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. 2019 Dec 17;116(51):25909-25916.
doi: 10.1073/pnas.1916224116. Epub 2019 Nov 27.

Division of labor in honey bee gut microbiota for plant polysaccharide digestion

Hao Zheng  1   2 , Julie Perreau  2 , J Elijah Powell  2 , Benfeng Han  3 , Zijing Zhang  3 , Waldan K Kwong  2 , Susannah G Tringe  4 , Nancy A Moran  5
Affiliations

Division of labor in honey bee gut microbiota for plant polysaccharide digestion

Hao Zheng et al. Proc Natl Acad Sci U S A. .

Abstract

Bees acquire carbohydrates from nectar and lipids; and amino acids from pollen, which also contains polysaccharides including cellulose, hemicellulose, and pectin. These potential energy sources could be degraded and fermented through microbial enzymatic activity, resulting in short chain fatty acids available to hosts. However, the contributions of individual microbiota members to polysaccharide digestion have remained unclear. Through analysis of bacterial isolate genomes and a metagenome of the honey bee gut microbiota, we identify that Bifidobacterium and Gilliamella are the principal degraders of hemicellulose and pectin. Both Bifidobacterium and Gilliamella show extensive strain-level diversity in gene repertoires linked to polysaccharide digestion. Strains from honey bees possess more such genes than strains from bumble bees. In Bifidobacterium, genes encoding carbohydrate-active enzymes are colocated within loci devoted to polysaccharide utilization, as in Bacteroides from the human gut. Carbohydrate-active enzyme-encoding gene expressions are up-regulated in response to particular hemicelluloses both in vitro and in vivo. Metabolomic analyses document that bees experimentally colonized by different strains generate distinctive gut metabolomic profiles, with enrichment for specific monosaccharides, corresponding to predictions from genomic data. The other 3 core gut species clusters (Snodgrassella and 2 Lactobacillus clusters) possess few or no genes for polysaccharide digestion. Together, these findings indicate that strain composition within individual hosts determines the metabolic capabilities and potentially affects host nutrition. Furthermore, the niche specialization revealed by our study may promote overall community stability in the gut microbiomes of bees.

Keywords: amino acid; gut microbiota; honey bee; polysaccharide; symbiosis.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
(A) The average relative abundance of GH and PL families in the genomes of Bifidobacterium, Gilliamella, and Lactobacillus from bee guts. Gilliamella genomes from A. mellifera, Apis cerana, and Bombus species are shown separately. A full list of the distribution of all GH/PL families in all analyzed genomes is given in Dataset S2. The numbers of genomes analyzed for each species are indicated in parentheses. The circle size indicates the average gene numbers of the GH/PL family per genome. The circle color represents the relative variability in number of GH/PL across genomes, calculated as the coefficient of variation (ratio of SD to the mean). (B) Relative abundances of bacterial groups in the gut microbiota of A. mellifera based on the best BLASTP hit distribution of 614,276 CDSs from the metagenomic data. Names in parentheses indicate likely bee gut taxa from which the CDSs derive. (C) Distributions of select GHs across different bacterial genera based on metagenomic data.
Fig. 2.
Fig. 2.
Phylogenetic tree of Bifidobacterium strains using the maximum-likelihood algorithm based on the concatenation of 101 core protein sequences (29,909 amino acid positions). Bootstrap values are indicated on nodes, and strains from Apis or Bombus are indicated by branch color. Strains of Bifidobacterium coryneforme and 3 clusters of Bifidobacterium asteroides are indicated by gray shading. A full tree is shown in SI Appendix, Fig. S1. The heatmap shows the numbers of genes belonging to GH43 subfamilies in each strain. The total numbers of GH43 genes are shown by bar plots.
Fig. 3.
Fig. 3.
Genomic organization, expression, and function of genes involved in digestion of polysaccharides. (A) Syntenic loci of GHs, transporter genes, and transcriptional regulators in B. asteroides and Bifidobacterium bohemicum strains. Homologous genes are connected by gray bars, and the GH family number is shown for respective genes. (B) Gene expression profiles of GHs in response to different hemicellulose substrates. Error bars represent SDs of 3 biological replicates. (C) Results of partial least squares discriminant analysis based on 687 metabolites detected from guts of W8111-colonized or W8103-colonized bees fed on sucrose supplemented with arabinan, galactan, or xyloglucan. Six biological replicates for each treatment. (D–F) Volcano plots of differentially abundant metabolites identified in guts of monoassociated bees fed on different polysaccharides.
Fig. 4.
Fig. 4.
(A) Phylogenetic tree of Gilliamella isolates using the maximum-likelihood algorithm based on the concatenation of 106 core protein sequences (32,259 amino acid positions). A full phylogenetic tree is shown in SI Appendix, Fig. S6. The presence/absence of the loci containing genes for PLs and CE12 and the gene for GH31 gene are indicated by open/closed boxes. (B) In vivo gene expression profiles of genes of G. apicola W8127 in response to pollen and polygalacturonic acid (PG) fed to the monoinoculated bees relative to controls (sucrose syrup). Error bars represent SDs of 3 biological replicates. (C) Gut concentrations of galacturonic acid of monoassociated and microbiota-free (MF) bees fed on polygalacturonic acid (n = 5 to 6). Tested by Mann–Whitney u test.
Fig. 5.
Fig. 5.
(A) Presence and absence of genes underlying amino acid synthesis in the genomes of 231 bacterial isolates from bee guts. Colored boxes indicate the presence of all genes required for a pathway, and white boxes indicate the absence of genes for a pathway. (B) The TCA cycle with the ASCT pathway and the methionine synthesis pathway found in Snodgrassella strains and Bartonella strains, which incorporates acetyl-CoA and acetate rather than succinyl-CoA.
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