Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome

The gut microbiome is a dynamic ecosystem formed by thousands of diverse bacterial species. This bacterial diversity is acquired early in life and shaped over time by a combination of multiple factors, including dietary exposure to distinct nutrients and xenobiotics. Alterations of the gut microbiot...

Full description

Bibliographic Details
Main Authors: Keng Po Lai, Alice Hoi-Man Ng, Hin Ting Wan, Aman Yi-Man Wong, Cherry Chi-Tim Leung, Rong Li, Chris Kong-Chu Wong
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02552/full
_version_ 1819073862207275008
author Keng Po Lai
Alice Hoi-Man Ng
Hin Ting Wan
Aman Yi-Man Wong
Cherry Chi-Tim Leung
Rong Li
Chris Kong-Chu Wong
author_facet Keng Po Lai
Alice Hoi-Man Ng
Hin Ting Wan
Aman Yi-Man Wong
Cherry Chi-Tim Leung
Rong Li
Chris Kong-Chu Wong
author_sort Keng Po Lai
collection DOAJ
description The gut microbiome is a dynamic ecosystem formed by thousands of diverse bacterial species. This bacterial diversity is acquired early in life and shaped over time by a combination of multiple factors, including dietary exposure to distinct nutrients and xenobiotics. Alterations of the gut microbiota composition and associated metabolic activities in the gut are linked to various immune and metabolic diseases. The microbiota could potentially interact with xenobiotics in the gut environment as a result of their board enzymatic capacities and thereby affect the bioavailability and toxicity of the xenobiotics in enterohepatic circulation. Consequently, microbiome-xenobiotic interactions might affect host health. Here, we aimed to investigate the effects of dietary perfluorooctane sulfonic acid (PFOS) exposure on gut microbiota in adult mice and examine the induced changes in animal metabolic functions. In mice exposed to dietary PFOS for 7 weeks, body PFOS and lipid contents were measured, and to elucidate the effects of PFOS exposure, the metabolic functions of the animals were assessed using oral glucose-tolerance test and intraperitoneal insulin-tolerance and pyruvate-tolerance tests; moreover, on Day 50, cecal bacterial DNA was isolated and subject to 16S rDNA sequencing. Our results demonstrated that PFOS exposure caused metabolic disturbances in the animals, particularly in lipid and glucose metabolism, but did not substantially affect the diversity of gut bacterial species. However, marked modulations were detected in the abundance of metabolism-associated bacteria belonging to the phyla Firmicutes, Bacteroidetes, Proteobacteria, and Cyanobacteria, including, at different taxonomic levels, Turicibacteraceae, Turicibacterales, Turicibacter, Dehalobacteriaceae, Dehalobacterium, Allobaculum, Bacteroides acidifaciens, Alphaproteobacteria, and 4Cod-2/YS2. The results of PICRUSt analysis further indicated that PFOS exposure perturbed gut metabolism, inducing notable changes in the metabolism of amino acids (arginine, proline, lysine), methane, and a short-chain fatty acid (butanoate), all of which are metabolites widely recognized to be associated with inflammation and metabolic functions. Collectively, our study findings provide key information regarding the biological relevance of microbiome–xenobiotic interactions associated with the ecology of gut microbiota and animal energy metabolism.
first_indexed 2024-12-21T18:00:22Z
format Article
id doaj.art-8322252088d640959f4338d3cf33bc19
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-21T18:00:22Z
publishDate 2018-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-8322252088d640959f4338d3cf33bc192022-12-21T18:55:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-10-01910.3389/fmicb.2018.02552409551Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic SyndromeKeng Po Lai0Alice Hoi-Man Ng1Hin Ting Wan2Aman Yi-Man Wong3Cherry Chi-Tim Leung4Rong Li5Chris Kong-Chu Wong6Department of Chemistry, City University of Hong Kong, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCroucher Institute for Environmental Sciences, Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongThe gut microbiome is a dynamic ecosystem formed by thousands of diverse bacterial species. This bacterial diversity is acquired early in life and shaped over time by a combination of multiple factors, including dietary exposure to distinct nutrients and xenobiotics. Alterations of the gut microbiota composition and associated metabolic activities in the gut are linked to various immune and metabolic diseases. The microbiota could potentially interact with xenobiotics in the gut environment as a result of their board enzymatic capacities and thereby affect the bioavailability and toxicity of the xenobiotics in enterohepatic circulation. Consequently, microbiome-xenobiotic interactions might affect host health. Here, we aimed to investigate the effects of dietary perfluorooctane sulfonic acid (PFOS) exposure on gut microbiota in adult mice and examine the induced changes in animal metabolic functions. In mice exposed to dietary PFOS for 7 weeks, body PFOS and lipid contents were measured, and to elucidate the effects of PFOS exposure, the metabolic functions of the animals were assessed using oral glucose-tolerance test and intraperitoneal insulin-tolerance and pyruvate-tolerance tests; moreover, on Day 50, cecal bacterial DNA was isolated and subject to 16S rDNA sequencing. Our results demonstrated that PFOS exposure caused metabolic disturbances in the animals, particularly in lipid and glucose metabolism, but did not substantially affect the diversity of gut bacterial species. However, marked modulations were detected in the abundance of metabolism-associated bacteria belonging to the phyla Firmicutes, Bacteroidetes, Proteobacteria, and Cyanobacteria, including, at different taxonomic levels, Turicibacteraceae, Turicibacterales, Turicibacter, Dehalobacteriaceae, Dehalobacterium, Allobaculum, Bacteroides acidifaciens, Alphaproteobacteria, and 4Cod-2/YS2. The results of PICRUSt analysis further indicated that PFOS exposure perturbed gut metabolism, inducing notable changes in the metabolism of amino acids (arginine, proline, lysine), methane, and a short-chain fatty acid (butanoate), all of which are metabolites widely recognized to be associated with inflammation and metabolic functions. Collectively, our study findings provide key information regarding the biological relevance of microbiome–xenobiotic interactions associated with the ecology of gut microbiota and animal energy metabolism.https://www.frontiersin.org/article/10.3389/fmicb.2018.02552/fullgut microbiomebacterial diversitymicrobiome-xenobiotic interactionPFOsenergy metabolism
spellingShingle Keng Po Lai
Alice Hoi-Man Ng
Hin Ting Wan
Aman Yi-Man Wong
Cherry Chi-Tim Leung
Rong Li
Chris Kong-Chu Wong
Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
Frontiers in Microbiology
gut microbiome
bacterial diversity
microbiome-xenobiotic interaction
PFOs
energy metabolism
title Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
title_full Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
title_fullStr Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
title_full_unstemmed Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
title_short Dietary Exposure to the Environmental Chemical, PFOS on the Diversity of Gut Microbiota, Associated With the Development of Metabolic Syndrome
title_sort dietary exposure to the environmental chemical pfos on the diversity of gut microbiota associated with the development of metabolic syndrome
topic gut microbiome
bacterial diversity
microbiome-xenobiotic interaction
PFOs
energy metabolism
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02552/full
work_keys_str_mv AT kengpolai dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT alicehoimanng dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT hintingwan dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT amanyimanwong dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT cherrychitimleung dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT rongli dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome
AT chriskongchuwong dietaryexposuretotheenvironmentalchemicalpfosonthediversityofgutmicrobiotaassociatedwiththedevelopmentofmetabolicsyndrome