RESUMO
Honey bees are a model for host-microbial interactions with experimental designs evolving towards conventionalized worker bees. Research on gut microbiome transmission and assembly has examined only a fraction of factors associated with the colony and hive environment. Here, we studied the effects of diet and social isolation on tissue-specific bacterial and fungal colonization of the midgut and two key hindgut regions. We found that both treatment factors significantly influenced early hindgut colonization explaining similar proportions of microbiome variation. In agreement with previous work, social interaction with older workers was unnecessary for core hindgut bacterial transmission. Exposure to natural eclosion and fresh stored pollen resulted in gut bacterial communities that were taxonomically and structurally equivalent to those produced in the natural colony setting. Stressed diets of no pollen or autoclaved pollen in social isolation resulted in decreased fungal abundance and bacterial diversity, and atypical microbiome structure and tissue-specific variation of functionally important core bacteria. Without exposure to the active hive environment, the abundance and strain diversity of keystone ileum species Gilliamella apicola was markedly reduced. These changes were associated with significantly larger ileum microbiotas suggesting that extended exposure to the active hive environment plays an antibiotic role in hindgut microbiome establishment. We conclude that core hindgut microbiome transmission is facultative horizontal with 5 of 6 core hindgut species readily acquired from the built hive structure and natural diet. Our findings contribute novel insights into factors influencing assembly and maintenance of honey bee gut microbiota and facilitate future experimental designs.
Assuntos
Microbioma Gastrointestinal , Microbiota , Abelhas , Animais , Interação Social , Bactérias/genética , DietaRESUMO
Honey bees are important pollinators of many major crops and add billions of dollars annually to the US economy through their services. Recent declines in the health of the honey bee have startled researchers and lay people alike as honey bees are agriculture's most important pollinator. One factor that may influence colony health is the microbial community. Although honey bee worker guts have a characteristic community of bee-specific microbes, the honey bee queen digestive tracts are colonized predominantly by a single acetic acid bacterium tentatively named 'Parasaccharibacter apium'. This bacterium is related to flower-associated microbes such as Saccharibacter floricola, and initial phylogenetic analyses placed it as sister to these environmental bacteria. We used a combination of phylogenetic and sequence identity methods to better resolve evolutionary relationships among 'P. apium', strains in the genus Saccharibacter, and strains in the closely related genus Bombella. Interestingly, measures of genome-wide average nucleotide identity and aligned fraction, coupled with phylogenetic placement, indicate that many strains labelled as 'P. apium' and Saccharibacter species are all the same species as Bombella apis. We propose reclassifying these strains as Bombella apis and outline the data supporting that classification below.
Assuntos
Acetobacteraceae , Ácidos Graxos , Acetobacteraceae/genética , Animais , Técnicas de Tipagem Bacteriana , Composição de Bases , Abelhas , DNA Bacteriano/genética , Ácidos Graxos/química , Filogenia , RNA Ribossômico 16S/genética , Análise de Sequência de DNARESUMO
Honey bees (Apis mellifera) provide vital pollination services for a variety of agricultural crops around the world and are known to host a consistent core bacterial microbiome. This symbiotic microbial community is essential to many facets of bee health, including likely nutrient acquisition, disease prevention and optimal physiological function. Being that the bee microbiome is likely involved in the digestion of nutrients, we either provided or excluded honey bee colonies from supplemental floral forage before being used for almond pollination. We then used 16S rRNA gene sequencing to examine the effects of forage treatment on the bees' microbial gut communities over four months. In agreement with previous studies, we found that the honey bee gut microbiota is quite stable over time. Similarly, we compared the gut communities of bees from separate colonies and sisters sampled from within the same hive over four months. Surprisingly, we found that the gut microbial communities of individual sisters from the same colony can exhibit as much variation as bees from different colonies. Supplemental floral forage had a subtle effect on the composition of the microbiome during the month of March only, with strains of Gilliamella apicola, Lactobacillus, and Bartonella being less proportionally abundant in bees exposed to forage in the winter. Collectively, our findings show that there is unexpected longitudinal variation within the gut microbial communities of sister honey bees and that supplemental floral forage can subtly alter the microbiome of managed honey bees.
