scholarly journals Honey bee genetics shape the strain-level structure of gut microbiota in social transmission

Microbiome ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Jiaqiang Wu ◽  
Haoyu Lang ◽  
Xiaohuan Mu ◽  
Zijing Zhang ◽  
Qinzhi Su ◽  
...  

Abstract Background Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. Results We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. Conclusions Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions.

2020 ◽  
Author(s):  
Jiaqiang Wu ◽  
Haoyu Lang ◽  
Xiaohuan Mu ◽  
Zijing Zhang ◽  
Qinzhi Su ◽  
...  

AbstractHoneybee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honeybees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of queen, we hypothesize that the microbiota structure can be shaped by host genetics. We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of individuals from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population”-level. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. A genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene that is specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the expression and alternative splicing of the gluR-B gene, which is associated with an altered circulating metabolomic profile. Our results indicated that host genetics influence the bee gut composition, and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honeybees have been used extensively as a model organism for social behaviors, genetics, and gut microbiome. Further identification of host genetic function as shaping force of microbial structure will advance our understanding of the host-microbe interactions.


2020 ◽  
Author(s):  
Jiaqiang Wu ◽  
Haoyu Lang ◽  
Xiaohuan Mu ◽  
Zijing Zhang ◽  
Qinzhi Su ◽  
...  

Abstract Background : Honeybee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honeybees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of queen, we hypothesize that the microbiota structure can be shaped by host genetics. Results : We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of individuals from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population”-level. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. A genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene that is specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the expression and alternative splicing of the gluR-B gene, which is associated with an altered circulating metabolomic profile. Conclusions : Our results indicated that host genetics influence the bee gut composition, and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honeybees have been used extensively as a model organism for social behaviors, genetics, and gut microbiome. Further identification of host genetic function as shaping force of microbial structure will advance our understanding of the host-microbe interactions.


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.


Author(s):  
Kirsten M Ellegaard ◽  
Shota Suenami ◽  
Ryo Miyazaki ◽  
Philipp Engel

AbstractMost bacterial species encompass strains with vastly different gene content. Strain diversity in microbial communities is therefore considered to be of functional importance. Yet, little is known about the extent to which related microbial communities differ in diversity at this level and which underlying mechanisms may constrain and maintain strain-level diversity. Here, we used shotgun metagenomics to characterize and compare the gut microbiota of two honey bee species, Apis mellifera and Apis cerana, which have diverged about 6 mio years ago. While both host species are colonized by largely overlapping bacterial 16S rRNA phylotypes, we find that their communities are highly host-specific when analyzed with genomic resolution. Despite their similar ecology, A. mellifera displayed a much higher extent of strain-level diversity and functional gene content in the microbiota than A. cerana, per colony and per individual bee. In particular, the gene repertoire for polysaccharide degradation was massively expanded in the microbiota of A. mellifera relative to A. cerana. Bee management practices, divergent ecological adaptation, or habitat size may have contributed to the observed differences in microbiota composition of these two key pollinator species. Our results illustrate that the gut microbiota of closely related animal hosts can differ vastly in genomic diversity despite sharing similar levels of diversity at the 16S rRNA gene. This is likely to have consequences for gut microbiota functioning and host-symbiont interactions, highlighting the need for metagenomic studies to understand the ecology and evolution of microbial communities.


2021 ◽  
Author(s):  
Yueqiong Ni ◽  
Zoltan Lohinai ◽  
Yoshitaro Heshiki ◽  
Balazs Dome ◽  
Judit Moldvay ◽  
...  

AbstractCachexia is associated with decreased survival in cancer patients and has a prevalence of up to 80%. The etiology of cachexia is poorly understood, and limited treatment options exist. Here, we investigated the role of the human gut microbiome in cachexia by integrating shotgun metagenomics and plasma metabolomics of 31 lung cancer patients. The cachexia group showed significant differences in the gut microbial composition, functional pathways of the metagenome, and the related plasma metabolites compared to non-cachectic patients. Branched-chain amino acids (BCAAs), methylhistamine, and vitamins were significantly depleted in the plasma of cachexia patients, which was also reflected in the depletion of relevant gut microbiota functional pathways. The enrichment of BCAAs and 3-oxocholic acid in non-cachectic patients were positively correlated with gut microbial species Prevotella copri and Lactobacillus gasseri, respectively. Furthermore, the gut microbiota capacity for lipopolysaccharides biosynthesis was significantly enriched in cachectic patients. The involvement of the gut microbiome in cachexia was further observed in a high-performance machine learning model using solely gut microbial features. Our study demonstrates the links between cachectic host metabolism and specific gut microbial species and functions in a clinical setting, suggesting that the gut microbiota could have an influence on cachexia with possible therapeutic applications.


