The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host

ABSTRACT The microbiota of Drosophila melanogaster has a substantial impact on host physiology and nutrition. Some effects may involve vitamin provisioning, but the relationships between microbe-derived vitamins, diet, and host health remain to be established systematically. We explored the contribu...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	David R. Sannino, Adam J. Dobson, Katie Edwards, Esther R. Angert, Nicolas Buchon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Acetobacter Drosophila gut microbiota synthetic diet thiamine vitamin B1 Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/36a2f016281848d09d2e8faa86a1c188
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:36a2f016281848d09d2e8faa86a1c188
record_format	dspace
spelling	oai:doaj.org-article:36a2f016281848d09d2e8faa86a1c1882021-11-15T15:53:27ZThe <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host10.1128/mBio.00155-182150-7511https://doaj.org/article/36a2f016281848d09d2e8faa86a1c1882018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00155-18https://doaj.org/toc/2150-7511ABSTRACT The microbiota of Drosophila melanogaster has a substantial impact on host physiology and nutrition. Some effects may involve vitamin provisioning, but the relationships between microbe-derived vitamins, diet, and host health remain to be established systematically. We explored the contribution of microbiota in supplying sufficient dietary thiamine (vitamin B1) to support D. melanogaster at different stages of its life cycle. Using chemically defined diets with different levels of available thiamine, we found that the interaction of thiamine concentration and microbiota did not affect the longevity of adult D. melanogaster. Likewise, this interplay did not have an impact on egg production. However, we determined that thiamine availability has a large impact on offspring development, as axenic offspring were unable to develop on a thiamine-free diet. Offspring survived on the diet only when the microbiota was present or added back, demonstrating that the microbiota was able to provide enough thiamine to support host development. Through gnotobiotic studies, we determined that Acetobacter pomorum, a common member of the microbiota, was able to rescue development of larvae raised on the no-thiamine diet. Further, it was the only microbiota member that produced measurable amounts of thiamine when grown on the thiamine-free fly medium. Its close relative Acetobacter pasteurianus also rescued larvae; however, a thiamine auxotrophic mutant strain was unable to support larval growth and development. The results demonstrate that the D. melanogaster microbiota functions to provision thiamine to its host in a low-thiamine environment. IMPORTANCE There has been a long-standing assumption that the microbiota of animals provides their hosts with essential B vitamins; however, there is not a wealth of empirical evidence supporting this idea, especially for vitamin B1 (thiamine). To determine whether this assumption is true, we used Drosophila melanogaster and chemically defined diets with different thiamine concentrations as a model. We found that the microbiota does provide thiamine to its host, enough to allow the development of flies on a thiamine-free diet. The power of the Drosophila-microbiota system allowed us to determine that one microbiota member in particular, Acetobacter pomorum, is responsible for the thiamine provisioning. Thereby, our study verifies this long-standing hypothesis. Finally, the methods used in this work are applicable for interrogating the underpinnings of other aspects of the tripartite interaction between diet, host, and microbiota.David R. SanninoAdam J. DobsonKatie EdwardsEsther R. AngertNicolas BuchonAmerican Society for MicrobiologyarticleAcetobacterDrosophilagut microbiotasynthetic dietthiaminevitamin B1MicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Acetobacter Drosophila gut microbiota synthetic diet thiamine vitamin B1 Microbiology QR1-502
spellingShingle	Acetobacter Drosophila gut microbiota synthetic diet thiamine vitamin B1 Microbiology QR1-502 David R. Sannino Adam J. Dobson Katie Edwards Esther R. Angert Nicolas Buchon The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
description	ABSTRACT The microbiota of Drosophila melanogaster has a substantial impact on host physiology and nutrition. Some effects may involve vitamin provisioning, but the relationships between microbe-derived vitamins, diet, and host health remain to be established systematically. We explored the contribution of microbiota in supplying sufficient dietary thiamine (vitamin B1) to support D. melanogaster at different stages of its life cycle. Using chemically defined diets with different levels of available thiamine, we found that the interaction of thiamine concentration and microbiota did not affect the longevity of adult D. melanogaster. Likewise, this interplay did not have an impact on egg production. However, we determined that thiamine availability has a large impact on offspring development, as axenic offspring were unable to develop on a thiamine-free diet. Offspring survived on the diet only when the microbiota was present or added back, demonstrating that the microbiota was able to provide enough thiamine to support host development. Through gnotobiotic studies, we determined that Acetobacter pomorum, a common member of the microbiota, was able to rescue development of larvae raised on the no-thiamine diet. Further, it was the only microbiota member that produced measurable amounts of thiamine when grown on the thiamine-free fly medium. Its close relative Acetobacter pasteurianus also rescued larvae; however, a thiamine auxotrophic mutant strain was unable to support larval growth and development. The results demonstrate that the D. melanogaster microbiota functions to provision thiamine to its host in a low-thiamine environment. IMPORTANCE There has been a long-standing assumption that the microbiota of animals provides their hosts with essential B vitamins; however, there is not a wealth of empirical evidence supporting this idea, especially for vitamin B1 (thiamine). To determine whether this assumption is true, we used Drosophila melanogaster and chemically defined diets with different thiamine concentrations as a model. We found that the microbiota does provide thiamine to its host, enough to allow the development of flies on a thiamine-free diet. The power of the Drosophila-microbiota system allowed us to determine that one microbiota member in particular, Acetobacter pomorum, is responsible for the thiamine provisioning. Thereby, our study verifies this long-standing hypothesis. Finally, the methods used in this work are applicable for interrogating the underpinnings of other aspects of the tripartite interaction between diet, host, and microbiota.
format	article
author	David R. Sannino Adam J. Dobson Katie Edwards Esther R. Angert Nicolas Buchon
author_facet	David R. Sannino Adam J. Dobson Katie Edwards Esther R. Angert Nicolas Buchon
author_sort	David R. Sannino
title	The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
title_short	The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
title_full	The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
title_fullStr	The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
title_full_unstemmed	The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host
title_sort	<italic toggle="yes">drosophila melanogaster</italic> gut microbiota provisions thiamine to its host
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/36a2f016281848d09d2e8faa86a1c188
work_keys_str_mv	AT davidrsannino theitalictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT adamjdobson theitalictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT katieedwards theitalictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT estherrangert theitalictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT nicolasbuchon theitalictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT davidrsannino italictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT adamjdobson italictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT katieedwards italictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT estherrangert italictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost AT nicolasbuchon italictoggleyesdrosophilamelanogasteritalicgutmicrobiotaprovisionsthiaminetoitshost
_version_	1718427266935947264

The <italic toggle="yes">Drosophila melanogaster</italic> Gut Microbiota Provisions Thiamine to Its Host

Ejemplares similares