scholarly journals The Queen Gut Refines with Age: Longevity Phenotypes in a Social Insect Model

2018 ◽  
Author(s):  
Kirk E. Anderson ◽  
Vincent A. Ricigliano ◽  
Brendon M. Mott ◽  
Duan C. Copeland ◽  
Amy S. Floyd ◽  
...  

AbstractBackgroundIn social insects, identical genotypes can show extreme lifespan variation providing a unique perspective on age-associated microbial succession. In honey bees, short and long-lived host phenotypes are polarized by a suite of age-associated factors including hormones, nutrition, immune senescence and oxidative stress. Similar to other model organisms, the aging gut microbiota of short-lived (worker) honey bees accrue Proteobacteria and are depleted of Lactobacillus and Bifidobacterium, consistent with a suite of host senescence markers. In contrast, long-lived (queen) honey bees maintain youthful cellular function without expressing oxidative stress genes, suggesting a very different host environment for age-associated microbial succession.ResultsWe sequenced the microbiota of 63 honey bee queens exploring two chronological ages and four alimentary tract niches. To control for individual variation we quantified carbonyl accumulation in queen fat body tissue as a proxy for biological aging. We compared our results to the age-specific microbial succession of worker guts. Accounting for queen source variation, two or more bacterial species per niche differed significantly by queen age. Biological aging in queens was correlated with microbiota composition highlighting the relationship of microbiota with oxidative stress. Queens and workers shared many major gut bacterial species, but differ markedly in community structure and age succession. In stark contrast to aging workers, carbonyl accumulation in queens was significantly associated with increased Lactobacillus and Bifidobacterium and depletion of various Proteobacteria.ConclusionsWe present a model system linking changes in gut microbiota to diet and longevity, two of the most confounding variables in human microbiota research. As described for other model systems, metabolic changes associated with diet and host longevity correspond to the changing microbiota. The pattern of age-associated succession in the queen microbiota is largely the reverse of that demonstrated for workers. The guts of short-lived worker phenotypes are progressively dominated by three major Proteobacteria, but these same species were sparse or significantly depleted in long-lived queen phenotypes. More broadly, our results suggest that lifespan evolution formed the context for host-microbial interactions and age-related succession of honey bee microbiota.

2013 ◽  
Vol 2013 ◽  
pp. 1-12 ◽  
Author(s):  
L. Vanysacker ◽  
C. Denis ◽  
P. Declerck ◽  
A. Piasecka ◽  
I. F. J. Vankelecom

Since many years, membrane biofouling has been described as the Achilles heel of membrane fouling. In the present study, an ecological assay was performed using model systems with increasing complexity: a monospecies assay usingPseudomonas aeruginosaorEscherichia coliseparately, a duospecies assay using both microorganisms, and a multispecies assay using activated sludge with or without spikedP. aeruginosa. The microbial adhesion and biofilm formation were evaluated in terms of bacterial cell densities, species richness, and bacterial community composition on polyvinyldifluoride, polyethylene, and polysulfone membranes. The data show that biofouling formation was strongly influenced by the kind of microorganism, the interactions between the organisms, and the changes in environmental conditions whereas the membrane effect was less important. The findings obtained in this study suggest that more knowledge in species composition and microbial interactions is needed in order to understand the complex biofouling process. This is the first report describing the microbial interactions with a membrane during the biofouling development.


2021 ◽  
Author(s):  
Kilea Ward ◽  
Hongmei Li-Byarlay

Molecular damage caused by oxidative stress may lead to organismal aging and resulted in acute mortality in organisms. Oxidative stress resistance and longevity are closely linked. Honey bees are the most important managed pollinator in agriculture but the long-term survival of honey bees is seriously threatened. Feral honey bee colonies displayed persistence to Varroa mites. However, it is unknown whether feral honey bees are stress-resistant or survive longer than managed bee populations. More work is needed to determine the impact of oxidative stress on honey bee health and survival. We used the paired colony design to determine the lifespan and levels of oxidative stress on worker bees from either a feral or a managed colony. Each pair of colonies shared similar foraging resources. Results exhibit longer survival time and lifespans of foragers in feral colonies than the managed colonies. The levels of oxidative stress from the lipid damage of feral colonies are higher than the managed colonies, indicating a tolerant mechanism not a repair mechanism to survive. Our study provided new insights into colony difference of physiology and oxidative stress resistance between feral honey bees and commercial stocks.


2018 ◽  
Vol 7 (3) ◽  
Author(s):  
Kirsten M. Ellegaard ◽  
Philipp Engel

We sequenced the genomes of 17 strains isolated from the gut of honey bees, including strains representing the genera Lactobacillus, Bifidobacterium, Gilliamella, Snodgrassella, Frischella, and Commensalibacter. These genome sequences represent an important step forward in the development of a comprehensive reference database to aid future analysis of this emerging gut microbiota model.


