The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species

ABSTRACT For mammals, oxalate enters the body through the diet or is endogenously produced by the liver; it is removed by microbial oxalate metabolism in the gut and/or excretion in feces or urine. Deficiencies in any one of the these pathways can lead to complications, such as calcium oxalate urina...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Aaron W. Miller, Colin Dale, M. Denise Dearing
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2017
Materias:
Acceso en línea:https://doaj.org/article/3182983fd427450098aaabb8447d44e4
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:3182983fd427450098aaabb8447d44e4
record_format dspace
spelling oai:doaj.org-article:3182983fd427450098aaabb8447d44e42021-12-02T19:47:35ZThe Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species10.1128/mSystems.00088-172379-5077https://doaj.org/article/3182983fd427450098aaabb8447d44e42017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00088-17https://doaj.org/toc/2379-5077ABSTRACT For mammals, oxalate enters the body through the diet or is endogenously produced by the liver; it is removed by microbial oxalate metabolism in the gut and/or excretion in feces or urine. Deficiencies in any one of the these pathways can lead to complications, such as calcium oxalate urinary stones. While considerable research has been conducted on individual oxalate-degrading bacterial isolates, interactions between oxalate and the gut microbiota as a whole are unknown. We examined the reduction in oxalate excretion in a rat model following oral administration of fecal microbes from a mammalian herbivore adapted to a high oxalate diet or to fecal transplants consisting of two different formulations of mixed oxalate-degrading isolates. While all transplants elicited a significant reduction in oxalate excretion initially, the greatest effect was seen with fecal microbial transplants, which persisted even in the absence of dietary oxalate. The reduction in oxalate excretion in animals given fecal transplants corresponded with the establishment of diverse bacteria, including known oxalate-degrading bacteria and a cohesive network of bacteria centered on oxalate-degrading specialists from the Oxalobacteraceae family. Results suggested that the administration of a complete community of bacteria facilitates a cohesive balance in terms of microbial interactions. Our work offers important insights into the development of targeted bacteriotherapies intended to reduce urinary oxalate excretion in patients at risk for recurrent calcium oxalate stones as well as bacteriotherapies targeting other toxins for elimination. IMPORTANCE Oxalate is a central component in 80% of kidney stones. While mammals do not possess the enzymes to degrade oxalate, many gastrointestinal bacteria are efficient oxalate degraders. We examined the role of cohesive microbial networks for oxalate metabolism, using Sprague-Dawley rats as a model host. While the transplantation of oxalate-degrading bacteria alone to the Sprague-Dawley hosts did increase oxalate metabolism, fecal transplants from a wild mammalian herbivore, Neotoma albigula, had a significantly greater effect. Furthermore, the boost for oxalate metabolism persisted only in animals that received fecal transplants. Animals receiving fecal transplants had a more diverse and cohesive network of bacteria associated with the Oxalobacteraceae, a family known to consist of specialist oxalate-degrading bacteria, than did animals that received oxalate-degrading bacteria alone. Our results indicate that fecal transplants are more effective at transferring specific functions than are microbial specialists alone, which has broad implications for the development of bacteriotherapies.Aaron W. MillerColin DaleM. Denise DearingAmerican Society for Microbiologyarticlefecal transplantgut microbiotaoxalateprobioticswoodratMicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution DOAJ
collection DOAJ
language EN
topic fecal transplant
gut microbiota
oxalate
probiotics
woodrat
Microbiology
QR1-502
spellingShingle fecal transplant
gut microbiota
oxalate
probiotics
woodrat
Microbiology
QR1-502
Aaron W. Miller
Colin Dale
M. Denise Dearing
The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
description ABSTRACT For mammals, oxalate enters the body through the diet or is endogenously produced by the liver; it is removed by microbial oxalate metabolism in the gut and/or excretion in feces or urine. Deficiencies in any one of the these pathways can lead to complications, such as calcium oxalate urinary stones. While considerable research has been conducted on individual oxalate-degrading bacterial isolates, interactions between oxalate and the gut microbiota as a whole are unknown. We examined the reduction in oxalate excretion in a rat model following oral administration of fecal microbes from a mammalian herbivore adapted to a high oxalate diet or to fecal transplants consisting of two different formulations of mixed oxalate-degrading isolates. While all transplants elicited a significant reduction in oxalate excretion initially, the greatest effect was seen with fecal microbial transplants, which persisted even in the absence of dietary oxalate. The reduction in oxalate excretion in animals given fecal transplants corresponded with the establishment of diverse bacteria, including known oxalate-degrading bacteria and a cohesive network of bacteria centered on oxalate-degrading specialists from the Oxalobacteraceae family. Results suggested that the administration of a complete community of bacteria facilitates a cohesive balance in terms of microbial interactions. Our work offers important insights into the development of targeted bacteriotherapies intended to reduce urinary oxalate excretion in patients at risk for recurrent calcium oxalate stones as well as bacteriotherapies targeting other toxins for elimination. IMPORTANCE Oxalate is a central component in 80% of kidney stones. While mammals do not possess the enzymes to degrade oxalate, many gastrointestinal bacteria are efficient oxalate degraders. We examined the role of cohesive microbial networks for oxalate metabolism, using Sprague-Dawley rats as a model host. While the transplantation of oxalate-degrading bacteria alone to the Sprague-Dawley hosts did increase oxalate metabolism, fecal transplants from a wild mammalian herbivore, Neotoma albigula, had a significantly greater effect. Furthermore, the boost for oxalate metabolism persisted only in animals that received fecal transplants. Animals receiving fecal transplants had a more diverse and cohesive network of bacteria associated with the Oxalobacteraceae, a family known to consist of specialist oxalate-degrading bacteria, than did animals that received oxalate-degrading bacteria alone. Our results indicate that fecal transplants are more effective at transferring specific functions than are microbial specialists alone, which has broad implications for the development of bacteriotherapies.
format article
author Aaron W. Miller
Colin Dale
M. Denise Dearing
author_facet Aaron W. Miller
Colin Dale
M. Denise Dearing
author_sort Aaron W. Miller
title The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
title_short The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
title_full The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
title_fullStr The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
title_full_unstemmed The Induction of Oxalate Metabolism <italic toggle="yes">In Vivo</italic> Is More Effective with Functional Microbial Communities than with Functional Microbial Species
title_sort induction of oxalate metabolism <italic toggle="yes">in vivo</italic> is more effective with functional microbial communities than with functional microbial species
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/3182983fd427450098aaabb8447d44e4
work_keys_str_mv AT aaronwmiller theinductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
AT colindale theinductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
AT mdenisedearing theinductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
AT aaronwmiller inductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
AT colindale inductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
AT mdenisedearing inductionofoxalatemetabolismitalictoggleyesinvivoitalicismoreeffectivewithfunctionalmicrobialcommunitiesthanwithfunctionalmicrobialspecies
_version_ 1718375951902965760