Oxidative status of honey bees infected with Nosema ceranae microsporidium and supplemented with Agaricus bisporus mushroom extract

Main Article Content

Marko Ristanic
https://orcid.org/0000-0002-6084-7321
Uros Glavinic
https://orcid.org/0000-0003-2143-1611
Danica Dzogovic
https://orcid.org/0000-0002-0977-2803
Stefan Jelisic
Minja Zorc
https://orcid.org/0000-0003-3330-7909
Nevenka Aleksic
Zoran Stanimirovic

Abstract

Nosema ceranae, a microsporidium species, is among the most common causes of bee diseases. The positive effect of Agaricus bisporus mushroom extract on the survival and immunity of Nosema-infected bees has been reported recently. The effect could be achieved by stimulating the expression of immune-related genes, but also by suppressing nosemosis. The aim of this work was to determine the effect of A. bisporus extract on the oxidative status of bees infected with N. ceranae. In a cage experiment on newly hatched bees, the effect of aqueous extract of champignon (A. bisporus, strain A15) was investigated. Six groups were formed: three groups were infected and received A. bisporus extract through food at different times (days 1, 3, and 6 after hatching), one group received the extract but was not infected (treatment control), one was only infected with Nosema (positive control) and one was neither infected nor received the extract (negative control). The effects were examined on samples taken on days 7 and 15 of the study. The activities of the antioxidant enzymes catalase (CAT), superoxide dismutase (SOD) and glutathione S-transferase (GST) and the concentrations of malondialdehyde (MDA) were determined. In comparison to the positive control, the enzyme activities and MDA concentrations were significantly lower in the groups fed with the mushroom extract supplement. In the negative control, the level of oxidative stress was lower than in the positive control. In comparison with the other groups, the values mostly did not differ significantly. The oxidative status of bees infected with N. ceranae was significantly better if they were fed with the A. bisporus extract.

Downloads

Download data is not yet available.

Article Details

How to Cite
Ristanic, M., Glavinic, U., Dzogovic, D., Jelisic, S., Zorc, M., Aleksic, N., & Stanimirovic, Z. (2023). Oxidative status of honey bees infected with Nosema ceranae microsporidium and supplemented with Agaricus bisporus mushroom extract. Veterinarski Glasnik, 77(1), 35–50. https://doi.org/10.2298/VETGL220715013G
Section
Full research article

References

Balieira K.V.B., Mazoo M., Bizerra P.F.V., Guimaraes A.R.J.S., Nicodemo D., Mingatto F.E. 2018. Imidacloprid-induced oxidative stress in honey bees and the antioxidant action of caffeine. Apidologie, 49:562-572. https://doi.org/10.1007/s13592-018-0583-1

Cantwell G.E. 1970. Standard methods for counting Nosema spores. American Bee Journal 110:222-223.

Chakrabarti P., Carlson E.A., Lucas H.M., Melathopoulos A.P., Sagili R.R. 2020. Field rates of Sivanto™ (flupyradifurone) and Transform® (sulfoxaflor) increase oxidative stress and induce apoptosis in honey bees (Apis mellifera L.). PLoS ONE, 15: e0233033. https://doi.org/10.1371/journal.pone.0233033

Djekic I., Vunduk J., Tomašević I., Kozarski M., Petrovic P., Niksic M., Pudja P., Klaus A. 2017. Total quality index of Agaricus bisporus mushrooms packed in modified atmosphere. Journal of the Science of Food and Agriculture, 97, pp.3013-3021. https://doi.org/10.1002/jsfa.8142

Dubovskiy I.M., Martemyanov V.V., Vorontsova Y.L., Rantala M.J., Gryzanova E.V., Glupov V.V. 2008. Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). Comparative biochemistry and physiology: Part C, 148:1–5. https://doi.org/10.1016/j.cbpc.2008.02.003

Dussaubat C., Brunet J.L., Higes M., Colbourne J.K., Lopez J., Choi J.H., Martín-Hernández R., Botías C., Cousin M., McDonnell C., Bonnet M., Belzunces L.P., Moritz R.F., Le Conte Y., Alaux C. 2012. Gut pathology and responses to the microsporidium Nosema ceranae in the Honey Bee Apis mellifera. PLoS One, 7:e37017. https://doi.org/10.1371/journal.pone.0037017

