Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera)

Abstract

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.

The role of the gut microbiome in health and disease of adult honey bee workers

“…If bees are manually removed from the comb at an early pupal stage (before the mouthparts harden) using sterile methods, guts of emerging adults will contain few or no bacteria and lack all core species, enabling experiments in which the gut community is inoculated in a controlled manner (e.g. [10,11 •• ,14 •• ,15 •• ,16 • ]). Experiments comparing microbiotia-free and inoculated bees have revealed some of the functions of the gut microbiome and its members (Table 1).…”

“…For example, Frischella perrara , a relative of G. apicola within the family Orbaceae, is widespread [18]. It colonizes in a distinctive manner in the pylorus region near the junction of the midgut and the hindgut; experiments involving inoculations of microbiota-free bees show that it causes a characteristic brown ‘scab’ [16 • ], which has been shown to result from stimulation of immune pathways including the melanization response [14 •• ]. This species also causes disordered cell division in gut epithelial cells and produces a complex polyketide molecule that affects cellular replication in human cell lines [19].…”

“…Indeed, poor nutrition has been shown to disrupt the normal gut microbiome, resulting in higher mortality and disease susceptibility [28 • ]. Disruption of the microbiome (dysbiosis) has many consequences for worker development: such disruption during early adult life affects expression of important developmental genes, including vitellogenin [29 • ] and is expected to affect immune system function, since the honey bee microbiome stimulates immune pathways [14 •• ,29 • ,30 • ]. In turn, honey bee innate immune function has been shown to be compromised by stimulation of cellular stress responses [31 • ].…”

“…Bees possessing the entire gut community and, to a smaller extent, bees mono-inoculated with S. alvi or with G. apicola cleared more bacteria from the hemolymph after E. coli injection, and contained more antimicrobial peptide than did microbiome-free bees, suggesting immune priming by these core gut community members [30 • ]. Immune priming has also been shown for F. perrara , which colonizes locally in the ileum region of the hindgut and stimulates a dramatic increase in production of the antimicrobial peptide apidaecin [14 •• ]. Although our focus is on adult workers, some studies have also examined potential interactions of gut microbiomes with larval pathogens.…”

Dietary specialization in mutualistic acacia‐ants affects relative abundance but not identity of host‐associated bacteria

“…We were also able to assemble the genome of a Frischella-related taxon present in Pseudomyrmex, but this species is present in a small number of individuals so is unlikely to play a substantial role in Pseudomyrmex biology. The best known Frischella species, F. perrara, appears to incur an immune cost to its honeybee hosts without providing any known benefit (Emery, Schmidt, & Engel, 2017;Engel, Bartlett, & Moran, 2015).…”