Abstract
Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in ...degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.
Different insect groups are host to a broad diversity of gut microbial communities, which vary in complexity, extent of adaptation to the host gut environment, and roles in host ecology and function.
The structure and distribution of genomic diversity in natural microbial communities is largely unexplored. Here, we used shotgun metagenomics to assess the diversity of the honey bee gut microbiota, ...a community consisting of few bacterial phylotypes. Our results show that most phylotypes are composed of sequence-discrete populations, which co-exist in individual bees and show age-specific abundance profiles. In contrast, strains present within these sequence-discrete populations were found to segregate into individual bees. Consequently, despite a conserved phylotype composition, each honey bee harbors a distinct community at the functional level. While ecological differentiation seems to facilitate coexistence at higher taxonomic levels, our findings suggest that, at the level of strains, priority effects during community assembly result in individualized profiles, despite the social lifestyle of the host. Our study underscores the need to move beyond phylotype-level characterizations to understand the function of this community, and illustrates its potential for strain-level analysis.
Gut bacteria engage in various symbiotic interactions with their host and impact gut immunity and homeostasis in different ways. In honey bees, the gut microbiota is composed of a relatively simple, ...but highly specialized bacterial community. One of its members, the gammaproteobacterium Frischella perrara induces the so‐called scab phenotype, a dark‐coloured band that develops on the epithelial surface of the pylorus. To understand the underlying host response, we analysed transcriptome changes in the pylorus in response to bacterial colonization. We find that, in contrast to the gut bacterium Snodgrassella alvi, F. perrara causes strong activation of the host immune system. Besides pattern recognition receptors, antimicrobial peptides and transporter genes, the melanization cascade was upregulated by F. perrara, suggesting that the scab phenotype corresponds to a melanization response of the host. In addition, transcriptome analysis of hive bees with and without the scab phenotype showed that F. perrara also stimulates the immune system under in‐hive conditions in the presence of other gut bacterial species. Collectively, our study demonstrates that the presence of F. perrara influences gut immunity and homeostasis in the pylorus. This may have implications for bee health, because F. perrara prevalence differs between colonies and increased abundance of this bacterium has been shown to correlate with dietary alteration and impaired host development. Our transcriptome analysis sets the groundwork for investigating the interplay of bee gut symbionts with the host immune system.
Animals living in social communities typically harbor a characteristic gut microbiota important for nutrition and pathogen defense. Accordingly, in the gut of the honey bee, Apis mellifera , a ...distinctive microbial community, composed of a taxonomically restricted set of species specific to social bees, has been identified. Despite the ecological and economical importance of honey bees and the increasing concern about population declines, the role of their gut symbionts for colony health and nutrition is unknown. Here, we sequenced the metagenome of the gut microbiota of honey bees. Unexpectedly, we found a remarkable degree of genetic diversity within the few bacterial species colonizing the bee gut. Comparative analysis of gene contents suggests that different species harbor distinct functional capabilities linked to host interaction, biofilm formation, and carbohydrate breakdown. Whereas the former two functions could be critical for pathogen defense and immunity, the latter one might assist nutrient utilization. In a γ-proteobacterial species, we identified genes encoding pectin-degrading enzymes likely involved in the breakdown of pollen walls. Experimental investigation showed that this activity is restricted to a subset of strains of this species providing evidence for niche specialization. Long-standing association of these gut symbionts with their hosts, favored by the eusocial lifestyle of honey bees, might have promoted the genetic and functional diversification of these bee-specific bacteria. Besides revealing insights into mutualistic functions governed by the microbiota of this important pollinator, our findings indicate that the honey bee can serve as a model for understanding more complex gut-associated microbial communities.
Gilliamella apicola and Snodgrassella alvi are dominant members of the honey bee (Apis spp.) and bumble bee (Bombus spp.) gut microbiota. We generated complete genomes of the type strains G. apicola ...wkB1 ᵀ and S. alvi wkB2 ᵀ (isolated from Apis), as well as draft genomes for four other strains from Bombus . G. apicola and S. alvi were found to occupy very different metabolic niches: The former is a saccharolytic fermenter, whereas the latter is an oxidizer of carboxylic acids. Together, they may form a syntrophic network for partitioning of metabolic resources. Both species possessed numerous genes type 6 secretion systems, repeats in toxin (RTX) toxins, RHS proteins, adhesins, and type IV pili that likely mediate cell–cell interactions and gut colonization. Variation in these genes could account for the host fidelity of strains observed in previous phylogenetic studies. Here, we also show the first experimental evidence, to our knowledge, for this specificity in vivo: Strains of S. alvi were able to colonize their native bee host but not bees of another genus. Consistent with specific, long-term host association, comparative genomic analysis revealed a deep divergence and little or no gene flow between Apis and Bombus gut symbionts. However, within a host type (Apis or Bombus), we detected signs of horizontal gene transfer between G. apicola and S. alvi , demonstrating the importance of the broader gut community in shaping the evolution of any one member. Our results show that host specificity is likely driven by multiple factors, including direct host–microbe interactions, microbe–microbe interactions, and social transmission.