2020 ◽  
Author(s):  
Yueqiong Ni ◽  
Zoltan Lohinai ◽  
Yoshitaro Heshiki ◽  
Balazs Dome ◽  
Judit Moldvay ◽  
...  

Abstract Background Cachexia is associated with decreased survival in cancer patients and has a prevalence of up to 80%. The etiology of cachexia is poorly understood, and limited treatment options exist. Here, we investigated the role of the human gut microbiome in the clinical setting by integrating shotgun metagenomics and plasma metabolomics of 38 lung cancer patients, with known cachexia status. Results The cachexia group showed significant differences in the gut microbial composition, functional pathways of the metagenome, and the related plasma metabolites compared to non-cachectic patients. Branched-chain amino acids (BCAAs), methylhistamine, as well as vitamins, were significantly depleted in the plasma of cachexia patients, which was also reflected in the depletion of relevant gut microbiota functional pathways. The enrichment of plasma BCAAs and 3-oxocholic acid in non-cachectic patients were positively correlated with the gut microbial species Prevotella copri and Lactobacillus gasseri, respectively. Furthermore, the gut microbiota capacity for lipopolysaccharides biosynthesis was significantly enriched in the cancer cachectic patients. The involvement of gut microbiome in cachexia was further observed in a high-performance machine learning model that uses solely gut microbial taxonomic and pathway features to differentiate cachectic from non-cachectic cancer patients. Conclusions Our study demonstrates the links between host metabolism and specific gut microbial species and functions in a clinical setting, suggesting that the gut microbiota could have an influence on cachexia with possible future therapeutic applications.


2021 ◽  
Vol 3 (1) ◽  
Author(s):  
Yuliaxis Ramayo-Caldas ◽  
Laura M. Zingaretti ◽  
David Pérez-Pascual ◽  
Pamela A. Alexandre ◽  
Antonio Reverter ◽  
...  

Abstract Background The gut microbiota influences host performance playing a relevant role in homeostasis and function of the immune system. The aim of the present work was to identify microbial signatures linked to immunity traits and to characterize the contribution of host-genome and gut microbiota to the immunocompetence in healthy pigs. Results To achieve this goal, we undertook a combination of network, mixed model and microbial-wide association studies (MWAS) for 21 immunity traits and the relative abundance of gut bacterial communities in 389 pigs genotyped for 70K SNPs. The heritability (h2; proportion of phenotypic variance explained by the host genetics) and microbiability (m2; proportion of variance explained by the microbial composition) showed similar values for most of the analyzed immunity traits, except for both IgM and IgG in plasma that was dominated by the host genetics, and the haptoglobin in serum which was the trait with larger m2 (0.275) compared to h2 (0.138). Results from the MWAS suggested a polymicrobial nature of the immunocompetence in pigs and revealed associations between pigs gut microbiota composition and 15 of the analyzed traits. The lymphocytes phagocytic capacity (quantified as mean fluorescence) and the total number of monocytes in blood were the traits associated with the largest number of taxa (6 taxa). Among the associations identified by MWAS, 30% were confirmed by an information theory network approach. The strongest confirmed associations were between Fibrobacter and phagocytic capacity of lymphocytes (r = 0.37), followed by correlations between Streptococcus and the percentage of phagocytic lymphocytes (r = -0.34) and between Megasphaera and serum concentration of haptoglobin (r = 0.26). In the interaction network, Streptococcus and percentage of phagocytic lymphocytes were the keystone bacterial and immune-trait, respectively. Conclusions Overall, our findings reveal an important connection between gut microbiota composition and immunity traits in pigs, and highlight the need to consider both sources of information, host genome and microbial levels, to accurately characterize immunocompetence in pigs.


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.


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