Dataset Information

The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee.

ABSTRACT: Queen bees and worker bees both develop from fertilized eggs, whereas queens live longer than workers. The mechanism of this phenomenon is worth exploring. Antioxidant capacity, immune and IIS are the conserved mechanisms of aging. The importance of gut bacteria for health prompted us to connect with bee aging. Therefore, the differences of antioxidant, immune, IIS and gut microflora between queen and worker bees were compared to find potential mechanisms of queens' longevity. The results showed queens had stronger antioxidant capacity and lower immune pathway and IIS activity than workers. The higher expression level of catalase and SOD1/2 in queens resulted in the stronger ROS scavenging ability, which leads to the lower ROS level and the reduced accumulation of oxidative damage products in queens. The lower IMD expression and higher antimicrobial peptides (AMPs) expressions in queens suggested that queens maintain lower immune pathway activity and stronger immune capacity than workers. Gut bacteria composition analysis indicated that queens had supernal Acetobacteraceae (notably Commensalibacter and Bombella), Lactobacillus and Bifidobacterium over workers. In conclusion, antioxidant, immune, IIS, and gut symbiotic bacteria all contribute to the longevity of queens. This study provides more insights into revealing the mechanisms of queens' longevity.

SUBMITTER: Wang H

PROVIDER: S-EPMC9506344 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee.

Wang Hongfang H Lei Li L Chen Wenfeng W Chi Xuepeng X Han Kai K Wang Ying Y Ma Lanting L Liu Zhenguo Z Xu Baohua B

Insects 20220826 9

Queen bees and worker bees both develop from fertilized eggs, whereas queens live longer than workers. The mechanism of this phenomenon is worth exploring. Antioxidant capacity, immune and IIS are the conserved mechanisms of aging. The importance of gut bacteria for health prompted us to connect with bee aging. Therefore, the differences of antioxidant, immune, IIS and gut microflora between queen and worker bees were compared to find potential mechanisms of queens' longevity. The results showed ...[more]

PMID: 36135473

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Project description:Queen and worker bees are natural models for aging research, as their lifespans vary considerably independent of genetic variation. Investigating the reasons why queens live longer than workers is of great significance for research on the universal processes of aging in animals. The gut microbiome has received attention as a vital regulator of host health, while its precise role in honeybee aging needs further investigation. The effects and mechanisms behind the relationship between gut microbiota and worker lifespan were measured by transplanting queen bee gut bacteria (QG) and worker bee gut bacteria (WG) into microbiota-free (MF) workers. The transplantation of QG to MF bees significantly extended the workers' lifespans compared with MF and WG bees. Untargeted metabolomics identified 49 lifespan-related differential metabolites, and Kyoto Encyclopedia of Genes and Genomes analysis of these revealed three lifespan-related metabolic pathways: insulin/insulin-like growth factor signaling, immune, and ketone body metabolism pathways. Further verification showed that QG inhibited the expression of insulin-like peptides (ILPs), and the expression of ILPs was lower in natural queens than in natural workers. QG transplantation also stimulated the expression of antioxidant genes and lowered oxidative damage products in natural queen bees. However, gut microbiota transplantation failed to mimic the immune properties and ketone body metabolism profiles of natural queens and workers. Concisely, QG could increase the antioxidant capacity to extend lifespan by inhibiting insulin signaling. These findings may help determine the mechanisms behind queen longevity and provide further insights into the role of gut symbionts.ImportanceQueen and worker bees share the same genetic background but have vastly different lifespans. The gut microbiome regulates host health, suggesting that differences in lifespan between queen and worker bees could be related to gut bacteria. Herein, we used an innovative method to transplant gut microbiota from adult queen or worker bees to microbiota-free bees. The transplantation of queen gut microbiota to microbiota-free bees extended their lifespan. Insulin/insulin-like growth factor signaling, a highly conserved metabolic pathway related to lifespan, displayed identical expression profiles in natural queen bees and microbiota-free bees transplanted with queen microbiota. This finding significantly expands our understanding of the relationships between intestinal bacteria, host health, and the biology of aging.

Project description:BackgroundHoneybees provide economically and ecologically vital pollination services to crops and wild plants. During the last decade elevated colony losses have been documented in Europe and North America. Despite growing consensus on the involvement of multiple causal factors, the underlying interactions impacting on honeybee health and colony failure are not fully resolved. Parasites and pathogens are among the main candidates, but sublethal exposure to widespread agricultural pesticides may also affect bees.Methodology/principal findingsTo investigate effects of sublethal dietary neonicotinoid exposure on honeybee colony performance, a fully crossed experimental design was implemented using 24 colonies, including sister-queens from two different strains, and experimental in-hive pollen feeding with or without environmentally relevant concentrations of thiamethoxam and clothianidin. Honeybee colonies chronically exposed to both neonicotinoids over two brood cycles exhibited decreased performance in the short-term resulting in declining numbers of adult bees (-28%) and brood (-13%), as well as a reduction in honey production (-29%) and pollen collections (-19%), but colonies recovered in the medium-term and overwintered successfully. However, significantly decelerated growth of neonicotinoid-exposed colonies during the following spring was associated with queen failure, revealing previously undocumented long-term impacts of neonicotinoids: queen supersedure was observed for 60% of the neonicotinoid-exposed colonies within a one year period, but not for control colonies. Linked to this, neonicotinoid exposure was significantly associated with a reduced propensity to swarm during the next spring. Both short-term and long-term effects of neonicotinoids on colony performance were significantly influenced by the honeybees' genetic background.Conclusions/significanceSublethal neonicotinoid exposure did not provoke increased winter losses. Yet, significant detrimental short and long-term impacts on colony performance and queen fate suggest that neonicotinoids may contribute to colony weakening in a complex manner. Further, we highlight the importance of the genetic basis of neonicotinoid susceptibility in honeybees which can vary substantially.

Dataset Information

The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee.

Publications

The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee.

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