Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola

Abstract

Social bees collect carbohydrate-rich food to support their colonies, and yet, certain carbohydrates present in their diet or produced through the breakdown of pollen are toxic to bees. The gut microbiota of social bees is dominated by a few core bacterial species, including the Gram-negative species Gilliamella apicola. We isolated 42 strains of G. apicola from guts of honey bees and bumble bees and sequenced their genomes. All of the G. apicola strains share high 16S rRNA gene similarity, but they vary extensively in gene repertoires related to carbohydrate metabolism. Predicted abilities to utilize different sugars were verified experimentally. Some strains can utilize mannose, arabinose, xylose, or rhamnose (monosaccharides that can cause toxicity in bees) as their sole carbon and energy source. All of the G. apicola strains possess a manO-associated mannose family phosphotransferase system; phylogenetic analyses suggest that this was acquired from Firmicutes through horizontal gene transfer. The metabolism of mannose is specifically dependent on the presence of mannose-6-phosphate isomerase (MPI). Neither growth rates nor the utilization of glucose and fructose are affected in the presence of mannose when the gene encoding MPI is absent from the genome, suggesting that mannose is not taken up by G. apicola strains which harbor the phosphotransferase system but do not encode the MPI. Given their ability to simultaneously utilize glucose, fructose, and mannose, as well as the ability of many strains to break down other potentially toxic carbohydrates, G. apicola bacteria may have key roles in improving dietary tolerances and maintaining the health of their bee hosts.

Dynamic microbiome evolution in social bees

“…For example, the transition to sociality in the wood roaches/termites enabled the development of a nutritionally specialized gut microbiota and a shift from an omnivorous to a wood-based diet ( 7 , 66 , 67 ). The corbiculate bee microbiota also appears to be metabolically optimized toward its host’s diet, with symbiont lineages such as Gilliamella , Lactobacillus , and Bifidobacterium able to enzymatically break down and ferment the sugars found in pollen, honey, and nectar ( 37 , 39 , 43 , 68 , 69 ). Other gut bacteria have specialized to particular physical locations, including Snodgrassella , which occupies the gut wall of the ileum ( 70 ); Frischella , which colonizes a small section of the pylorus ( 71 ); and Parasaccharibacter , which is found in relative abundance in larval food and worker hypopharyngeal glands ( 72 ).…”

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

“…Extensive strain diversity of A. mellifera core gut bacteria, corresponding to different gene repertoires and metabolic capabilities, has been shown for G. apicola [8 • ], and for the two Lactobacillus clades and Bifidobacterium [9]. Accessory genes (genes present in some strains but not others within a species) include many involved in carbohydrate utilization, as well as genes encoding toxins likely targeted to competing bacteria.…”

“…Accessory genes (genes present in some strains but not others within a species) include many involved in carbohydrate utilization, as well as genes encoding toxins likely targeted to competing bacteria. Strain level variation is even greater when comparing strains present in Apis versus Bombus , the latter having far fewer genes for using diverse carbohydrates [8 • ,10]. …”

“…The gut microbiome has major effects on the profile of short chain fatty acids in the gut and in the hemolymph; for example, butyrate dominates in conventional bees but is entirely absent in microbiota-free bees [15 •• ]. Genomic studies reveal that some core gut bacteria harbor many genes for carbohydrate metabolism [8 • ,10,38], and different strain compositions possess different abilities to metabolize carbohydrates [8 • ,9,39 •• ]. …”

Genetic Engineering of Bee Gut Microbiome Bacteria with a Toolkit for Modular Assembly of Broad-Host-Range Plasmids

“…22,26,28,29 Major members of the core BGM — Snodgrassella alvi , Gilliamella apicola , and Bartonella apis — have been the subject of detailed genomic analyses. 30–32 But aside from random transposon mutagenesis in S. alvi , 33 no genetic tools have been reported for these species.…”