Assuntos
Bactérias/isolamento & purificação , Abelhas/microbiologia , Microbioma Gastrointestinal , Animais , Bactérias/classificação , Bactérias/genética , Abelhas/fisiologia , Trato Gastrointestinal/microbiologia , Filogenia , Polinização , SimbioseRESUMO
Carbohydrate-active enzymes play an important role in the honey bee (Apis mellifera) due to its dietary specialization on plant-based nutrition. Secretory glycoside hydrolases (GHs) produced in worker head glands aid in the processing of floral nectar into honey and are expressed in accordance with age-based division of labor. Pollen utilization by the honey bee has been investigated in considerable detail, but little is known about the metabolic fate of indigestible carbohydrates and glycosides in pollen biomass. Here, we demonstrate that pollen consumption stimulates the hydrolysis of sugars that are toxic to the bee (xylose, arabinose, mannose). GHs produced in the head accumulate in the midgut and persist in the hindgut that harbors a core microbial community composed of approximately 108 bacterial cells. Pollen consumption significantly impacted total and specific bacterial abundance in the digestive tract. Bacterial isolates representing major fermentative gut phylotypes exhibited primarily membrane-bound GH activities that may function in tandem with soluble host enzymes retained in the hindgut. Additionally, we found that plant-originating ß-galactosidase activity in pollen may be sufficient, in some cases, for probable physiological activity in the gut. These findings emphasize the potential relative contributions of host, bacteria, and pollen enzyme activities to carbohydrate breakdown, which may be tied to gut microbiome dynamics and associated host nutrition.
Assuntos
Abelhas/fisiologia , Metabolismo dos Carboidratos , Digestão , Microbiota , Pólen , Animais , Abelhas/microbiologia , Trato Gastrointestinal/microbiologia , Glicosídeo Hidrolases/metabolismoRESUMO
Dysbiosis, defined as unhealthy shifts in bacterial community composition, can lower the colonization resistance of the gut to intrinsic pathogens. Here, we determined the effect of diet age and type on the health and bacterial community composition of the honeybee (Apis mellifera). We fed newly emerged bees fresh or aged diets, and then recorded host development and bacterial community composition from four distinct regions of the hosts' digestive tract. Feeding fresh pollen or fresh substitute, we found no difference in host mortality, diet consumption, development or microbial community composition. In contrast, bees fed aged diets suffered impaired development, increased mortality and developed a significantly dysbiotic microbiome. The consumption of aged diets resulted in a significant reduction in the core ileum bacterium Snodgrassella alvi and a corresponding increase in intrinsic pathogen Frischella perrara. Moreover, the relative abundance of S. alvi in the ileum was positively correlated with host survival and development. The inverse was true for both F. perrara and Parasacharibacter apium. Collectively, our findings suggest that the early establishment of S. alvi is associated with healthy nurse development and potentially excludes F. perrara and P. apium from the ileum. Although at low abundance, establishment of the common midgut pathogen Nosema spp. was significantly associated with ileum dysbiosis and associated host deficiencies. Moreover, dysbiosis in the ileum was reflected in the rectum, mouthparts and hypopharyngeal glands, suggesting a systemic host effect. Our findings demonstrate that typically occurring alterations in diet quality play a significant role in colony health and the establishment of a dysbiotic gut microbiome.
