Global composition of the bacteriophage community in honeybees

The microbial communities in animal digestive systems are critical to host development and health. These assemblages of primarily viruses, bacteria, and fungi stimulate the immune system during development, synthesize important chemical compounds like hormones, aid in digestion, competitively exclude pathogens, etc. The bacteriophages in animal microbiomes are harder to characterize than the bacterial or fungal components of the microbiome and thus we know comparatively little about the temporal and spatial dynamics of bacteriophage communities in animal digestive systems. Recently, the bacteriophages of the honeybee gut were characterized in two European bee populations. Most of the bacteriophages described in these two reports were novel, encoded many metabolic genes in their genomes, and had a community structure that suggests coevolution with their bacterial hosts. To describe the conservation of bacteriophages in bees and begin to understand their role in the bee microbiome, we sequenced the virome of Apis mellifera from Austin, Texas and compared bacteriophage composition between three locations around the world. We found that most bacteriophages from Austin are novel, sharing no sequence similarity to anything in public repositories. However, many bacteriophages are shared among the three bee viromes, indicating specialization of bacteriophages in the bee gut. Our study along with the two previous bee virome studies shows that the bee gut bacteriophage community is simple compared to that of many animals, consisting of several hundred types of bacteriophages that primarily infect four of the dominant bacterial phylotypes in the bee gut.

Compartmentalization of bacterial and fungal microbiomes in the gut of adult honeybees

The core gut microbiome of adult honeybee comprises a set of recurring bacterial phylotypes, accompanied by lineage-specific, variable, and less abundant environmental bacterial phylotypes. Several mutual interactions and functional services to the host, including the support provided for growth, hormonal signaling, and behavior, are attributed to the core and lineage-specific taxa. By contrast, the diversity and distribution of the minor environmental phylotypes and fungal members in the gut remain overlooked. In the present study, we hypothesized that the microbial components of forager honeybees (i.e., core bacteria, minor environmental phylotypes, and fungal members) are compartmentalized along the gut portions. The diversity and distribution of such three microbial components were investigated in the context of the physico-chemical conditions of different gut compartments. We observed that changes in the distribution and abundance of microbial components in the gut are consistently compartment-specific for all the three microbial components, indicating that the ecological and physiological interactions among the host and microbiome vary with changing physico-chemical and metabolic conditions of the gut.

Honeybee gut microbiota modulates host behaviors and neurological processes

Honeybee is a highly social insect with a reach behavioral repertoire and is a versatile model for neurobiological research. The honeybee gut microbiota is composed of a limited number of bacterial phylotypes that play an important role in host health. However, it remains unclear whether the microbiota can shape brain profiles and behaviors. Here, we revealed that the gut microbiota is requisite for the olfactory learning and memory ability of honeybees and alters the level of neurotransmitters in the brain. Transcriptomic and proteomic analysis showed distinctive gene expression and protein signatures for gnotobiotic bees associated with different gut bacteria. Specifically, genes related to olfactory functions and labor division are most upregulated. Moreover, differentially spliced genes in the brains of colonized bees largely overlapped with the datasets for human autism. The circulating metabolome profiles identified that different gut species regulated specific module of metabolites in the host hemolymph. Most altered metabolites are involved in the amino acid and glycerophospholipid metabolism pathways for the production of neuroactive compounds. Finally, antibiotic treatment disturbed the gut community and the nursing behavior of worker bees under field conditions. The brain transcripts and gut metabolism was also greatly interfered in treated bees. Collectively, we demonstrate that the gut microbiota regulates honeybee behaviors, brain gene transcription, and the circulating metabolism. Our findings highlight the contributions of honeybee gut microbes in the neurological processes with striking parallels to those found in other animals, thus providing a promising model to understand the host-microbe interactions via the gut-brain axis.

