High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice

Liang Xiao, Si Brask Sonne, Qiang Feng, Ning Chen, Zhongkui Xia, Xiaoping Li, Zhiwei Fang, Dongya Zhang, Even Fjære, Lisa Kolden Midtbø, Muriel Derrien, Floor Hugenholtz, Longqing Tang, Junhua Li, Jianfeng Zhang, Chuan Liu, Qin Hao, Ulla Birgitte Vogel, Alicja Mortensen, Michiel Kleerebezem & 8 others Tine Rask Licht, Huanming Yang, Jian Wang, Yingrui Li, Manimozhiyan Arumugam, Jun Wang, Lise Madsen, Karsten Kristiansen

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Abstract

BACKGROUND: It is well known that the microbiota of high-fat (HF) diet-induced obese mice differs from that of lean mice, but to what extent, this difference reflects the obese state or the diet is unclear. To dissociate changes in the gut microbiota associated with high HF feeding from those associated with obesity, we took advantage of the different susceptibility of C57BL/6JBomTac (BL6) and 129S6/SvEvTac (Sv129) mice to diet-induced obesity and of their different responses to inhibition of cyclooxygenase (COX) activity, where inhibition of COX activity in BL6 mice prevents HF diet-induced obesity, but in Sv129 mice accentuates obesity.

RESULTS: Using HiSeq-based whole genome sequencing, we identified taxonomic and functional differences in the gut microbiota of the two mouse strains fed regular low-fat or HF diets with or without supplementation with the COX-inhibitor, indomethacin. HF feeding rather than obesity development led to distinct changes in the gut microbiota. We observed a robust increase in alpha diversity, gene count, abundance of genera known to be butyrate producers, and abundance of genes involved in butyrate production in Sv129 mice compared to BL6 mice fed either a LF or a HF diet. Conversely, the abundance of genes involved in propionate metabolism, associated with increased energy harvest, was higher in BL6 mice than Sv129 mice.

CONCLUSIONS: The changes in the composition of the gut microbiota were predominantly driven by high-fat feeding rather than reflecting the obese state of the mice. Differences in the abundance of butyrate and propionate producing bacteria in the gut may at least in part contribute to the observed differences in obesity propensity in Sv129 and BL6 mice.

Original languageEnglish
Pages (from-to)43
JournalMicrobiome
Volume5
DOIs
Publication statusPublished - 2017

Fingerprint

Obesity
Fats
High Fat Diet
Butyrates
Obese Mice
Propionates
Prostaglandin-Endoperoxide Synthases
Gastrointestinal Microbiome
Genes
Diet
Cyclooxygenase Inhibitors
Microbiota
Indomethacin
Genome
Bacteria

Keywords

  • 129S6/Sv mice
  • C57BL/6J mice
  • High-fat feeding
  • Indomethacin
  • Microbiome
  • Microbiota
  • Obesity