Assuntos
Abelhas/microbiologia , Dieta/veterinária , Disbiose/microbiologia , Trato Gastrointestinal/microbiologia , Nosema , AnimaisRESUMO
In many vertebrates, social interactions and nutrition can affect the colonization of gut symbionts across generations. In the highly social honey bee, it is unknown to what extent the hive environment and older worker individuals contribute to the generational transmission of core gut bacteria. We used high-throughput sequencing to investigate the effect of nest materials and social contact on the colonization and succession of core hindgut microbiota in workers. With only brief exposure to hive materials following natural eclosion, gut bacterial communities at 3 and 7 days contained phylotypes typically found in the guts of mature adults regardless of treatment. Continuous exposure to nest materials or direct social interactions with mature adults did not affect the diversity or abundance of gut bacterial communities at the scale examined. Similarly, a common pollen supplement fed by beekeepers during pollen dearth had no effect. A consideration of unique OTUs revealed extensive microbial succession independent of treatment. The dominant Lactobacillus strain at 3 days was largely replaced by a different strain at day 7, revealing the colonization signature of a pioneer species. Similar but less pronounced patterns were evident in less abundant OTU's, many of which may influence community succession via alteration of the gut environment. Our results indicate that the process of bacterial community colonization in the hindgut is resilient to changes in the nutritional, hive, and social environment. Greater taxonomic resolution is needed to accurately resolve questions of ecological succession and typical proportional variation within and between core members of the gut bacterial community.
Assuntos
Abelhas/microbiologia , Ecologia , Lactobacillus/classificação , Animais , Carga Bacteriana , Abelhas/crescimento & desenvolvimento , Biodiversidade , Microbioma Gastrointestinal , Relações Interpessoais , Lactobacillus/genética , Lactobacillus/crescimento & desenvolvimento , Microbiota , Filogenia , Pólen/microbiologia , SimbioseRESUMO
BACKGROUND: Honey bees (Apis mellifera) contribute substantially to the worldwide economy and ecosystem health as pollinators. Pollen is essential to the bee's diet, providing protein, lipids, and micronutrients. The dramatic shifts in physiology, anatomy, and behavior that accompany normal worker development are highly plastic and recent work demonstrates that development, particularly the transition from nurse to foraging roles, is greatly impacted by diet. However, the role that diet plays in the developmental transition of newly eclosed bees to nurse workers is poorly understood. To further understand honey bee nutrition and the role of diet in nurse development, we used a high-throughput screen of the transcriptome of 3 day and 8 day old worker bees fed either honey and stored pollen (rich diet) or honey alone (poor diet) within the hive. We employed a three factor (age, diet, age x diet) analysis of the transcriptome to determine whether diet affected nurse worker physiology and whether poor diet altered the developmental processes normally associated with aging. RESULTS: Substantial changes in gene expression occurred due to starvation. Diet-induced changes in gene transcription occurring in younger bees were largely a subset of those occurring in older bees, but certain signatures of starvation were only evident 8 day old workers. Of the 18,542 annotated transcripts in the A. mellifera genome, 150 transcripts exhibited differential expression due to poor diet at 3d of age compared with 17,226 transcripts that differed due to poor diet at 8d of age, and poor diet caused more frequent down-regulation of gene expression in younger bees compared to older bees. In addition, the age-related physiological changes that accompanied early adult development differed due to the diet these young adult bees were fed. More frequent down-regulation of gene expression was observed in developing bees fed a poor diet compared to those fed an adequate diet. Functional analyses also suggest that the physiological and developmental processes occurring in well-fed bees are vastly different than those occurring in pollen deprived bees. Our data support the hypothesis that poor diet causes normal age-related development to go awry. CONCLUSION: Poor nutrition has major consequences for the expression of genes underlying the physiology and age-related development of nurse worker bees. More work is certainly needed to fully understand the consequences of starvation and the complex biology of nutrition and development in this system, but the genes identified in the present study provide a starting point for understanding the consequences of poor diet and for mitigating the economic costs of colony starvation.
