Host-derived organic acids enable gut colonization of the honey bee symbiont Snodgrassella alvi

• Published in: Nature microbiology Vol. 9; no. 2; pp. 477 - 489
• Main Authors: Quinn, Andrew, El Chazli, Yassine, Escrig, Stéphane, Daraspe, Jean, Neuschwander, Nicolas, McNally, Aoife, Genoud, Christel, Meibom, Anders, Engel, Philipp
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.02.2024; Nature Publishing Group
• Subjects: 101/28; 101/58; 45/77; 631/326/2565/2134; 631/326/2565/547; 631/326/41/547; 64; 96/63; Animals; Apis mellifera; Bacteria; Bees; Biomedical and Life Sciences; Colonization; Gastrointestinal Microbiome; Gastrointestinal Tract - microbiology; Infectious Diseases; Intestinal microflora; Life Sciences; Mass spectroscopy; Medical Microbiology; Metabolism; Metabolites; Metabolomics; Microbiology; Microbiota; Neisseriaceae; Niches; Nutrients; Organic acids; Parasitology; Snodgrassella alvi; Symbiosis; Tryptophan; Virology
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-023-01572-y

Diverse bacteria can colonize the animal gut using dietary nutrients or by engaging in microbial crossfeeding interactions. Less is known about the role of host-derived nutrients in enabling gut bacterial colonization. Here we examined metabolic interactions within the evolutionary ancient symbiosis between the honey bee ( Apis mellifera ) and the core gut microbiota member Snodgrassella alvi . This betaproteobacterium is incapable of metabolizing saccharides, yet colonizes the honey bee gut in the presence of a sugar-only diet. Using comparative metabolomics, 13 C-tracers and nanoscale secondary ion mass spectrometry (NanoSIMS), we show in vivo that S. alvi grows on host-derived organic acids, including citrate, glycerate and 3-hydroxy-3-methylglutarate, which are actively secreted by the host into the gut lumen. S. alvi also modulates tryptophan metabolism in the gut by converting kynurenine to anthranilate. These results suggest that S. alvi is adapted to a specific metabolic niche in the honey bee gut that depends on host-derived nutritional resources. Comparative metabolomics and NanoSIMs reveal that the honey bee symbiont Snodgrassella alvi uses host-derived metabolites to colonize the gut, indicating adaptation to a specific metabolic niche in its host.