Changes in Antioxidant Enzymes Activity and Metabolomic Profiles in the Guts of Honey Bee (Apis mellifera) Larvae Infected with Ascosphaera apis

Abstract

<jats:p>The fungus Ascosphaera apis, an obligate fungal pathogen of honey bee brood, causes chalkbrood disease in honey bee larvae worldwide. Biological characteristics of the fungal pathogen and the molecular interactions between A. apis and honey bees have been studied extensively. However, little is known about the effects of A. apis infection on antioxidant enzyme activities and metabolic profiles of the gut of honey bee larvae. In this study, sandwich enzyme-linked immunosorbent assay and LC-MS based untargeted metabolomic analysis were employed to determine the changes in the specific activities of antioxidant enzymes and the metabolomic profiles in gut tissues of A. apis-infected larvae (105 A. apis spores per larva) and controls. Results showed that specific activities of superoxide dismutase, catalase and glutathione S-transferase were significantly higher in the guts of the control larvae than in the guts of the A. apis-infected larvae. The metabolomic data revealed that levels of 28 and 52 metabolites were significantly higher and lower, respectively, in the guts of A. apis-infected larvae than in the guts of control larvae. The 5-oxo-ETE level in the infected larvae was two times higher than that in the control larvae. Elevated 5-oxo-ETE levels may act as a potential metabolic biomarker for chalkbrood disease diagnosis, suggesting that A. apis infection induced obvious oxidative stress in the honey bee larvae. The levels of metabolites such as taurine, docosahexaenoic acid, and L-carnitine involved in combating oxidative stress were significantly decreased in the gut of A. apis-infected larvae. Overall, our results suggest that A. apis infection may compromise the ability of infected larvae to cope with oxidative stress, providing new insight into changing patterns of physiological responses to A. apis infection in honey bee larvae by concurrent use of conventional biochemical assays and untargeted metabolomics.</jats:p>

Probiotic Properties and Potentiality of Lactiplantibacillus plantarum Strains for the Biological Control of Chalkbrood Disease

“…Even during the excessive proliferation of pathogens, the intestinal epithelium produces and releases high levels of ROS, causing significant oxidative stress [ 111 , 112 , 113 ]. Li et al [ 4 ] recently reported that A. apis infection induced oxidative stress in honeybee larvae, and decreased levels of the metabolites involved in combating oxidative stress could compromise the antioxidant defenses of the infected larvae. The specific activities of antioxidant enzymes (CAT, GST and SOD) and the levels of metabolites (taurine, docosahexaenoic acid and l -carnitine) involved in combating oxidative stress were significantly decreased in the guts of infected honeybee larvae.…”

“…This disease is economically important since it results in significant losses of both honeybees (under certain circumstances, it can kill colonies) and colony productivity [ 2 ], and indications suggest that its incidence may be increasing [ 3 ]. Recent research demonstrated that A. apis infection, together with other biotic and abiotic factors, induces oxidative stress and impairs the antioxidant defensive capacity of honeybee larvae [ 4 ].…”

Cold stress induces specific antioxidant responses in honey bee brood

“…The movement of managed honey bee colonies across different agricultural landscapes and the location of colonies inside greenhouses impact on the levels of oxidative stress (Morimoto et al 2011;Simone-Finstrom et al 2016). Moreover, flight activity, invasive predator species, and pathogens in hives as well as pesticides used for pest control in numerous crops disturb the honey bee oxidative homeostasis (Balieira et al 2018;Gregorc et al 2018;Margotta et al 2018;Leza et al 2019;Li et al 2020). Oxidative stress has been suggested to lead to damage in insects exposed to low temperatures (Lalouette et al 2011;Kojić et al 2019;Tawfik et al 2020).…”

Functional Properties and Antimicrobial Activity from Lactic Acid Bacteria as Resources to Improve the Health and Welfare of Honey Bees

“…Recent research demonstrated that several biotic and abiotic factors, induce oxidative stress and impair the antioxidant defensive capacity of honey bee larvae [ 9 , 157 , 158 , 159 , 160 ].…”