Assuntos
Marcadores Genéticos , Estado Nutricional , Animais , Abelhas/genética , Abelhas/crescimento & desenvolvimento , Pólen , RNA Mensageiro/química , RNA Mensageiro/metabolismo , Análise de Sequência de RNA , Fatores de Tempo , TranscriptomaRESUMO
The honey bee hive environment contains a rich microbial community that differs according to niche. Acetobacteraceae Alpha 2.2 (Alpha 2.2) bacteria are present in the food stores, the forager crop, and larvae but at negligible levels in the nurse and forager midgut and hindgut. We first sought to determine the source of Alpha 2.2 in young larvae by assaying the diversity of microbes in nurse crops, hypopharyngeal glands (HGs), and royal jelly (RJ). Amplicon-based pyrosequencing showed that Alpha 2.2 bacteria occupy each of these environments along with a variety of other bacteria, including Lactobacillus kunkeei. RJ and the crop contained fewer bacteria than the HGs, suggesting that these tissues are rather selective environments. Phylogenetic analyses showed that honey bee-derived Alpha 2.2 bacteria are specific to bees that "nurse" the hive's developing brood with HG secretions and are distinct from the Saccharibacter-type bacteria found in bees that provision their young differently, such as with a pollen ball coated in crop-derived contents. Acetobacteraceae can form symbiotic relationships with insects, so we next tested whether Alpha 2.2 increased larval fitness. We cultured 44 Alpha 2.2 strains from young larvae that grouped into nine distinct clades. Three isolates from these nine clades flourished in royal jelly, and one isolate increased larval survival in vitro. We conclude that Alpha 2.2 bacteria are not gut bacteria but are prolific in the crop-HG-RJ-larva niche, passed to the developing brood through nurse worker feeding behavior. We propose the name Parasaccharibacter apium for this bacterial symbiont of bees in the genus Apis.
Assuntos
Acetobacteraceae/isolamento & purificação , Abelhas/microbiologia , Larva/microbiologia , Acetobacteraceae/classificação , Acetobacteraceae/genética , Animais , Abelhas/crescimento & desenvolvimento , Abelhas/fisiologia , DNA Bacteriano/genética , Larva/crescimento & desenvolvimento , Larva/fisiologia , Dados de Sequência Molecular , Filogenia , RNA Ribossômico 16S/genética , SimbioseRESUMO
Honey bee hives are filled with stored pollen, honey, plant resins and wax, all antimicrobial to differing degrees. Stored pollen is the nutritionally rich currency used for colony growth and consists of 40-50% simple sugars. Many studies speculate that prior to consumption by bees, stored pollen undergoes long-term nutrient conversion, becoming more nutritious 'bee bread' as microbes predigest the pollen. We quantified both structural and functional aspects associated with this hypothesis using behavioural assays, bacterial plate counts, microscopy and 454 amplicon sequencing of the 16S rRNA gene from both newly collected and hive-stored pollen. We found that bees preferentially consume fresh pollen stored for <3 days. Newly collected pollen contained few bacteria, values which decreased significantly as pollen were stored >96 h. The estimated microbe to pollen grain surface area ratio was 1:1 000 000 indicating a negligible effect of microbial metabolism on hive-stored pollen. Consistent with these findings, hive-stored pollen grains did not appear compromised according to microscopy. Based on year round 454 amplicon sequencing, bacterial communities of newly collected and hive-stored pollen did not differ, indicating the lack of an emergent microbial community co-evolved to digest stored pollen. In accord with previous culturing and 16S cloning, acid resistant and osmotolerant bacteria like Lactobacillus kunkeei were found in greatest abundance in stored pollen, consistent with the harsh character of this microenvironment. We conclude that stored pollen is not evolved for microbially mediated nutrient conversion, but is a preservative environment due primarily to added honey, nectar, bee secretions and properties of pollen itself.
