Waldan K. Kwong, Bee Microbes
Much of my recent research is on the gut microbiota of bees. This page is a brief introduction to the system, which is currently in the very early stages of development. This field of research is growing and changing rapidly, thus I recommend referring to the primary literature for a more nuanced and up-to-date discussion of the topic.

What bees do you study?

My main focus is a group of bees known as the corbiculates. These include the highly social honey bees, stingless bees, and bumble bees. They comprise ~1000 of the >20,000 bee species (mostly solitary) in the world. The corbiculates have long fascinated humanity due to their ubiquity, agricultural importance, and eusocial behaviour. Now it becoming apparent that they also possess a uniquely specialized microbiota.

What is the bee microbiota?

The microbiota is defined as all the microbial associates of an organism, which may include microscopic bacteria, fungi, protists, archaea, and viruses. In the case of bees, the microbiota consists of various pathogens, transient microorganisms picked up from flowers, and symbiotic bacteria that reside in the gut. The gut bacteria are particularly interesting, as they appear to comprise a stable set of members in adult worker bees and are incredibly numerous (with up to 1 billion cells per bee). In honey bees and bumble bees sampled world-wide, the same community of gut symbionts are found. This suggests that certain ecological and evolutionary forces are working to maintain a unique consortium of resident bacteria in these bees.

I, my colleagues, and researchers at several other labs have recently worked to identify and characterize the members of the corbiculate gut microbiota. The first systematic, community-level descriptions of the bee gut microbiota came through culture-independent studies. Although too numerous to comprehensively list, key early examples include: Jeyaprakash et al. 2003, Babendreier et al. 2007, Cox-Foster et al. 2007, Martinson et al. 2011, Koch & Schmid-Hempel 2011, and Moran et al. 2012. Subsequent efforts have focused on culturing, sequencing, and describing the individual members of this bacterial community. The following table is a ‘who’s who’ of the core bee gut microbiota, updated as of March 2015.

Bee gut microbes

 
Bee larvae begin their lives devoid of bacteria. Through feeding and interactions with workers, they may pick up some microbes, but these are again lost as the gut lining is shed during metamorphosis to adults. As new adults emerge from pupation, they are germ-free; bees at this stage are ideal for use in gnotobiotic experiments. Contact with older workers and hive material enables full establishment of the normal microbiota after 4-6 days. For more on how microbes colonize the bee gut, see Martinson et al. 2012, Vojvodic et al. 2013, Powell et al. 2014, and Tarpy et al. 2015.

localization2

In the gut, bacteria are not simply haphazardly mixed together. Akin to most communities of organisms, a distinct spatial structuring prevails, likely indicative of the different niches each symbiont species has carved out for itself. Snodgrassella adheres closely to the gut wall, while Gilliamella is typically found as a second layer above Snodgrassella. Both these species are abundant in the ileum, a highly folded region of the gut. Lactobacillus species dominate the distal hindgut (rectum), a store for waste and digested pollen particles. Parasaccharibacter appears to thrive in the hypopharyngeal glands, the source of royal jelly, which is toxic to most bacteria.

 
 
 
How are the bee gut microbiota beneficial?Engel2012v3

The normal gut microbiota protects against Crithidia, an intestinal parasite, in bumble bees (Koch & Schmid-Hempel 2011 &2012). Fermentative species such as Gilliamella and Bifidobaterium are capable of breaking down carbohydrates such as mannose and pectin, which would aid in the digestion of pollen (reviewed in Kwong et al. 2016). These fermentation products are absorbed by the bee intestine, and bees with the normal gut microbiota gain weight faster than germ-free bees (Zheng et al. 2017). The bee gut microbiota also triggers expression of the bee immune system, which may be important in “priming” host defenses against pathogens (Kwong et al. 2017). In humans, the gut microbiota is well known to perform many beneficial functions, including nutrient provisioning, immune system modulation, and developmental regulation. The microbiota of bees is still poorly studied, hence many aspects of their host-microbe relationship, including beneficial interactions, remain to be revealed.

What are the advantages of the bee gut system?

The bee gut is an attractive model system for the study of co-evolved microbial communities. Many animals possess gut microbiotas, but they can be difficult to study in detail; for example, the human gut community consists of >500 species. In contrast, the bee gut has only 8 or so major groups of bacteria. In addition to being of a manageable number, the bee gut symbionts are also all cultivable in-vitro. This allows for the development of genetic tools for manipulating individual bacterial strains and testing them in gnotobiotic bees.

Bees are of tremendous ecological and economic importance due to their pollination services and products (e.g. honey, wax, propolis). Hence, there are potential applied benefits for bee microbiome research. Bees have also been domesticated and studied for centuries, and there is a large body of existing knowledge on the genetics, behaviour, and natural history of these insects; to have such resources is a rarity and a great advantage for a new microbial model system.

What are the big questions?
conceptsummary
Symbiotic relationships are everywhere in nature, and that of animals and their associated microbes are among the most common. Yet, it is unclear how these relationships arise and persist through millions of years of evolution. A major goal in the field of microbiota research is to identify factors that enable symbioses. For example, what adaptations permit a bacterium’s lifestyle change from free-living to host-associated? How does the host accommodate for the presence of the symbionts?

What is the role of sociality in maintaining symbioses? Studies of gut microbial communities in several animal lineages have shown heritability: microbes can be passed down the generations from parent to offspring. This means gut microbes are not randomly shared among different animal species, but instead are closely tied to the host from which it came. Although this finding may seem sensible from a human perspective, for we raise young from birth and live in large social groups, many organisms lack this transgenerational contact. Instead, they may rely on other means to pass along beneficial microbes, or may lack a stable microbiota altogether. The latter appears to be the case for solitary bees; thus, can the stable microbiota found in the coribculates be ascribed to their social nature?

Microbes that are stably transmitted from one generation to another enhances allopatry, which may result in co-evolution, host specialization, and co-speciation. These processes are critical for explaining biological diversity and how new species arise and evolve. The symbionts of the bee gut may prove a valuable model: their association with bees likely began >80 million years ago, at the origin of the corbiculates, and strains from different hosts can have extremely divergent genomic sequences. In the question of how bacteria diverge and speciate, the bee gut system gives insight into the effects of host background on bacterial dispersal, gene flow, adaptation, and specialization.

Finally, it should not be forgotten that a particular gut bacterium does not live alone, but in a community of millions to trillions. This complexity gives rise to many dynamic interactions that are only beginning to be studied. How do bacteria colonize, grow, cooperate, and compete in the gut environment? sociality3What gives rise to spatial patterning? How do gut communities deal with perturbation or foreign invaders? What kinds of intra-community interactions contribute to community stability? Community dynamics have long been studied by ecologists, but can the principles of the macroscopic world also be applied to microorganisms?

The bee system has parallels with mammalian gut communities in being host-adapted and socially transmitted, and is thus a good general model for the evolution of host-associated microbiotas. How animal-microbe relationships develop and maintain specificity to each other is not only a question of scientific curiosity, but one of great general interest given the widespread symbiotic associations found in organisms of health, economic, and environmental consequence.


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