2021 ◽  
Vol 22 (2) ◽  
pp. 834
Author(s):  
Xiaofei Wang ◽  
Zhaopeng Zhong ◽  
Xiangyin Chen ◽  
Ziyun Hong ◽  
Weimin Lin ◽  
...  

HFD (high-fat diet) induces obesity and metabolic disorders, which is associated with the alteration in gut microbiota profiles. However, the underlying molecular mechanisms of the processes are poorly understood. In this study, we used the simple model organism honey bee to explore how different amounts and types of dietary fats affect the host metabolism and the gut microbiota. Excess dietary fat, especially palm oil, elicited higher weight gain, lower survival rates, hyperglycemic, and fat accumulation in honey bees. However, microbiota-free honey bees reared on high-fat diets did not significantly change their phenotypes. Different fatty acid compositions in palm and soybean oil altered the lipid profiles of the honey bee body. Remarkably, dietary fats regulated lipid metabolism and immune-related gene expression at the transcriptional level. Gene set enrichment analysis showed that biological processes, including transcription factors, insulin secretion, and Toll and Imd signaling pathways, were significantly different in the gut of bees on different dietary fats. Moreover, a high-fat diet increased the relative abundance of Gilliamella, while the level of Bartonella was significantly decreased in palm oil groups. This study establishes a novel honey bee model of studying the crosstalk between dietary fat, gut microbiota, and host metabolism.


2021 ◽  
Vol 9 (4) ◽  
pp. 871
Author(s):  
Christopher Dosch ◽  
Anja Manigk ◽  
Tabea Streicher ◽  
Anja Tehel ◽  
Robert J. Paxton ◽  
...  

Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey bees (Apis mellifera) against their viral pathogens. Here we set out to fill this knowledge gap by investigating how the gut microbiota modulates the virulence of a major honey bee viral pathogen, deformed wing virus (DWV). We found that, upon oral virus exposure, honey bee survival was significantly increased in bees with an experimentally established normal gut microbiota compared to control bees with a perturbed (dysbiotic) gut microbiota. Interestingly, viral titers were similar in bees with normal gut microbiota and dysbiotic bees, pointing to higher viral tolerance in bees with normal gut microbiota. Taken together, our results provide evidence for a positive role of the gut microbiota for honey bee fitness upon viral infection. We hypothesize that environmental stressors altering honey bee gut microbiota composition, e.g., antibiotics in beekeeping or pesticides in modern agriculture, could interact synergistically with pathogens, leading to negative effects on honey bee health and the epidemiology and impact of their viruses.


2020 ◽  
Author(s):  
Yakun Zhang ◽  
Meiling Su ◽  
Lon Wang ◽  
Shaokang Huang ◽  
Songkun Su ◽  
...  

Abstract Background: Vairimorpha (Nosema) ceranae is the most common eukaryotic gut pathogen in honey bees, Apis mellifera. Infection is typically chronic but may result in mortality. Additional factors may be involved in mortality, including the honey bee gut microbiota. Previous studies of V. ceranae and gut microbiota identified positive associations between core bacteria and V. ceranae infection. These possibly synergistic or mutualistic associations are often disregarded because some core bacteria act as probiotic symbionts. Methods: To clarify the effects caused by the positive associations, we added isomaltooligosaccharide (IMO), a prebiotic also found in honey, to alter the interactions between V. ceranae and gut bacteria. Mortality and sugar consumption of the caged bees were monitored. Infection intensities and gut bacteria were examed after 12 days post inoculation, the plateau phase of infection. The gut bacteria were evaluated using both qPCR and 16S rDNA sequencing.Results: We confirmed that V. ceranae infections alone significantly enhance several core bacterial populations, including Bifidobacterium spp., Snodgrassella alvi, and Gilliamella apicola in the honey bee hindgut microbiota. Moreover, the qPCR results suggested that V. ceranae infected bees had significantly higher bacterial microbiota populations. In addition to the enhanced core bacteria, Commensalibacter and Bartonella were significantly increased in the fecal microbiome. Infected bees fed IMO had significantly higher V. ceranae spore counts but lower mortality; however, infected bees fed IMO did not have significant changes in gut bacteria populations compared to those fed only sucrose, but feeding IMO further reduced the fecal microbiome alpha-diversity. Conclusions: The microbiota alterations caused by infection were similar to the microbiota differences found between summer bees and winter bees, the latter of which have longer lifespans, and feeding IMO increased this similarity. Our results indicated that the interactions between gut bacteria and V. ceranae not only enhanced both the pathogen and bacteria populations but also sustained the host survival. This mutualistic interaction potentially enhances disease transmission and avoids social immune responses of the honey bee hosts.


2021 ◽  
Author(s):  
Kirk E. Anderson ◽  
Patrick Maes

Abstract 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.


