Specificity between Lactobacilli and Hymenopteran Hosts Is the Exception Rather than the Rule

Abstract

c Lactobacilli (Lactobacillales: Lactobacillaceae) are well known for their roles in food fermentation, as probiotics, and in human health, but they can also be dominant members of the microbiota of some species of Hymenoptera (ants, bees, and wasps). Honey bees and bumble bees associate with host-specific lactobacilli, and some evidence suggests that these lactobacilli are important for bee health. Social transmission helps maintain associations between these bees and their respective microbiota. To determine whether lactobacilli associated with social hymenopteran hosts are generally host specific, we gathered publicly available Lactobacillus 16S rRNA gene sequences, along with Lactobacillus sequences from 454 pyrosequencing surveys of six other hymenopteran species (three sweat bees and three ants). We determined the comparative secondary structural models of 16S rRNA, which allowed us to accurately align the entire 16S rRNA gene, including fast-evolving regions. BLAST searches and maximum-likelihood phylogenetic reconstructions confirmed that honey and bumble bees have host-specific Lactobacillus associates. Regardless of colony size or within-colony oral sharing of food (trophallaxis), sweat bees and ants associate with lactobacilli that are closely related to those found in vertebrate hosts or in diverse environments. Why honey and bumble bees associate with host-specific lactobacilli while other social Hymenoptera do not remains an open question. Lactobacilli are known to inhibit the growth of other microbes and can be beneficial whether they are coevolved with their host or are recruited by the host from environmental sources through mechanisms of partner choice.

Routes of Acquisition of the Gut Microbiota of the Honey Bee Apis mellifera

“…Thus, Firm-5 can be routinely transmitted by contact with hive materials. This observation is consistent with previous studies in which lactobacilli (including Firm-5 isolates) were recovered from hive components (39)(40)(41). Workers exposed only to oral trophallaxis contained scarce gut communities similar to those of unexposed bees, whereas those bees exposed to frame material alone had the largest communities (Fig.…”

Interactions between Cooccurring Lactic Acid Bacteria in Honey Bee Hives

“…A large number of diverse lactic acid bacteria are found associated with insects, including bees, and have been suggested to provide health benefits in various contexts (8,(25)(26)(27). Bacteria that comprise the lactic acid bacteria are not a phylogenetically cohesive designation, based on 16S rRNA evolution, but instead are grouped based on common metabolic characteristics, including the production of lactic acid through fermentative metabolism.…”

Evolution of host specialization in gut microbes: the bee gut as a model

“…9,10 Phylogenetic analyses indicate that they each comprise monophyletic clades of bee-associated bacteria, which is suggestive of an intimate symbiosis persisting over evolutionary time scales. 4,[11][12][13][14] The simplicity of the bee gut community, and its analogy to more complex mammalian models, offer a unique opportunity to study gut microbiomes from the perspective of microbial evolution and ecology in an experimentally tractable system. Specialized microbial symbionts often exhibit host range restriction and codiversification with host lineages.…”

“…11,12,18 However, specialization to particular host lineages remains mostly untested by transplantation experiments, and 16S rRNA lacks sufficient resolution to reconstruct detailed phylogenetic histories of these bacteria at the strain level. New approaches leveraging the power of high-throughput genomics may help unravel the processes behind the evolution of specialization: shotgun metagenomics and metatranscriptomics enable functional profiling of whole communities, 5,25 16S rRNA gene surveys allows broad assessment of community composition at the genus level, 10 and an increasing number of sequenced strains and single cells 7,[26][27][28][29][30][31] permit analysis of diversity at the individual bacterium level.…”

“…80 Mya 60 ), and are presently all found in Apis and Bombus bees. 4,12,14,18 Stingless bees (Meliponini) appear to have lost Gilliamella and Snodgrassella, 18,61 but retain Lactobacillus and Bifidobacterium.…”