Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>

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-negati...

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Autores principales:	Hao Zheng, Alex Nishida, Waldan K. Kwong, Hauke Koch, Philipp Engel, Margaret I. Steele, Nancy A. Moran
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/95ab0336c4494264945519e8ae167979
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spelling	oai:doaj.org-article:95ab0336c4494264945519e8ae1679792021-11-15T15:50:16ZMetabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>10.1128/mBio.01326-162150-7511https://doaj.org/article/95ab0336c4494264945519e8ae1679792016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01326-16https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Bees are important pollinators of agricultural plants. Our study documents the ability of Gilliamella apicola, a dominant gut bacterium in honey bees and bumble bees, to utilize several sugars that are harmful to bee hosts. Using genome sequencing and growth assays, we found that the ability to metabolize certain toxic carbohydrates is directly correlated with the presence of their respective degradation pathways, indicating that metabolic potential can be accurately predicted from genomic data in these gut symbionts. Strains vary considerably in their range of utilizable carbohydrates, which likely reflects historical horizontal gene transfer and gene deletion events. Unlike their bee hosts, G. apicola bacteria are not detrimentally affected by growth on mannose-containing medium, even in strains that cannot metabolize this sugar. These results suggest that G. apicola may be an important player in modulating nutrition in the bee gut, with ultimate effects on host health.Hao ZhengAlex NishidaWaldan K. KwongHauke KochPhilipp EngelMargaret I. SteeleNancy A. MoranAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Hao Zheng Alex Nishida Waldan K. Kwong Hauke Koch Philipp Engel Margaret I. Steele Nancy A. Moran Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
description	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. IMPORTANCE Bees are important pollinators of agricultural plants. Our study documents the ability of Gilliamella apicola, a dominant gut bacterium in honey bees and bumble bees, to utilize several sugars that are harmful to bee hosts. Using genome sequencing and growth assays, we found that the ability to metabolize certain toxic carbohydrates is directly correlated with the presence of their respective degradation pathways, indicating that metabolic potential can be accurately predicted from genomic data in these gut symbionts. Strains vary considerably in their range of utilizable carbohydrates, which likely reflects historical horizontal gene transfer and gene deletion events. Unlike their bee hosts, G. apicola bacteria are not detrimentally affected by growth on mannose-containing medium, even in strains that cannot metabolize this sugar. These results suggest that G. apicola may be an important player in modulating nutrition in the bee gut, with ultimate effects on host health.
format	article
author	Hao Zheng Alex Nishida Waldan K. Kwong Hauke Koch Philipp Engel Margaret I. Steele Nancy A. Moran
author_facet	Hao Zheng Alex Nishida Waldan K. Kwong Hauke Koch Philipp Engel Margaret I. Steele Nancy A. Moran
author_sort	Hao Zheng
title	Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
title_short	Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
title_full	Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
title_fullStr	Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
title_full_unstemmed	Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>
title_sort	metabolism of toxic sugars by strains of the bee gut symbiont <named-content content-type="genus-species">gilliamella apicola</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/95ab0336c4494264945519e8ae167979
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Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont <named-content content-type="genus-species">Gilliamella apicola</named-content>

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