•The gut microbiota is emerging as a regulator of neurophysiology and behavior.•Similar processes may govern the gut microbiota — brain axis across mammals and insects.•The honey bee allows ...disentangling microbial effects on behavior in a eusocial animal.
Research on the connections between gut microbes and the neurophysiology and behavior of their animal hosts has grown exponentially in just a few years. Most studies have focused on mammalian models as their relevance to human health is widely established. However, evidence is accumulating that insect behavior may be governed by molecular mechanisms that are partly homologous to those of mammals, and therefore relevant for the understanding of their behavioral dysfunctions. Social insects in particular may provide experimentally amenable models to disentangle the contributions of individual bacterial symbionts to the gut microbiota — brain axis. In this review, we summarize findings from recent research on the neurological and behavioral effects of the gut microbiota of insects and propose an integrated approach to unravel the extended behavioral phenotypes of gut microbes in the honey bee.
Most 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 diverged about 6 mya. Although the host species are colonized largely by the same bacterial 16S rRNA phylotypes, we find that their communities are host specific when analyzed with genomic resolution. Moreover, despite their similar ecology, A. mellifera displayed a much higher diversity of strains and functional gene content in the microbiota compared to A. cerana, both 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 genomic diversity of these key pollinator species. Our results illustrate that the gut microbiota of closely related animal hosts can differ vastly in genomic diversity while displaying similar levels of diversity based on the 16S rRNA gene. Such differences are 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.
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•Metagenomics reveals differences in gut microbiota diversity beyond the 16S rRNA gene•Apis cerana and Apis mellifera harbor distinct species and strains in their gut•Diversity is much higher in A. mellifera per individual bee and within colonies•Major differences in functions are related to polysaccharide degradation
Bacteria have highly flexible gene content; functions of bacterial communities therefore depend on their strain-level composition. Using metagenomics, Ellegaard et al. find major differences in composition and diversity in the gut microbiota of two related honey bees, raising new questions on function and evolution of host-associated bacteria.
Microbial communities in animal guts are composed of diverse, specialized bacterial species, but little is known about how gut bacteria diversify to produce genetically and ecologically distinct ...entities. The gut microbiota of the honey bee, Apis mellifera, presents a useful model, because it consists of a small number of characteristic bacterial species, each showing signs of diversification. Here, we used single-cell genomics to study the variation within two species of the bee gut microbiota: Gilliamella apicola and Snodgrassella alvi. For both species, our analyses revealed extensive variation in intraspecific divergence of protein-coding genes but uniformly high levels of 16S rRNA similarity. In both species, the divergence of 16S rRNA loci appears to have been curtailed by frequent recombination within populations, while other genomic regions have continuously diverged. Furthermore, gene repertoires differ markedly among strains in both species, implying distinct metabolic capabilities. Our results show that, despite minimal divergence at 16S rRNA genes, in situ diversification occurs within gut communities and generates bacterial lineages with distinct ecological niches. Therefore, important dimensions of microbial diversity are not evident from analyses of 16S rRNA, and single cell genomics has potential to elucidate processes of bacterial diversification.
It is presently unclear how much individual community members contribute to the overall metabolic output of a gut microbiota. To address this question, we used the honey bee, which harbors a ...relatively simple and remarkably conserved gut microbiota with striking parallels to the mammalian system and importance for bee health. Using untargeted metabolomics, we profiled metabolic changes in gnotobiotic bees that were colonized with the complete microbiota reconstituted from cultured strains. We then determined the contribution of individual community members in mono-colonized bees and recapitulated our findings using in vitro cultures. Our results show that the honey bee gut microbiota utilizes a wide range of pollen-derived substrates, including flavonoids and outer pollen wall components, suggesting a key role for degradation of recalcitrant secondary plant metabolites and pollen digestion. In turn, multiple species were responsible for the accumulation of organic acids and aromatic compound degradation intermediates. Moreover, a specific gut symbiont, Bifidobacterium asteroides, stimulated the production of host hormones known to impact bee development. While we found evidence for cross-feeding interactions, approximately 80% of the identified metabolic changes were also observed in mono-colonized bees, with Lactobacilli being responsible for the largest share of the metabolic output. These results show that, despite prolonged evolutionary associations, honey bee gut bacteria can independently establish and metabolize a wide range of compounds in the gut. Our study reveals diverse bacterial functions that are likely to contribute to bee health and provide fundamental insights into how metabolic activities are partitioned within gut communities.
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