Differential expression of antioxidant system genes in honey bee (Apis mellifera L.) caste development mitigates ROS-mediated oxidative damage in queen larvae

Santos, Douglas Elias; Souza, Anderson de Oliveira; Tibério, Gustavo Jacomini; Alberici, Luciane C.; Hartfelder, Klaus

doi:10.1590/1678-4685-gmb-2020-0173

Cited by 8 publications

(6 citation statements)

References 57 publications

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“…This is in agreement with two evolutionary pathways proposed for understanding senescence: the free radical and adaptive senescence theories [ 31 , 42 ]. The response of the ADSs of our queens fits the free radical adaptation (compare Santos et al [ 46 ]), whereas the workers fit adaptive senescence [ 31 , 32 ]. Consequently, eusocial evolution must have shaped queen and worker ABSs very differently (H1), but our study revealed that this could be not useful, and even unfavorable, for workers, particularly forgers that dwell in the anthropogenic ecosystems, especially when exposed to pesticides.…”

Section: Discussionmentioning

confidence: 67%

“…Vitellogenin is also a strong antioxidant [ 9 , 43 ] with lower expression in workers, decreasing with age as opposed to queens, in which the expression increases as they progress in age [ 44 , 45 ]. Differences in the expression of ADS genes were also revealed during the individual development of these castes [ 46 ]. Therefore, the ADSs of our queens have to work differently and may involve many more different components than the ADSs of our workers during exposure to ID stress, particularly in the case of the oldest queens.…”

Section: Discussionmentioning

confidence: 99%

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Antioxidation Defenses of Apis mellifera Queens and Workers Respond to Imidacloprid in Different Age-Dependent Ways: Old Queens Are Resistant, Foragers Are Not

Paleolog

Wilde

Miszczak

et al. 2021

Animals

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We investigated how different antioxidant defenses (ADSs) were shaped by evolution in young/old Apis mellifera workers and queens to broaden the limited knowledge on whether ADSs are effective in contemporary pesticide environments and to complete bee oxidative-aging theory. We acquired 1-day-old, 20-day-old, and 2-year-old queens and 1-day-old and 20-day-old workers (foragers) fed 0, 5, or 200 ppb imidacloprid, a pesticide oxidative stressor. The activities of catalase, glutathione peroxidase, glutathione S-transferase, and superoxide dismutase and the level of total antioxidant potential were determined in hemolymph. The ADS was upregulated in workers with age but downregulated in queens. Imidacloprid suppressed the ADS in all workers, particularly in foragers with an upregulated ADS, but it did not affect the ADS in 1-day-old queens. In contrast to foragers, the downregulated ADS of 2-year-old queens was unexpectedly highly upregulated by imidacloprid, which has not been previously shown in such old queens. The principal component analysis confirmed that queen and worker ADSs responded to imidacloprid in opposite ways, and ADS of 2-year-queens was markedly different from those of others. Thus, evolutionary shaped ADSs of older queens and workers may be of the limited use for foragers dwelling in pesticide ecosystems, but not for old queens.

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Section: Discussionmentioning

confidence: 67%

Section: Discussionmentioning

confidence: 99%

Antioxidation Defenses of Apis mellifera Queens and Workers Respond to Imidacloprid in Different Age-Dependent Ways: Old Queens Are Resistant, Foragers Are Not

Paleolog

Wilde

Miszczak

et al. 2021

Animals

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“…It can guide the conversion of oxygen radicals in cells into hydrogen peroxide, with lower oxidative activity, and then be broken down, thus reducing the degree of cellular oxidation [35]. Studies have shown that Cat is significantly expressed at a higher level in queen larvae than in worker larvae, suggesting that the queen is more efficient in removing reactive oxygen species (ROS) and has a stronger antioxidant capacity than workers [36]. In our results, the expression of the Cat gene was down-regulated after AmKr-h1 RNAi, suggesting that AmKr-h1 may influence the antioxidant capacity of honey bees by regulating the Cat gene.…”

Section: Discussionmentioning

confidence: 99%

The Juvenile-Hormone-Responsive Factor AmKr-h1 Regulates Caste Differentiation in Honey Bees

