7 [PMID: 29587997]
  70. Comput Struct Biotechnol J. 2018 May 31;16:197-210 [PMID: 30002790]
  71. Infection. 1992 Jul-Aug;20(4):227-9 [PMID: 1521889]
  72. Science. 2013 Mar 29;339(6127):1608-11 [PMID: 23449997]
  73. Pharmazie. 1982 Dec;37(12):864-5 [PMID: 6819589]
  74. PLoS Pathog. 2020 Jun 18;16(6):e1008580 [PMID: 32555676]
  75. Biotechnol Adv. 2018 Jul - Aug;36(4):1167-1184 [PMID: 29608951]
  76. Vet Microbiol. 2014 Mar 14;169(3-4):203-10 [PMID: 24485932]
  77. Front Microbiol. 2014 Feb 10;5:50 [PMID: 24575088]
  78. Microorganisms. 2020 May 29;8(6): [PMID: 32486107]
  79. Appl Environ Microbiol. 1985 Sep;50(3):602-4 [PMID: 16346880]
  80. NPJ Biofilms Microbiomes. 2021 May 7;7(1):42 [PMID: 33963194]
  81. Stud Mycol. 2020 Jun 27;95:5-169 [PMID: 32855739]
  82. Microorganisms. 2021 Feb 25;9(3): [PMID: 33668904]
  83. Molecules. 2018 Dec 19;23(12): [PMID: 30572614]
  84. Food Chem Toxicol. 2012 Jun;50(6):1955-61 [PMID: 22497901]
  85. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2012;47(11):1665-71 [PMID: 22702827]
  86. Acta Microbiol Immunol Hung. 2009 Sep;56(3):285-95 [PMID: 19789142]
  87. PLoS One. 2018 Dec 31;13(12):e0209589 [PMID: 30596703]
  88. PLoS One. 2021 Mar 18;16(3):e0248772 [PMID: 33735295]
  89. Genetics. 2020 Oct;216(2):481-497 [PMID: 32817009]
  90. J Environ Health Sci Eng. 2020 Mar 26;18(1):297-302 [PMID: 32399241]
  91. Annu Rev Entomol. 2014;59:467-85 [PMID: 24160418]
  92. J Apic Res. 2013 Jan;52(1): [PMID: 24198438]
  93. Clin Microbiol Rev. 2009 Jul;22(3):447-65 [PMID: 19597008]
  94. Proc Biol Sci. 2019 Jan 16;286(1894):20182499 [PMID: 30963859]
  95. J Chem Ecol. 2018 Dec;44(12):1170-1177 [PMID: 30370473]
  96. mBio. 2021 Jun 29;12(3):e0050321 [PMID: 34101488]
  97. Z Lebensm Unters Forsch. 1978 Jun 28;166(5):280-3 [PMID: 685476]
  98. Science. 1969 Aug 8;165(3893):607 [PMID: 17770861]
  99. Compr Rev Food Sci Food Saf. 2020 Nov;19(6):2797-2842 [PMID: 33337039]
  100. Environ Sci Pollut Res Int. 2021 Sep;28(34):47251-47261 [PMID: 33893577]
  101. PLoS One. 2015 Jun 23;10(6):e0130560 [PMID: 26102072]
  102. Nature. 1953 Jan 31;171(4344):212-3 [PMID: 13036831]
  103. Sci Rep. 2020 Jun 9;10(1):9279 [PMID: 32518251]
  104. J Invertebr Pathol. 2021 Sep;184:107628 [PMID: 34090931]
  105. Asian Pac J Trop Biomed. 2014 Aug;4(8):633-41 [PMID: 25183333]
  106. J Toxicol Environ Health A. 2013;76(10):587-600 [PMID: 23859127]
  107. PLoS One. 2012;7(2):e31051 [PMID: 22319603]
  108. Med Mycol. 2015 Nov;53(8):765-97 [PMID: 26316211]
  109. Front Microbiol. 2022 Apr 12;13:843842 [PMID: 35495671]
  110. Phytother Res. 2014 Mar;28(3):437-43 [PMID: 23722631]

Word Cloud

Created with Highcharts 10.0.0beesmaypathogenicfungalpathogensspeciesresponsesbeerelationshipsstrainsmycobiotafactorsBesidesrepresentingonerelevantthreatsoriginhumananimalhealthgenusincludesopportunisticinfectHymenopteraApoideadevelopmentalstagesleast30differentisolatedmanagedwildefficientbehavioralegdiseasedbroodremovalexertednegativelyaffectchancediagnosepathologycontributeunderestimationaspergillosisimportancebeekeepinghandimmuneaffectedbioticabioticstressessufferlooseco-evolutionaryHoweverhivecomponentscanprovebeneficialaffectinginteractionparasitesdetoxifyingxenobioticsaptitudespplikelyderivescombinedactiontoxinshydrolyticenzymeswhoseeffectslargelyoverlookedrecentlyVariationproductionvirulenceobservedamongevenbelongingToxigenicnon-toxigenicstrains/speciesco-existhomeostaticequilibriumsusceptibleperturbedseveralexternalleadingmutualistic/antagonisticswitch-bees:dynamicsymbioticassociationAspergillaceaeimmunityentomopathogensmycotoxinspollinatorssaprophyticfungi

Similar Articles

Cited By