Abstract
Lactic acid bacteria (LAB) are well recognized beneficial host-associated members of the microbiota of humans and animals. Yet LAB-associations of invertebrates have been poorly characterized and their functions remain obscure. Here we show that honeybees possess an abundant, diverse and ancient LAB microbiota in their honey crop with beneficial effects for bee health, defending them against microbial threats. Our studies of LAB in all extant honeybee species plus related apid bees reveal one of the largest collections of novel species from the genera Lactobacillus and Bifidobacterium ever discovered within a single insect and suggest a long (>80 mya) history of association. Bee associated microbiotas highlight Lactobacillus kunkeei as the dominant LAB member. Those showing potent antimicrobial properties are acquired by callow honey bee workers from nestmates and maintained within the crop in biofilms, though beekeeping management practices can negatively impact this microbiota. Prophylactic practices that enhance LAB, or supplementary feeding of LAB, may serve in integrated approaches to sustainable pollinator service provision. We anticipate this microbiota will become central to studies on honeybee health, including colony collapse disorder, and act as an exemplar case of insect-microbe symbiosis.
Highlights
Symbiosis is common in nature, in which symbionts as commensals or mutualists evolved to benefit each other
Lactic acid bacteria (LAB) diversity All 9 Apis and the 3 Meliponini species studied possess a similar microbiota, comprising together approximately 50 novel LAB species in the genera Lactobacillus and Bifidobacterium (Figure 1), using the threshold used to define a bacterial species based on rRNA gene sequencing of,97% similarity [25] (,98.5% is often found to imply possibly novel species)
Many Lactobacillus and Bifidobacterium were found to be common across bee species (Figure 1), including L. kunkeei in stingless bees from Central America (M. beecheii) and Africa (M. bocandei), though not in Trigona sp. from Borneo and Thailand, where it is sympatric with five native Apis species
Summary
Symbiosis is common in nature, in which symbionts as commensals or mutualists evolved to benefit each other. Cultureindependent studies of the human microbiota identified recently a complex symbiotic environment with more than 1,000 bacterial phylotypes representing more than 7,000 strains [1]. The composition of this microbiota has been suggested to be a result of a highly coevolved symbiosis and commensalism influenced by nutrition, physiology and immunological factors [2,3]. Ryu and colleagues [5] established the importance of the normal flora in the fruit fly gut in order to sustain health This small microbiota was sufficient to suppress growth of pathogens. Studies have shown that symbiosis between social insects and microbial species are often highly coevolved [7] and that these symbionts are evolutionary shaped distinctly from the forces acting upon symbionts of solitary organisms, which normally lack a homeostatic fortress environment [8]
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