2013 ◽  
Vol 4 (1) ◽  
pp. 31-37 ◽  
Author(s):  
M. Rothe ◽  
M. Blaut

Diet is a major force that shapes the composition and activity of the gut microbiota. This is evident from alterations in gut microbiota composition after weaning or drastic dietary changes. Owing to the complexity of the microbiota, interactions of intestinal bacteria with the host are difficult to study. Gnotobiotic animal models offer the opportunity to reduce the complexity and the interindividual variability of the intestinal microbiota. Germ-free animals were associated with a simplified microbial community consisting of eight bacterial species, that are found in the human gut. These microbes were selected because their genome sequences are available, and they mimic to some extent the metabolic activity of the human gut microbiota. The microbiota responded to dietary modifications by changes in the relative proportions of the community members. This model offers the chance to better define the role of intestinal bacteria in obesity development, but little is known on how diet affects intestinal bacteria at the cellular level. Mice monoassociated with Escherichia coli were used as a simplified model to investigate the influence of dietary factors on bacterial protein expression in the intestine. The mice were fed three different diets: a carbohydrate (lactose)-rich diet, a protein-rich diet and a diet rich in starch. The lactose-rich diet led to an induction of proteins involved in E. coli's oxidative stress response (Fur, AhpF, Dps). The corresponding genes are under control of the OxyR transcriptional regulator which is activated by oxidative stress. Further experiments demonstrated that osmotic stress exerted by various carbohydrates leads to an upregulation of proteins belonging to the oxyR regulon. The data suggest that the upregulated proteins enable intestinal E. coli to better cope with diet-induced osmotic stress. These examples demonstrate that gnotobiotic animal models are a valuable tool for studying diet-induced changes at the community and the cell level.


2020 ◽  
pp. 1-14
Author(s):  
M.L. Saccà ◽  
M. Lodesani

The honey bee parasitic mite Varroa destructor is one of the main causes of depopulation of bee colonies. Bacterial symbionts associated to honey bees are known to produce a variety of bioactive molecules that have been suggested to play a protective role against honey bee pathogens. We hypothesised that among these bacteria, those colonising the external body of honey bees, and therefore able to survive and reproduce in the hive environment outside the insect gut, may be good candidate biocontrol agents to be tested against V. destructor. The aim of this study was to isolate bacterial species from healthy honey bees and dead varroa mites and to evaluate the potential miticidal effect of their spent medium containing both bacterial metabolites and viable cells, with the final objective of finding a long-lasting solution for mite control. 61 bacterial strains belonging to the Firmicutes, Proteobacteria and Actinobacteria phyla were isolated from the surface of foragers, nurse bees and larvae collected in 10 different apiaries. The most common species was Lactobacillus kunkeei (62%). Growth capability of a selection of isolates was observed at 30 and 34 °C with 1% and 20% glucose and fructose. Laboratory bioassays were conducted by spraying mites with six-day-grown bacterial cultures containing 107 cfu/ml of four strains of L. kunkeei, Bacillus thuringiensis, Bifidobacterium asteroides and an Acetobacteraceae bacterium. The effect of each strain on varroa survival was tested independently. The first three caused 95-100% mortality of mites in 3 days, indicating a potential role as natural antagonists towards varroa. The mediation of pH of the bacterial cultures did not appear to be determinant in mite inhibition, suggesting the involvement of other modes of action against varroa. The exploitation of honey bee microbiota for controlling one of the major threats for honey bee health may be a promising approach deserving further investigation.


2020 ◽  
Vol 117 (13) ◽  
pp. 7355-7362 ◽  
Author(s):  
Germán Bonilla-Rosso ◽  
Théodora Steiner ◽  
Fabienne Wichmann ◽  
Evan Bexkens ◽  
Philipp Engel

The honey bee gut microbiota influences bee health and has become an important model to study the ecology and evolution of microbiota–host interactions. Yet, little is known about the phage community associated with the bee gut, despite its potential to modulate bacterial diversity or to govern important symbiotic functions. Here we analyzed two metagenomes derived from virus-like particles, analyzed the prevalence of the identified phages across 73 bacterial metagenomes from individual bees, and tested the host range of isolated phages. Our results show that the honey bee gut virome is composed of at least 118 distinct clusters corresponding to both temperate and lytic phages and representing novel genera with a large repertoire of unknown gene functions. We find that the phage community is prevalent in honey bees across space and time and targets the core members of the bee gut microbiota. The large number and high genetic diversity of the viral clusters seems to mirror the high extent of strain-level diversity in the bee gut microbiota. We isolated eight lytic phages that target the core microbiota member Bifidobacterium asteroides, but that exhibited different host ranges at the strain level, resulting in a nested interaction network of coexisting phages and bacterial strains. Collectively, our results show that the honey bee gut virome consists of a complex and diverse phage community that likely plays an important role in regulating strain-level diversity in the bee gut and that holds promise as an experimental model to study bacteria–phage dynamics in natural microbial communities.


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