Assuntos
Bactérias/isolamento & purificação , Abelhas , Pólen/microbiologia , Animais , Bactérias/genética , Contagem de Colônia Microbiana , DNA Bacteriano/genética , Valor Nutritivo , Pólen/química , RNA Ribossômico 16S/genética , Fatores de TempoRESUMO
The health of honey bee queens is crucial for colony success, particularly during stressful periods like overwintering. To accompany a previous longitudinal study of colony and worker health, we explored niche-specific gut microbiota, host gene expression, and pathogen prevalence in honey bee queens overwintering in a warm southern climate. We found differential gene expression and bacterial abundance with respect to various pathogens throughout the season. Biologically older queens had larger microbiotas, particularly enriched in Bombella and Bifidobacterium. Both Deformed Wing Virus A and B subtypes were highest in the fat body tissue in January, correlating with colony Varroa levels, and Deformed Wing Virus titers in workers. High viral titers in queens were associated with decreased vitellogenin expression, suggesting a potential trade-off between immune function and reproductive capacity. Additionally, we found a complex and dynamic relationship between these viral loads and immune gene expression, indicating a possible breakdown in the coordinated immune response as the season progressed. Our study also revealed a potential link between Nosema and Melissococcus plutonius infections in queens, demonstrating that seasonal opportunism is not confined to just workers. Overall, our findings highlight the intricate interplay between pathogens, metabolic state, and immune response in honey bee queens. Combined with worker and colony-level metrics from the same colonies, our findings illustrate the social aspect of queen health and resilience over the winter dearth.
Assuntos
Clima , Vírus de RNA , Abelhas , Animais , Estações do Ano , Estudos LongitudinaisRESUMO
Probiotics are widely used in agriculture including commercial beekeeping, but there is little evidence supporting their effectiveness. Antibiotic treatments can greatly distort the gut microbiome, reducing its protective abilities and facilitating the growth of antibiotic resistant pathogens. Commercial beekeepers regularly apply antibiotics to combat bacterial infections, often followed by an application of non-native probiotics advertised to ease the impact of antibiotic-induced gut dysbiosis. We tested whether probiotics affect the gut microbiome or disease prevalence, or rescue the negative effects of antibiotic induced gut dysbiosis. We found no difference in the gut microbiome or disease markers by probiotic application or antibiotic recovery associated with probiotic treatment. A colony-level application of the antibiotics oxytetracycline and tylosin produced an immediate decrease in gut microbiome size, and over the longer-term, very different and persistent dysbiotic effects on the composition and membership of the hindgut microbiome. Our results demonstrate the lack of probiotic effect or antibiotic rescue, detail the duration and character of dysbiotic states resulting from different antibiotics, and highlight the importance of the gut microbiome for honeybee health.
Assuntos
Oxitetraciclina , Probióticos , Abelhas , Animais , Disbiose , Antibacterianos , TilosinaRESUMO
Honey bee colonies are resource rich and densely populated, generating a constant battle to control microbial growth. Honey is relatively sterile in comparison with beebread: a food storage medium comprising pollen mixed with honey and worker head-gland secretions. Within colonies, the microbes that dominate aerobic niches are abundant throughout social resource space including stored pollen, honey, royal jelly, and the anterior gut segments and mouthparts of both queens and workers. Here, we identify and discuss the microbial load in stored pollen associated with non-Nosema fungi (primarily yeast) and bacteria. We also measured abiotic changes associated with pollen storage and used culturing and qPCR of both fungi and bacteria to investigate changes in stored pollen microbiology by both storage time and season. Over the first week of pollen storage, pH and water availability decreased significantly. Following an initial drop in microbial abundance at day one, both yeasts and bacteria multiply rapidly during day two. Both types of microbes then decline at 3-7 days, but the highly osmotolerant yeasts persist longer than the bacteria. Based on measures of absolute abundance, bacteria and yeast are controlled by similar factors during pollen storage. This work contributes to our understanding of host-microbial interactions in the honey bee gut and colony and the effect of pollen storage on microbial growth, nutrition, and bee health.
