Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice

ABSTRACT Fluoridation of drinking water and dental products prevents dental caries primarily by inhibiting energy harvest in oral cariogenic bacteria (such as Streptococcus mutans and Streptococcus sanguinis), thus leading to their depletion. However, the extent to which oral and gut microbial commu...

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Autores principales: Koji Yasuda, Tiffany Hsu, Carey A. Gallini, Lauren J. Mclver, Emma Schwager, Andy Shi, Casey R. DuLong, Randall N. Schwager, Galeb S. Abu-Ali, Eric A. Franzosa, Wendy S. Garrett, Curtis Huttenhower, Xochitl C. Morgan
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:91531918179a4700924bdcda6e2ab7442021-12-02T18:39:32ZFluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice10.1128/mSystems.00047-172379-5077https://doaj.org/article/91531918179a4700924bdcda6e2ab7442017-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00047-17https://doaj.org/toc/2379-5077ABSTRACT Fluoridation of drinking water and dental products prevents dental caries primarily by inhibiting energy harvest in oral cariogenic bacteria (such as Streptococcus mutans and Streptococcus sanguinis), thus leading to their depletion. However, the extent to which oral and gut microbial communities are affected by host fluoride exposure has been underexplored. In this study, we modeled human fluoride exposures to municipal water and dental products by treating mice with low or high levels of fluoride over a 12-week period. We then used 16S rRNA gene amplicon and shotgun metagenomic sequencing to assess fluoride’s effects on oral and gut microbiome composition and function. In both the low- and high-fluoride groups, several operational taxonomic units (OTUs) belonging to acidogenic bacterial genera (such as Parabacteroides, Bacteroides, and Bilophila) were depleted in the oral community. In addition, fluoride-associated changes in oral community composition resulted in depletion of gene families involved in central carbon metabolism and energy harvest (2-oxoglutarate ferredoxin oxidoreductase, succinate dehydrogenase, and the glyoxylate cycle). In contrast, fluoride treatment did not induce a significant shift in gut microbial community composition or function in our mouse model, possibly due to absorption in the upper gastrointestinal tract. Fluoride-associated perturbations thus appeared to have a selective effect on the composition of the oral but not gut microbial community in mice. Future studies will be necessary to understand possible implications of fluoride exposure for the human microbiome. IMPORTANCE Fluoride has been added to drinking water and dental products since the 1950s. The beneficial effects of fluoride on oral health are due to its ability to inhibit the growth of bacteria that cause dental caries. Despite widespread human consumption of fluoride, there have been only two studies of humans that considered the effect of fluoride on human-associated microbial communities, which are increasingly understood to play important roles in health and disease. Notably, neither of these studies included a true cross-sectional control lacking fluoride exposure, as study subjects continued baseline fluoride treatment in their daily dental hygiene routines. To our knowledge, this work (in mice) is the first controlled study to assess the independent effects of fluoride exposure on the oral and gut microbial communities. Investigating how fluoride interacts with host-associated microbial communities in this controlled setting represents an effort toward understanding how common environmental exposures may potentially influence health.Koji YasudaTiffany HsuCarey A. GalliniLauren J. MclverEmma SchwagerAndy ShiCasey R. DuLongRandall N. SchwagerGaleb S. Abu-AliEric A. FranzosaWendy S. GarrettCurtis HuttenhowerXochitl C. MorganAmerican Society for Microbiologyarticle16S rRNA sequencingfluoridationfluoridegut microbiomemouseoral microbiomeMicrobiologyQR1-502ENmSystems, Vol 2, Iss 4 (2017)
institution DOAJ
collection DOAJ
language EN
topic 16S rRNA sequencing
fluoridation
fluoride
gut microbiome
mouse
oral microbiome
Microbiology
QR1-502
spellingShingle 16S rRNA sequencing
fluoridation
fluoride
gut microbiome
mouse
oral microbiome
Microbiology
QR1-502
Koji Yasuda
Tiffany Hsu
Carey A. Gallini
Lauren J. Mclver
Emma Schwager
Andy Shi
Casey R. DuLong
Randall N. Schwager
Galeb S. Abu-Ali
Eric A. Franzosa
Wendy S. Garrett
Curtis Huttenhower
Xochitl C. Morgan
Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
description ABSTRACT Fluoridation of drinking water and dental products prevents dental caries primarily by inhibiting energy harvest in oral cariogenic bacteria (such as Streptococcus mutans and Streptococcus sanguinis), thus leading to their depletion. However, the extent to which oral and gut microbial communities are affected by host fluoride exposure has been underexplored. In this study, we modeled human fluoride exposures to municipal water and dental products by treating mice with low or high levels of fluoride over a 12-week period. We then used 16S rRNA gene amplicon and shotgun metagenomic sequencing to assess fluoride’s effects on oral and gut microbiome composition and function. In both the low- and high-fluoride groups, several operational taxonomic units (OTUs) belonging to acidogenic bacterial genera (such as Parabacteroides, Bacteroides, and Bilophila) were depleted in the oral community. In addition, fluoride-associated changes in oral community composition resulted in depletion of gene families involved in central carbon metabolism and energy harvest (2-oxoglutarate ferredoxin oxidoreductase, succinate dehydrogenase, and the glyoxylate cycle). In contrast, fluoride treatment did not induce a significant shift in gut microbial community composition or function in our mouse model, possibly due to absorption in the upper gastrointestinal tract. Fluoride-associated perturbations thus appeared to have a selective effect on the composition of the oral but not gut microbial community in mice. Future studies will be necessary to understand possible implications of fluoride exposure for the human microbiome. IMPORTANCE Fluoride has been added to drinking water and dental products since the 1950s. The beneficial effects of fluoride on oral health are due to its ability to inhibit the growth of bacteria that cause dental caries. Despite widespread human consumption of fluoride, there have been only two studies of humans that considered the effect of fluoride on human-associated microbial communities, which are increasingly understood to play important roles in health and disease. Notably, neither of these studies included a true cross-sectional control lacking fluoride exposure, as study subjects continued baseline fluoride treatment in their daily dental hygiene routines. To our knowledge, this work (in mice) is the first controlled study to assess the independent effects of fluoride exposure on the oral and gut microbial communities. Investigating how fluoride interacts with host-associated microbial communities in this controlled setting represents an effort toward understanding how common environmental exposures may potentially influence health.
format article
author Koji Yasuda
Tiffany Hsu
Carey A. Gallini
Lauren J. Mclver
Emma Schwager
Andy Shi
Casey R. DuLong
Randall N. Schwager
Galeb S. Abu-Ali
Eric A. Franzosa
Wendy S. Garrett
Curtis Huttenhower
Xochitl C. Morgan
author_facet Koji Yasuda
Tiffany Hsu
Carey A. Gallini
Lauren J. Mclver
Emma Schwager
Andy Shi
Casey R. DuLong
Randall N. Schwager
Galeb S. Abu-Ali
Eric A. Franzosa
Wendy S. Garrett
Curtis Huttenhower
Xochitl C. Morgan
author_sort Koji Yasuda
title Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
title_short Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
title_full Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
title_fullStr Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
title_full_unstemmed Fluoride Depletes Acidogenic Taxa in Oral but Not Gut Microbial Communities in Mice
title_sort fluoride depletes acidogenic taxa in oral but not gut microbial communities in mice
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/91531918179a4700924bdcda6e2ab744
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