Cite this

Xiao, Liang ; Sonne, Si Brask ; Feng, Qiang ; Chen, Ning ; Xia, Zhongkui ; Li, Xiaoping ; Fang, Zhiwei ; Zhang, Dongya ; Fjære, Even ; Midtbø, Lisa Kolden ; Derrien, Muriel ; Hugenholtz, Floor ; Tang, Longqing ; Li, Junhua ; Zhang, Jianfeng ; Liu, Chuan ; Hao, Qin ; Vogel, Ulla Birgitte ; Mortensen, Alicja ; Kleerebezem, Michiel ; Licht, Tine Rask ; Yang, Huanming ; Wang, Jian ; Li, Yingrui ; Arumugam, Manimozhiyan ; Wang, Jun ; Madsen, Lise ; Kristiansen, Karsten. / High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice. In: Microbiome. 2017 ; Vol. 5. pp. 43.
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title = "High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice",
abstract = "BACKGROUND: It is well known that the microbiota of high-fat (HF) diet-induced obese mice differs from that of lean mice, but to what extent, this difference reflects the obese state or the diet is unclear. To dissociate changes in the gut microbiota associated with high HF feeding from those associated with obesity, we took advantage of the different susceptibility of C57BL/6JBomTac (BL6) and 129S6/SvEvTac (Sv129) mice to diet-induced obesity and of their different responses to inhibition of cyclooxygenase (COX) activity, where inhibition of COX activity in BL6 mice prevents HF diet-induced obesity, but in Sv129 mice accentuates obesity.RESULTS: Using HiSeq-based whole genome sequencing, we identified taxonomic and functional differences in the gut microbiota of the two mouse strains fed regular low-fat or HF diets with or without supplementation with the COX-inhibitor, indomethacin. HF feeding rather than obesity development led to distinct changes in the gut microbiota. We observed a robust increase in alpha diversity, gene count, abundance of genera known to be butyrate producers, and abundance of genes involved in butyrate production in Sv129 mice compared to BL6 mice fed either a LF or a HF diet. Conversely, the abundance of genes involved in propionate metabolism, associated with increased energy harvest, was higher in BL6 mice than Sv129 mice.CONCLUSIONS: The changes in the composition of the gut microbiota were predominantly driven by high-fat feeding rather than reflecting the obese state of the mice. Differences in the abundance of butyrate and propionate producing bacteria in the gut may at least in part contribute to the observed differences in obesity propensity in Sv129 and BL6 mice.",
keywords = "129S6/Sv mice, C57BL/6J mice, High-fat feeding, Indomethacin, Microbiome, Microbiota, Obesity",
author = "Liang Xiao and Sonne, {Si Brask} and Qiang Feng and Ning Chen and Zhongkui Xia and Xiaoping Li and Zhiwei Fang and Dongya Zhang and Even Fj{\ae}re and Midtb{\o}, {Lisa Kolden} and Muriel Derrien and Floor Hugenholtz and Longqing Tang and Junhua Li and Jianfeng Zhang and Chuan Liu and Qin Hao and Vogel, {Ulla Birgitte} and Alicja Mortensen and Michiel Kleerebezem and Licht, {Tine Rask} and Huanming Yang and Jian Wang and Yingrui Li and Manimozhiyan Arumugam and Jun Wang and Lise Madsen and Karsten Kristiansen",
year = "2017",
doi = "10.1186/s40168-017-0258-6",
language = "English",
volume = "5",
pages = "43",
journal = "Microbiome",
issn = "2049-2618",
publisher = "Springer Verlag",

}

Xiao, L, Sonne, SB, Feng, Q, Chen, N, Xia, Z, Li, X, Fang, Z, Zhang, D, Fjære, E, Midtbø, LK, Derrien, M, Hugenholtz, F, Tang, L, Li, J, Zhang, J, Liu, C, Hao, Q, Vogel, UB, Mortensen, A, Kleerebezem, M, Licht, TR, Yang, H, Wang, J, Li, Y, Arumugam, M, Wang, J, Madsen, L & Kristiansen, K 2017, 'High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice', Microbiome, vol. 5, pp. 43. https://doi.org/10.1186/s40168-017-0258-6

High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice. / Xiao, Liang; Sonne, Si Brask; Feng, Qiang; Chen, Ning; Xia, Zhongkui; Li, Xiaoping; Fang, Zhiwei; Zhang, Dongya; Fjære, Even; Midtbø, Lisa Kolden; Derrien, Muriel; Hugenholtz, Floor; Tang, Longqing; Li, Junhua; Zhang, Jianfeng; Liu, Chuan; Hao, Qin; Vogel, Ulla Birgitte; Mortensen, Alicja; Kleerebezem, Michiel; Licht, Tine Rask; Yang, Huanming; Wang, Jian; Li, Yingrui; Arumugam, Manimozhiyan; Wang, Jun; Madsen, Lise; Kristiansen, Karsten.