Honeybee gut microbiota modulates host behaviors and neurological processes

Honeybee is a highly social insect with a reach behavioral repertoire and is a versatile model for neurobiological research. The honeybee gut microbiota is composed of a limited number of bacterial phylotypes that play an important role in host health. However, it remains unclear whether the microbiota can shape brain profiles and behaviors. Here, we revealed that the gut microbiota is requisite for the olfactory learning and memory ability of honeybees and alters the level of neurotransmitters in the brain. Transcriptomic and proteomic analysis showed distinctive gene expression and protein signatures for gnotobiotic bees associated with different gut bacteria. Specifically, genes related to olfactory functions and labor division are most upregulated. Moreover, differentially spliced genes in the brains of colonized bees largely overlapped with the datasets for human autism. The circulating metabolome profiles identified that different gut species regulated specific module of metabolites in the host hemolymph. Most altered metabolites are involved in the amino acid and glycerophospholipid metabolism pathways for the production of neuroactive compounds. Finally, antibiotic treatment disturbed the gut community and the nursing behavior of worker bees under field conditions. The brain transcripts and gut metabolism was also greatly interfered in treated bees. Collectively, we demonstrate that the gut microbiota regulates honeybee behaviors, brain gene transcription, and the circulating metabolism. Our findings highlight the contributions of honeybee gut microbes in the neurological processes with striking parallels to those found in other animals, thus providing a promising model to understand the host-microbe interactions via the gut-brain axis.

Consistent effects of vegetation loss on abundant and rare soil microbial phylotypes across nitrogen-enrichment levels

Soil harbors highly diverse abundant and rare microbial phylotypes that drive multiple soil functions. Given increasing intensity and frequency of vegetation loss and anthropogenic reactive nitrogen (N) inputs to the soil in the future, we lack a mechanistic understanding of how vegetation loss may influence abundant and rare microbial phylotypes at various N-enrichment levels. In the current study, we assessed the effects of vegetation loss on abundant and rare phylotypes of soil bacteria and fungi across three N-enrichment levels in a semi-arid grassland ecosystem. After six years of experimentation in with and without vegetation plots, the vegetation loss increased the total relative abundance of abundant soil bacterial phylotypes but not that of abundant fungal phylotypes at across N-enrichment levels. It is very likely because the number of abundant bacterial phylotypes with positive than negative responses to vegetation loss was higher; however, the number of abundant fungal phylotypes with positive than negative responses to vegetation loss was similar during this period. Moreover, the vegetation loss did not alter the alpha-diversity of abundant or rare bacterial phylotypes, or, of abundant fungal phylotypes; however, it reduced the alpha-diversity of rare fungal phylotypes at across N-enrichment levels. The vegetation loss, however, altered the beta-diversity of abundant and rare bacterial and fungal phylotypes across N-enrichment levels. We found that, against expectations, the effects of vegetation loss on the diversity of abundant and rare phylotypes of both bacteria and fungi were relatively consistent across N-enrichment levels. Our findings provide, for the first time, the phylotype-based data on how vegetation loss affects abundant and rare phylotypes of soil bacteria and fungi across N-enrichment levels. The results also indicate that the effects of vegetation loss on belowground functions may be relatively insensitive to the differences in the N-deposition rates.

Genome reduction in an abundant and ubiquitous soil bacterial lineage

Although bacteria within theVerrucomicrobiaphylum are pervasive in soils around the world, they are underrepresented in both isolate collections and genomic databases. Here we describe a single verrucomicrobial phylotype within the classSpartobacteriathat is not closely related to any previously described taxa. We examined >1000 soils and found this spartobacterial phylotype to be ubiquitous and consistently one of the most abundant soil bacterial phylotypes, particularly in grasslands, where it was typically the most abundant phylotype. We reconstructed a nearly complete genome of this phylotype from a soil metagenome for which we propose the provisional name ‘CandidatusUdaeobacter copiosus’. TheCa. U. copiosus genome is unusually small for soil bacteria, estimated to be only 2.81 Mbp compared to the predicted effective mean genome size of 4.74 Mbp for soil bacteria. Metabolic reconstruction suggests thatCa. U. copiosus is an aerobic chemoorganoheterotroph with numerous amino acid and vitamin auxotrophies. The large population size, relatively small genome and multiple putative auxotrophies characteristic ofCa. U. copiosus suggests that it may be undergoing streamlining selection to minimize cellular architecture, a phenomenon previously thought to be restricted to aquatic bacteria. Although many soil bacteria need relatively large, complex genomes to be successful in soil,Ca. U. copiosus appears to have identified an alternate strategy, sacrificing metabolic versatility for efficiency to become dominant in the soil environment.