Farjan M., Dmitryjuk M., Lipinski Z., Biernat-Lopienska E., Zoltowska K. 2012/15. Supplementation of the honey bee diet with vitamin C: the effect on the antioxidative system of Apis mellifera carnica brood at different stages. Journal of Apicultural Research, 51:263-270. https://doi.org/10.3896/IBRA.1.51.3.07

Fries I. 2010. Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology, 103: 73–79. https://doi.org/10.1016/j.jip.2009.06.017

Fries I., Chauzat M.P., Chen Y.P., Doublet V., Genersch E., Gisder S., Higes M., McMahon D.P., Martín-Hernández R., Natsopoulou M., Paxton R., Tanner G., Webster T.C., Williams G.R. 2013. Standard methods for Nosema research. In Dietemann V; Ellis J.D., Neumann P. The COLOSS BEEBOOK: Volume II: Standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research, 52:1-28. https://doi.org/10.3896/IBRA.1.52.1.14

Gisder S., Hedtke K., Möckel N., Frielitz M.C., Linde A., Genersch E. 2010. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76:3032-3038. https://doi.org/10.1128/AEM.03097-09

Glavinic U., Stevanovic J., Gajic B., Simeunovic P., Đuric S., Vejnovic B., Stanimirovic Z. 2014. Nosema ceranae DNA in honey bee haemolymph and honey bee mite Varroa destructor. Acta Veterinaria-Beograd, 64:349-357. https://doi.org/10.2478/acve-2014-0033

Glavinic U., Stankovic B., Draskovic V., Stevanovic J., Petrovic T., Lakic N., Stanimirovic Z. 2017. Dietary amino acid and vitamin complex protects honey bee from immunosuppression caused by Nosema ceranae. PLoS One, 12: e0187726. https://doi.org/10.1371/journal.pone.0187726

Glavinic U. 2019. Uticaj razlicitih antimikrobnih preparata i aditiva na ekspresiju gena znacajnih za imunitet, oksidativni stres i prezivljavanje pcela Apis mellifera inficiranih mikrosporidijom Nosema ceranae.

Glavinic U., Stevanovic J., Ristanic M., Rajkovic M., Davitkov D., Lakic N., Stanimmirovic Z. 2021a. Potential of fumagillin and Agaricus blazei mushroom extract to reduce Nosema ceranae in honey bees. Insects, 12:282. https://doi.org/10.3390/insects12040282

Glavinic U., Rajkovic M., Vunduk J., Vejnovic B., Stevanovic J., Milenkovic I., Stanimirovic Z. 2021b. Effects of Agaricus bisporus mushroom extract on honey bees infected with Nosema ceranae. Insects, 12:915. https://doi.org/10.3390/insects12100915

Glavinic U., Blagojevic J., Ristanic M., Stevanovic J., Lakic N., Mirilovic M., Stanimirovic Zoran. 2022. Use of thymol in Nosema ceranae control and health improvement of infected honey bees. Insects, 13:574. https://doi.org/10.3390/insects13070574

Higes M., Martín-Hernández R., Garrido-Bailón E., Botías C., Meana A. 2009. First detection of Nosema ceranae (Microsporidia) in African honey bees (Apis mellifera intermissa). Journal of Apicultural Research, 48:217–219. http://dx.doi.org/10.3896/IBRA.1.48.3.12

Higes M., Meana A., Bartolomé C., Botías C., Martín-Hernández R. 2013. Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental Microbiology Reports, 51:17–29. https://doi.org/10.1111/1758-2229.12024

Jovanovic N., Glavinic U., Delic B., Vejnovic B., Aleksic N., Mladjan V., Stanimirovic Z. 2021. Plant-based supplement containing B complex vitamins can improve bee health and increase colony performance. Preventive Veterinary Medicine, 190:105322. https://doi.org/10.1016/j.prevetmed.2021.105322

Klaus A., Kozarski M., Niksic M., Jakovljevic D., Todorovic N., Van Griensven L.J.L.D. 2011. Antioxidative activities and chemical characterization of polysaccharides extracted from the basidiomycete Schizophyllum commune. LWT – Food Science and Technology, 44:1-7. https://doi.org/10.1016/j.lwt.2011.05.010