In: Microbiome, Vol. 5, 2017, p. 43.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice

AU - Xiao, Liang

AU - Sonne, Si Brask

AU - Feng, Qiang

AU - Chen, Ning

AU - Xia, Zhongkui

AU - Li, Xiaoping

AU - Fang, Zhiwei

AU - Zhang, Dongya

AU - Fjære, Even

AU - Midtbø, Lisa Kolden

AU - Derrien, Muriel

AU - Hugenholtz, Floor

AU - Tang, Longqing

AU - Li, Junhua

AU - Zhang, Jianfeng

AU - Liu, Chuan

AU - Hao, Qin

AU - Vogel, Ulla Birgitte

AU - Mortensen, Alicja

AU - Kleerebezem, Michiel

AU - Licht, Tine Rask

AU - Yang, Huanming

AU - Wang, Jian

AU - Li, Yingrui

AU - Arumugam, Manimozhiyan

AU - Wang, Jun

AU - Madsen, Lise

AU - Kristiansen, Karsten

PY - 2017

Y1 - 2017

N2 - BACKGROUND: It is well known that the microbiota of high-fat (HF) diet-induced obese mice differs from that of lean mice, but to what extent, this difference reflects the obese state or the diet is unclear. To dissociate changes in the gut microbiota associated with high HF feeding from those associated with obesity, we took advantage of the different susceptibility of C57BL/6JBomTac (BL6) and 129S6/SvEvTac (Sv129) mice to diet-induced obesity and of their different responses to inhibition of cyclooxygenase (COX) activity, where inhibition of COX activity in BL6 mice prevents HF diet-induced obesity, but in Sv129 mice accentuates obesity.RESULTS: Using HiSeq-based whole genome sequencing, we identified taxonomic and functional differences in the gut microbiota of the two mouse strains fed regular low-fat or HF diets with or without supplementation with the COX-inhibitor, indomethacin. HF feeding rather than obesity development led to distinct changes in the gut microbiota. We observed a robust increase in alpha diversity, gene count, abundance of genera known to be butyrate producers, and abundance of genes involved in butyrate production in Sv129 mice compared to BL6 mice fed either a LF or a HF diet. Conversely, the abundance of genes involved in propionate metabolism, associated with increased energy harvest, was higher in BL6 mice than Sv129 mice.CONCLUSIONS: The changes in the composition of the gut microbiota were predominantly driven by high-fat feeding rather than reflecting the obese state of the mice. Differences in the abundance of butyrate and propionate producing bacteria in the gut may at least in part contribute to the observed differences in obesity propensity in Sv129 and BL6 mice.

AB - BACKGROUND: It is well known that the microbiota of high-fat (HF) diet-induced obese mice differs from that of lean mice, but to what extent, this difference reflects the obese state or the diet is unclear. To dissociate changes in the gut microbiota associated with high HF feeding from those associated with obesity, we took advantage of the different susceptibility of C57BL/6JBomTac (BL6) and 129S6/SvEvTac (Sv129) mice to diet-induced obesity and of their different responses to inhibition of cyclooxygenase (COX) activity, where inhibition of COX activity in BL6 mice prevents HF diet-induced obesity, but in Sv129 mice accentuates obesity.RESULTS: Using HiSeq-based whole genome sequencing, we identified taxonomic and functional differences in the gut microbiota of the two mouse strains fed regular low-fat or HF diets with or without supplementation with the COX-inhibitor, indomethacin. HF feeding rather than obesity development led to distinct changes in the gut microbiota. We observed a robust increase in alpha diversity, gene count, abundance of genera known to be butyrate producers, and abundance of genes involved in butyrate production in Sv129 mice compared to BL6 mice fed either a LF or a HF diet. Conversely, the abundance of genes involved in propionate metabolism, associated with increased energy harvest, was higher in BL6 mice than Sv129 mice.CONCLUSIONS: The changes in the composition of the gut microbiota were predominantly driven by high-fat feeding rather than reflecting the obese state of the mice. Differences in the abundance of butyrate and propionate producing bacteria in the gut may at least in part contribute to the observed differences in obesity propensity in Sv129 and BL6 mice.

KW - 129S6/Sv mice

KW - C57BL/6J mice

KW - High-fat feeding

KW - Indomethacin

KW - Microbiome

KW - Microbiota

KW - Obesity

UR - https://doi.org/10.6084/m9.figshare.c.3737993

U2 - 10.1186/s40168-017-0258-6

DO - 10.1186/s40168-017-0258-6

M3 - Article

VL - 5

SP - 43

JO - Microbiome

JF - Microbiome

SN - 2049-2618

ER -