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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.
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Clima , Virus ARN , Abejas , Animales , Estaciones del Año , Estudios LongitudinalesRESUMEN
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.
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Oxitetraciclina , Probióticos , Abejas , Animales , Disbiosis , Antibacterianos , TilosinaRESUMEN
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.
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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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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.
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Bacterias , Ecosistema , Abejas , Animales , Larva/microbiología , Bacterias Grampositivas , ApiculturaRESUMEN
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.
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Microbioma Gastrointestinal , Microbiota , Abejas , Animales , Interacción Social , Bacterias/genética , DietaRESUMEN
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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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.
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Microbioma Gastrointestinal , Microbiota , Animales , Bacterias/genética , Abejas , Bifidobacterium , Humanos , Lactobacillus/genética , Medio SocialRESUMEN
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.
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Clima , Microbiota , Animales , Abejas/genética , Expresión Génica , Humanos , Longevidad/genética , Microbiota/genética , Estaciones del AñoRESUMEN
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.
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Acetobacteraceae , Ácidos Grasos , Acetobacteraceae/genética , Animales , Técnicas de Tipificación Bacteriana , Composición de Base , Abejas , ADN Bacteriano/genética , Ácidos Grasos/química , Filogenia , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADNRESUMEN
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.
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[This corrects the article DOI: 10.1371/journal.pone.0175933.].
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European honey bees (Apis mellifera Linnaeus) are beneficial insects that provide essential pollination services for agriculture and ecosystems worldwide. Modern commercial beekeeping is plagued by a variety of pathogenic and environmental stressors often confounding attempts to understand colony loss. European foulbrood (EFB) is considered a larval-specific disease whose causative agent, Melissococcus plutonius, has received limited attention due to methodological challenges in the field and laboratory. Here, we improve the experimental and informational context of larval disease with the end goal of developing an EFB management strategy. We sequenced the bacterial microbiota associated with larval disease transmission, isolated a variety of M.plutonius strains, determined their virulence against larvae in vitro, and explored the potential for probiotic treatment of EFB disease. The larval microbiota was a low diversity environment similar to honey, while worker mouthparts and stored pollen contained significantly greater bacterial diversity. Virulence of M. plutonius against larvae varied markedly by strain and inoculant concentration. Our chosen probiotic, Parasaccharibacter apium strain C6, did not improve larval survival when introduced alone, or in combination with a virulent EFB strain. We discuss the importance of positive and negative controls for in vitro studies of the larval microbiome and disease.
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Honey bees collect and apply plant resins to the interior of their nest cavity, in order to form a layer around the nest cavity called a propolis envelope. Propolis displays antimicrobial activity against honey bee pathogens, but the effect of propolis on the honey bee microbiome is unknown. Honey bees do not intentionally consume propolis, but they do manipulate propolis with their mouthparts. Because honey bee mouthparts are used for collecting and storing nectar and pollen, grooming and trophallaxis between adults, feeding larvae, and cleaning the colony, they are an important interface between the bees' external and internal environments and serve as a transmission route for core gut bacteria and pathogens alike. We hypothesized that the antimicrobial activity of an experimentally applied propolis envelope would influence the bacterial diversity and abundance of the worker mouthpart microbiome. The results revealed that the mouthparts of worker bees in colonies with a propolis envelope exhibited a significantly lower bacterial diversity and significantly higher bacterial abundance compared to the mouthparts of bees in colonies without a propolis envelope. Based on the taxonomic results, the propolis envelope appeared to reduce pathogenic or opportunistic microbes and promote the proliferation of putatively beneficial microbes on the honey bee mouthparts, thus reinforcing the core microbiome of the mouthpart niche.
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Microbial metabolites are considered important drivers of diet-based microbiota influence on the host, however, mechanistic models are confounded by interactions between diet, microbiota function, and host physiology. The honey bee harbors a simple microbiota that produces organic acids as fermentation products of dietary nectar and pollen, making it a model for gut microbiota research. Herein, we demonstrate that bacterial abundance in the honey bee gut is partially associated with the anterior rectum epithelium. We used dietary pollen restriction and organic acid feeding treatments to obtain information about the role of undigested pollen as a microbiota growth substrate and the impact of bacterial fermentation products on honey bee enteroendocrine signaling. Pollen restriction markedly reduced total and specific bacterial 16S rRNA abundance in the anterior rectum but not in the ileum. Anterior rectum expression levels of bacterial fermentative enzyme gene transcripts (acetate kinase, lactate dehydrogenase, and hydroxybutyryl-CoA dehydrogenase) were reduced in association with diet-induced microbiota shifts. To evaluate the effects of fermentative metabolites on host enteroendocrine function, pollen-restricted bees were fed an equimolar mixture of organic acid sodium salts (acetate, lactate, butyrate, formate, and succinate). Organic acid feeding significantly impacted hindgut enteroendocrine signaling gene expression, rescuing some effects of pollen restriction. This was specifically manifested by tissue-dependent expression patterns of neuropeptide F and allatostatin pathways, which are implicated in energy metabolism and feeding behaviors. Our findings provide new insights into the diet-microbiota-host axis in honey bees and may inform future efforts to improve bee health through diet-based microbiota manipulations.