Gong,

Cheng,

et al. 2023

Biomolecules

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Honey bees are typical model organisms for the study of caste differentiation, and the juvenile hormone (JH) is a crucial link in the regulatory network of caste differentiation in honey bees. To investigate the mechanism of JH-mediated caste differentiation, we analyzed the effect of the JH response gene AmKr-h1 on this process. We observed that AmKr-h1 expression levels were significantly higher in queen larvae than in worker larvae at the 48 h, 84 h, and 120 h larval stages, and were regulated by JH. Inhibiting AmKr-h1 expression in honey bee larvae using RNAi could lead to the development of larvae toward workers. We also analyzed the transcriptome changes in honey bee larvae after AmKr-h1 RNAi and identified 191 differentially expressed genes (DEGs) and 682 differentially expressed alternative splicing events (DEASEs); of these, many were related to honey bee caste differentiation. Our results indicate that AmKr-h1 regulates caste differentiation in honey bees by acting as a JH-responsive gene.

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“…In contrast, colonies kept outdoors in southern environments suffered dysbiosis that proliferates in the midgut. Workers born during the winter in southern environments were susceptible to opportunism, while workers funded by fall nutrition were expressing the diutinus phenotype (queen-like physiology) to some degree to nance an environment of individual and social immunity [102,118,119]. At the colony level, the cost/bene t ratio associated with this phenotypic expression may be a major factor in overwintering survival.…”

Section: Conclusion/perspectivementioning

confidence: 99%

“…The indoor CW colonies showed no strong associations with Vg expression overwinter and no immune response, indicative of energy conservation and no microbial challenge. Although queen and queen-like (diutinus) phenotypes often possess higher mean ROS than workers in the form of H 2 O 2 , similar levels of fat body protein carboxylation between castes are maintained because queens or queen-like phenotypes can afford to mount an immune response, expressing antioxidant genes that include MnSOD and CuZnSOD [102]. There may be a similar explanation for the different response to opportunism between 50-70 day old (KA) workers and workers > 30 days-old (WW) sampled in late winter.…”

Section: The Redox Environment / Ros Gene Expressionmentioning

confidence: 99%

Gut and Colony Microbiota of Honey Bees Apis mellifera: Social Immunity, Opportunistic Disease and Survival Overwinter.

Anderson¹,

Maes

2021

Preprint

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BackgroundOverwintering is a major contributor to honey bee colony loss and involves changes in environmental conditions, host physiology and group behavior that influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the extended colony environment on many levels, producing pro-oxidants, antioxidants and antimicrobial peptides. With the coming of winter, colonies produce a long-lived (diutinus) worker phenotype that survives until environmental conditions improve. We used a known-age worker cohort to investigate microbiome integrity and social gene expression of diutinus workers overwinter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor overwintering environments. ResultsWe produce the first evidence that social immune gene expression is associated with the core hindgut and colony microbiota in honey bees, and highlight the midgut as a target of opportunistic disease overwinter. We discovered a distinct physiological and microbiological trajectory for diutinus workers that differs drastically from younger, short-lived workers in the colony. Diutinus bees were associated with decreased fungal load and decreased bacterial diversity, and increased core microbiota and longevity. Colonies overwintered indoors maintained a stable or improved microbiota structure and complimentary gene expression overwinter. In contrast, workers from colonies overwintered outdoors in warm southern conditions possessed changes co-occurring throughout the alimentary tract microbiota that suggest opportunistic disease progression and resistance in diutinus workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and bacterial diversity abundance. ConclusionsOur results highlight social selection pressures that shaped the colony and hindgut microbiome with evolution to a perennial life history. The results are consistent with a “group level” explanation of social immunity, including host associations with the colony microbiota, and a social immune response by long-lived diutinus workers to accompany microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival overwinter. The relationship of colony and gut microbiota with social immune function highlights the range of host-microbial interaction associated with the honey bee superorganism, and its potential influence on colony health, disease resistance and gut integrity.

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Differential expression of antioxidant system genes in honey bee (Apis mellifera L.) caste development mitigates ROS-mediated oxidative damage in queen larvae

Cited by 8 publications

References 57 publications

Antioxidation Defenses of Apis mellifera Queens and Workers Respond to Imidacloprid in Different Age-Dependent Ways: Old Queens Are Resistant, Foragers Are Not

Antioxidation Defenses of Apis mellifera Queens and Workers Respond to Imidacloprid in Different Age-Dependent Ways: Old Queens Are Resistant, Foragers Are Not

The Juvenile-Hormone-Responsive Factor AmKr-h1 Regulates Caste Differentiation in Honey Bees

Gut and Colony Microbiota of Honey Bees Apis mellifera: Social Immunity, Opportunistic Disease and Survival Overwinter.

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