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Honey bee colonies maintain viable queens in part through communication with Queen Mandibular Pheromone (QMP), a mixture that signals the queen's presence and reproductive quality to workers. In turn, workers are thought to provide retinue queen care or replace queens partially based on QMP profiles. We examined the effects of seasonal dearth (overwintering in a warm subtropical location) on queen-worker interactions. Retinue worker responses to continuously ovipositing queens were considered in view of QMP signaling and queen reproductive quality. QMP signaling was estimated from QMP residues recovered from nest worker bodies, which is the primary mode of QMP transfer from the queen to the colony at large. QMP residues varied seasonally but not at all with queen reproductive quality (spermatheca sperm storage, ovary protein and lipid contents). 9-HDA and 9-ODA were lower in January than other months. HOB decreased from July to January, while HVA, a component associated with mated queens, increased sharply in January. Despite these seasonal signaling differences, retinue workers attended queens at similar levels through the months. In terms of reproductive quality, queens did not differ over the months in matedness (spermatheca sperm storage) or physiological age (protein carbonyl content), but varied in nutrient allocation to reproductive and non-reproductive tissues. Queen ovaries contained more protein in September than in November, and more lipid in July and September than in November and January. Queen fat bodies had more protein in July than September or November, but less lipid in July and September than November or January. Retinue worker responses did not vary with seasonal QMP changes, but reflected overall continuous brood rearing efforts and queen matedness throughout the year. The absence of seasonal differences in worker responses to QMP should be considered in the broader context of continuous reproductive efforts in warm subtropical colonies.
RESUMO
As essential pollinators of ecosystems and agriculture, honey bees (Apis mellifera) are host to a variety of pathogens that result in colony loss. Two highly prevalent larval diseases are European foulbrood (EFB) attributed to the bacterium Melissococcus plutonius, and Varroosis wherein larvae can be afflicted by one or more paralytic viruses. Here we used high-throughput sequencing and qPCR to detail microbial succession of larval development from six diseased, and one disease-free apiary. The disease-free larval microbiome revealed a variety of disease-associated bacteria in early larval instars, but later developmental stages were dominated by beneficial symbionts. Microbial succession associated with EFB pathology differed by apiary, characterized by associations with various gram-positive bacteria. At one apiary, diseased larvae were uniquely described as "melting and deflated", symptoms associated with Varroosis. We found that Acute Bee Paralysis Virus (ABPV) levels were significantly associated with these symptoms, and various gram-negative bacteria became opportunistic in the guts of ABPV afflicted larvae. Perhaps contributing to disease progression, the ABPV associated microbiome was significantly depleted of gram-positive bacteria, a likely result of recent antibiotic application. Our results contribute to the understanding of brood disease diagnosis and treatment, a growing problem for beekeeping and agriculture worldwide.
Assuntos
Bactérias , Ecossistema , Abelhas , Animais , Larva/microbiologia , Bactérias Gram-Positivas , Criação de AbelhasRESUMO
Ants dominate many terrestrial ecosystems, yet we know little about their nutritional physiology and ecology. While traditionally viewed as predators and scavengers, recent isotopic studies revealed that many dominant ant species are functional herbivores. As with other insects with nitrogen-poor diets, it is hypothesized that these ants rely on symbiotic bacteria for nutritional supplementation. In this study, we used cloning and 16S sequencing to further characterize the bacterial flora of several herbivorous ants, while also examining the beta diversity of bacterial communities within and between ant species from different trophic levels. Through estimating phylogenetic overlap between these communities, we tested the hypothesis that ecologically or phylogenetically similar groups of ants harbor similar microbial flora. Our findings reveal: (i) clear differences in bacterial communities harbored by predatory and herbivorous ants; (ii) notable similarities among communities from distantly related herbivorous ants and (iii) similar communities shared by different predatory army ant species. Focusing on one herbivorous ant tribe, the Cephalotini, we detected five major bacterial taxa that likely represent the core microbiota. Metabolic functions of bacterial relatives suggest that these microbes may play roles in fixing, recycling, or upgrading nitrogen. Overall, our findings reveal that similar microbial communities are harbored by ants from similar trophic niches and, to a greater extent, by related ants from the same colonies, species, genera, and tribes. These trends hint at coevolved histories between ants and microbes, suggesting new possibilities for roles of bacteria in the evolution of both herbivores and carnivores from the ant family Formicidae.