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Honey bee colony performance and health are intimately linked to the foraging environment. Recent evidence suggests that the US Conservation Reserve Program (CRP) has a positive impact on environmental suitability for supporting honey bee apiaries. However, relatively little is known about the influence of habitat conservation efforts on honey bee colony health. Identifying specific factors that influence bee health at the colony level incorporates longitudinal monitoring of physiology across diverse environments. Using a pooled-sampling method to overcome individual variation, we monitored colony-level molecular biomarkers during critical pre- and post-winter time points. Major categories of colony health (nutrition, oxidative stress resistance, and immunity) were impacted by apiary site. In general, apiaries within foraging distance of CRP lands showed improved performance and higher gene expression of vitellogenin (vg), a nutritionally regulated protein with central storage and regulatory functions. Mirroring vg levels, gene transcripts encoding antioxidant enzymes and immune-related proteins were typically higher in colonies exposed to CRP environments. Our study highlights the potential of CRP lands to improve pollinator health and the utility of colony-level molecular diagnostics to assess environmental suitability for honey bees.
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Apicultura , Abejas/fisiología , Conservación de los Recursos Naturales , Animales , Ecosistema , Estado Nutricional , Estaciones del Año , Vitelogeninas/metabolismoRESUMEN
Honey bee colony nutritional ecology relies on the acquisition and assimilation of floral resources across a landscape with changing forage conditions. Here, we examined the impact of nutrition and queen age on colony health across extended periods of reduced forage in a southern climate. We measured conventional hive metrics as well as colony-level gene expression of eight immune-related genes and three recently identified homologs of vitellogenin (vg), a storage glycolipoprotein central to colony nutritional state, immunity, oxidative stress resistance and life span regulation. Across three apiary sites, concurrent longitudinal changes in colony-level gene expression and nutritional state reflected the production of diutinus (winter) bees physiologically altered for long-term nutrient storage. Brood production by young queens was significantly greater than that of old queens, and was augmented by feeding colonies supplemental pollen. Expression analyses of recently identified vg homologs (vg-like-A, -B, and -C) revealed distinct patterns that correlated with colony performance, phenology, and immune-related gene transcript levels. Our findings provide new insights into dynamics underlying managed colony performance on a large scale. Colony-level, molecular physiological profiling is a promising approach to effectively identify factors influencing honey bee health in future landscape and nutrition studies.
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Adaptación Fisiológica , Abejas/fisiología , Clima , Estado Nutricional , Estaciones del Año , Factores de Edad , Animales , Colapso de Colonias/prevención & control , Regulación de la Expresión Génica , Longevidad , Estrés Oxidativo , VitelogeninasRESUMEN
BACKGROUND: In 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 with much lower expression of oxidative stress genes, suggesting a very different host environment for age-associated microbial succession. RESULTS: We sequenced the microbiota of 63 honey bee queens exploring two chronological ages and four alimentary tract niches. To control for genetic and environmental 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. CONCLUSIONS: We present a model system linking changes in gut microbiota to diet and longevity, two of the most confounding variables in human microbiota research. 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, age-related changes in the honey bee microbiota reflect the regulatory anatomy of reproductive host metabolism. Our synthesis suggests that the evolution of colony-level reproductive physiology formed the context for host-microbial interactions and age-related succession of honey bee microbiota.
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Bifidobacterium/aislamiento & purificación , Microbioma Gastrointestinal/genética , Tracto Gastrointestinal/microbiología , Lactobacillus/aislamiento & purificación , Longevidad/fisiología , Proteobacteria/aislamiento & purificación , Animales , Secuencia de Bases , Abejas , Bifidobacterium/clasificación , Bifidobacterium/genética , Lactobacillus/clasificación , Lactobacillus/genética , Estrés Oxidativo/genética , Proteobacteria/clasificación , Proteobacteria/genética , ARN Ribosómico 16S/genética , Análisis de Secuencia de ADNRESUMEN
Parasaccharibacter apium displays multiple ecological strategies in its honey bee host. We sequenced the genomes of four strains found in larvae and the adult gut in order to better understand its ecology and relationship to other Acetobacteraceae The P. apium genome consists of 2,009,892 bp and 1,830 protein-coding genes.
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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.