Klee J., Besana A.M, Genersch E., Gisder S., Nanetti A., Tam D.Q., Chinh T.X., Puerta F., Ruz J.M., Kryger P., Message D., Hatjina F., Korpela S., Fries I., Paxton R.J. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96:1–10

Liu T., Sun L., Zhang Y., Wang Y., Zheng J. 2022. Imbalanced GSH/ROS and sequential cell death. Journal of Biochemical and Molecular Toxicology, 36, p.e22942. https://doi.org/10.1002/jbt.22942

Martin-Hernandez R., Meana A., Prieto L., Salvador A.M., Garrido-Bailón E., Higes M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73:6331-6338. https://doi.org/10.1128/AEM.00270-07

Morimoto T., Kojima Y., Toki T., Komeda Y., Yoshiyama M., Kimura K., Nirasawa K., Kadowaki T. 2011. The habitat disruption induces immune‐suppression and oxidative stress in honey bees. Ecology and Evolution, 1:201-217. https://doi.org/10.1002/ece3.21

Nikolic T., Purac J., Orcic S., Kojic D., Vujanovic D., Stanimirovic Z., Grzetic I., Ilijevic K., Sikoparija B., Blagojević P.D. 2015. Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Archives of Insect Biochemistry and Physiology, 90:181-194. https://doi.org/10.1002/arch.21253

Roussel M., Villay A., Delbac F., Michaud P., Laroche C., Roriz D., El Alaoui H., Diogon M. 2015. Antimicrosporidian activity of sulphated polysaccharides from algae and their potential to control honeybee nosemosis. Carbohydrate polymers 133:213-220. https://doi.org/10.1016/j.carbpol.2015.07.022

Sokolov V.P., Grobov O.F. 1963. Nosema spores in the hemolymph of the bee. Pchelovodstvo, 7:39.

Stanimirovic Z., Glavinic U., Ristanic M., Aleksic N., Jovanovic N., Vejnovic B., Stevanovic J. 2019. Looking for the causes of and solutions to the issue of honey bee colony losses. Acta veterinaria-beograd, 69:1-31. https://doi.org/10.2478/acve-2019-0001

Stanimirovic Z., Glavinic U., Ristanic M., Jelisic S., Vejnovic B., Niketic M., Stevanovic J. 2022. Diet supplementation helps honey bee colonies in combat infections by enhancing their hygienic behaviour. Acta Veterinaria-Beograd, 72:145-166 https://doi.org/10.2478/acve-2022-0013

Steche W. 1960. A atiologie und therapie der nosematose der honigbiene. Zeitung Bienenfarsche 5:49–52.

Stevanovic J., Stanimirovic Z., Genersch E., Kovacevic R.S., Ljubenkovic J., Radakovic M., Aleksic N. 2011. Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie, 41:49–58. https://doi.org/10.1051/apido/2010034

Stevanovic J., Simeunovic P., Gajic B., Lakic N., Radovic D., Fries I., Stanimirovic Z. 2013. Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie, 44:522-536. https://doi.org/10.1007/s13592-013-0203-z

Simone-Finstrom M., Li-Byarlay H., Huang M.H., Strand M.K., Rueppell O., Tarpy, D.R. 2016. Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Scientific reports, 6:1-10. https://doi.org/10.1038/srep32023

Van den Heever J.P., Thompson, T.S., Curtis J.M., Ibrahim A., Pernal S.F. 2014. Fumagillin: An overview of recent scientific advances and their significance for apiculture. Journal of Agricultural and Food Chemistry, 62:2728–2737. https://doi.org/10.1021/jf4055374

Vidau C., Diogon M., Aufauvre J., Fontbonne R., Viguès B., Brunet J.L., Texier C., Biron D.G., Blot N., Alaoui H.E., Belzunces L.P., Delbac F. 2011. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One, 6:e21550. https://doi.org/10.1371/journal.pone.0021550

Vunduk, J., Djekic I., Petrović P., Tomašević I., Kozarski M., Despotović S., Nikšić M., Klaus A. 2018. Challenging the difference between white and brown Agaricus bisporus mushrooms: Science behind consumers’ choice. British Food Journal, 120:1381–1394. https://doi.org/10.1108/BFJ-10-2017-0550

Most read articles by the same author(s)