Assuntos
Formigas/microbiologia , Bactérias/classificação , Bactérias/genética , Metagenoma , Animais , Formigas/classificação , Formigas/fisiologia , Biodiversidade , Sistema Digestório/microbiologia , Herbivoria , RNA Bacteriano/genética , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , SimbioseRESUMO
Winter forage dearth is a major contributor to honey bee colony loss and can influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the social environment on many levels. During winter or forage dearth, 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 workers in early and late winter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor environments. Our results provide novel evidence that social immune gene expression is associated with worker longevity, and highlight the midgut as a target of opportunistic disease during winter. Host microbial interactions suggest opportunistic disease progression and resistance in long-lived workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and non-core bacterial abundance. The results are consistent with increased social immunity, including host associations with the social microbiota, and a social immune response by long-lived workers to combat microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival during winter forage dearth.
Assuntos
Clima , Microbiota , Animais , Abelhas/genética , Expressão Gênica , Humanos , Longevidade/genética , Microbiota/genética , Estações do AnoRESUMO
The highly social honey bee has dense populations but a significantly reduced repertoire of immune genes relative to solitary species, suggesting a greater reliance on social immunity. Here we investigate immune gene expression and gut microbial succession in queens during colony introduction. Recently mated queens were placed into an active colony or a storage hive for multiple queens: a queen-bank. Feeding intensity, social context, and metabolic demand differ greatly between the two environments. After 3 weeks, we examined gene expression associated with oxidative stress and immunity and performed high-throughput sequencing of the queen gut microbiome across four alimentary tract niches. Microbiota and gene expression in the queen hindgut differed by time, queen breeder source, and metabolic environment. In the ileum, upregulation of most immune and oxidative stress genes occurred regardless of treatment conditions, suggesting postmating effects on gut gene expression. Counterintuitively, queens exposed to the more social colony environment contained significantly less bacterial diversity indicative of social immune factors shaping the queens microbiome. Queen bank queens resembled much older queens with decreased Alpha 2.1, greater abundance of Lactobacillus firm5 and Bifidobacterium in the hindgut, and significantly larger ileum microbiotas, dominated by blooms of Snodgrassella alvi. Combined with earlier findings, we conclude that the queen gut microbiota experiences an extended period of microbial succession associated with queen breeder source, postmating development, and colony assimilation. IMPORTANCE In modern agriculture, honey bee queen failure is repeatedly cited as one of the major reasons for yearly colony loss. Here we discovered that the honey bee queen gut microbiota alters according to early social environment and is strongly tied to the identity of the queen breeder. Like human examples, this early life variation appears to set the trajectory for ecological succession associated with social assimilation and queen productivity. The high metabolic demand of natural colony assimilation is associated with less bacterial diversity, a smaller hindgut microbiome, and a downregulation of genes that control pathogens and oxidative stress. Queens placed in less social environments with low metabolic demand (queen banks) developed a gut microbiota that resembled much older queens that produce fewer eggs. The queens key reproductive role in the colony may rely in part on a gut microbiome shaped by social immunity and the early queen rearing environment.
Assuntos
Microbioma Gastrointestinal , Microbiota , Animais , Bactérias/genética , Abelhas , Bifidobacterium , Humanos , Lactobacillus/genética , Meio SocialRESUMO
Honey bees exhibit an elaborate social structure based in part on an age-related division of labor. Young workers perform tasks inside the hive, while older workers forage outside the hive, tasks associated with distinct diets and metabolism. Critical to colony fitness, the work force can respond rapidly to changes in the environment or colony demography and assume emergency tasks, resulting in young foragers or old nurses. We hypothesized that both task and age affect the gut microbiota consistent with changes to host diet and physiology. We performed two experiments inducing precocious foragers and reverted nurses, then quantified tissue-specific gut microbiota and host metabolic state associated with nutrition, immunity and oxidative stress. In the precocious forager experiment, both age and ontogeny explained differences in midgut and ileum microbiota, but host gene expression was best explained by an interaction of these factors. Precocious foragers were nutritionally deficient, and incurred higher levels of oxidative damage relative to age-matched nurses. In the oldest workers, reverted nurses, the oxidative damage associated with age and past foraging was compensated by high Vitellogenin expression, which exceeded that of young nurses. Host-microbial interactions were evident throughout the dataset, highlighted by an age-based increase of Gilliamella abundance and diversity concurrent with increased carbonyl accumulation and CuZnSOD expression. The results in general contribute to an understanding of ecological succession of the worker gut microbiota, defining the species-level transition from nurse to forager.
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In insect societies, worker vs. queen development (reproductive caste) is typically governed by environmental factors, but many Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Same-lineage matings produce fertile queens while alternate-lineage matings produce sterile workers. Because new virgin queens mate randomly with multiple males of each lineage type, and both worker and queen phenotypes are required for colony growth and future reproduction, fitness is influenced by the relative frequency of each lineage involved in the mutualistic breeding system. While models based solely on frequency-dependent selection predict the convergence of lineage frequencies towards equal (0.5/0.5), we surveyed the lineage ratios of 49 systems across the range of the mutualism and found that the global lineage frequency differed significantly from equal. Multiple regression analysis of our system survey data revealed that the density and relative frequency of one lineage decreases at lower elevations, while the frequency of the alternate lineage increases with total colony density. While the production of the first worker cohort is largely frequency dependent, relying on the random acquisition of worker-biased sperm stores, subsequent colony growth is independent of lineage frequency. We provide a simulation model showing that a net ecological advantage held by one lineage can lead to the maintenance of stable but asymmetric lineage frequencies. Collectively, these findings suggest that a combination of frequency-dependent and frequency-independent mechanisms can generate many different localized and independently evolving system equilibria.
Assuntos
Formigas/fisiologia , Reprodução/fisiologia , Comportamento Sexual Animal , Simbiose , Animais , Formigas/genética , Arizona , Meio Ambiente , Feminino , Genes de Insetos , Masculino , Modelos Biológicos , Dados de Sequência Molecular , New Mexico , Densidade Demográfica , Análise de Regressão , Reprodução/genéticaRESUMO
Honey bee overwintering health is essential to meet the demands of spring pollination. Managed honey bee colonies are overwintered in a variety of climates, and increasing rates of winter colony loss have prompted investigations into overwintering management, including indoor climate controlled overwintering. Central to colony health, the worker hindgut gut microbiota has been largely ignored in this context. We sequenced the hindgut microbiota of overwintering workers from both a warm southern climate and controlled indoor cold climate. Congruently, we sampled a cohort of known chronological age to estimate worker longevity in southern climates, and assess age-associated changes in the core hindgut microbiota. We found that worker longevity over winter in southern climates was much lower than that recorded for northern climates. Workers showed decreased bacterial and fungal load with age, but the relative structure of the core hindgut microbiome remained stable. Compared to cold indoor wintering, collective microbiota changes in the southern outdoor climate suggest compromised host physiology. Fungal abundance increased by two orders of magnitude in southern climate hindguts and was positively correlated with non-core, likely opportunistic bacteria. Our results contribute to understanding overwintering honey bee biology and microbial ecology and provide insight into overwintering strategies.