Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model

Jie Zhang; Xiyue Chen; Ping Liu; Jinbiao Zhao; Jian Sun; Wenyi Guan; Lee J. Johnston; Crystal L. Levesque; Peixin Fan; Ting He; Guolong Zhang; Xi Ma

doi:10.1021/acs.jafc.8b01253

Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model

Jie Zhang, Xiyue Chen, Ping Liu, Jinbiao Zhao, Jian Sun, Wenyi Guan, Lee J. Johnston, Crystal L. Levesque, Peixin Fan, Ting He, Guolong Zhang, Xi Ma

West Central Research and Outreach Center

Research output: Contribution to journal › Article › peer-review

33 Scopus citations

Abstract

Clostridium butyricum is known as a butyrate producer and a regulator of gut health, but whether it exerts a beneficial effect as a dietary supplement via modulating the intestinal microbiota remains elusive. This study investigated the impact of C. butyricum on the fecal microbiota composition and their metabolites 14 and 28 days after weaning with 10 g/kg dietary supplementation of C. butyricum. Dynamic changes of microbial compositions showed dramatically increasing Selenomonadales and decreasing Clostridiales on days 14 and 28. Within Selenomonadales, Megasphaera became the main responder by increasing from 3.79 to 11.31%. Following the prevalence of some acetate producers (Magasphaera) and utilizers (Eubacterium-hallii) at the genus level and even with a significant decrease in fecal acetate on day 28, the present data suggested that C. butyricum influenced microbial metabolism by optimizing the structure of microbiota and enhancing acetate production and utilization for butyrate production.

Original language	English (US)
Pages (from-to)	5157-5166
Number of pages	10
Journal	Journal of agricultural and food chemistry
Volume	66
Issue number	20
DOIs	https://doi.org/10.1021/acs.jafc.8b01253
State	Published - May 23 2018

Bibliographical note

Funding Information:
*E-mail: zguolon@okstate.edu. *E-mail: maxi@cau.edu.cn. Phone: 86-13811794292. Fax: 86-10-62733688. ORCID Jie Zhang: 0000-0001-5010-0833 Ping Liu: 0000-0002-8298-6576 Xi Ma: 0000-0002-2856-9501 Author Contributions □These authors contributed equally to this work. Author Contributions The work was mainly conceived and designed by X.M. and G.L.Z. Experimental data were collected and analyzed by J.Z., X.Y.C., P.L., and J.B.Z. The manuscript was mainly written by J.Z. and X.Y.C. with revisions of the draft assisted by J.S., W.Y.G., and P.X.F. and edited by L.J.J., C.L.L., T.H., and X.M; X.M. resourced the project. All of the authors contributed to, read, and approved of the final manuscript. Funding This work was supported by grants from the National Key R&D Program of China (2017YFD0500501), the National Basic Research Program of China (973 Program, 2013CB117301), the National Natural Science Foundation of China (31722054, 31472101, and 31528018), the College of Animal Science and Technology “Young Talents Program” in China Agricultural University (2017DKA001), the 111 Project (B16044), National Department Public Benefit Research Foundation (201403047), the developmental fund for animal science by Shenzhen Jinxinnong Feed Co., Ltd., and the Beijing Nova Programme Interdisciplinary Cooperation Project (xxjc201804). Notes The authors declare no competing financial interest.

Keywords

Clostridium butyricum
acetate production
fecal microbiota
phased shift
short chain fatty acid
weaned piglet

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10.1021/acs.jafc.8b01253

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Zhang, J., Chen, X., Liu, P., Zhao, J., Sun, J., Guan, W., Johnston, L. J., Levesque, C. L., Fan, P., He, T., Zhang, G., & Ma, X. (2018). Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model. Journal of agricultural and food chemistry, 66(20), 5157-5166. https://doi.org/10.1021/acs.jafc.8b01253

Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model. / Zhang, Jie; Chen, Xiyue; Liu, Ping; Zhao, Jinbiao; Sun, Jian; Guan, Wenyi; Johnston, Lee J.; Levesque, Crystal L.; Fan, Peixin; He, Ting; Zhang, Guolong; Ma, Xi.

In: Journal of agricultural and food chemistry, Vol. 66, No. 20, 23.05.2018, p. 5157-5166.

Research output: Contribution to journal › Article › peer-review

Zhang, J, Chen, X, Liu, P, Zhao, J, Sun, J, Guan, W, Johnston, LJ, Levesque, CL, Fan, P, He, T, Zhang, G & Ma, X 2018, 'Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model', Journal of agricultural and food chemistry, vol. 66, no. 20, pp. 5157-5166. https://doi.org/10.1021/acs.jafc.8b01253

Zhang, Jie ; Chen, Xiyue ; Liu, Ping ; Zhao, Jinbiao ; Sun, Jian ; Guan, Wenyi ; Johnston, Lee J. ; Levesque, Crystal L. ; Fan, Peixin ; He, Ting ; Zhang, Guolong ; Ma, Xi. / Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model. In: Journal of agricultural and food chemistry. 2018 ; Vol. 66, No. 20. pp. 5157-5166.

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title = "Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model",

abstract = "Clostridium butyricum is known as a butyrate producer and a regulator of gut health, but whether it exerts a beneficial effect as a dietary supplement via modulating the intestinal microbiota remains elusive. This study investigated the impact of C. butyricum on the fecal microbiota composition and their metabolites 14 and 28 days after weaning with 10 g/kg dietary supplementation of C. butyricum. Dynamic changes of microbial compositions showed dramatically increasing Selenomonadales and decreasing Clostridiales on days 14 and 28. Within Selenomonadales, Megasphaera became the main responder by increasing from 3.79 to 11.31%. Following the prevalence of some acetate producers (Magasphaera) and utilizers (Eubacterium-hallii) at the genus level and even with a significant decrease in fecal acetate on day 28, the present data suggested that C. butyricum influenced microbial metabolism by optimizing the structure of microbiota and enhancing acetate production and utilization for butyrate production.",

keywords = "Clostridium butyricum, acetate production, fecal microbiota, phased shift, short chain fatty acid, weaned piglet",

author = "Jie Zhang and Xiyue Chen and Ping Liu and Jinbiao Zhao and Jian Sun and Wenyi Guan and Johnston, {Lee J.} and Levesque, {Crystal L.} and Peixin Fan and Ting He and Guolong Zhang and Xi Ma",

note = "Funding Information: *E-mail: zguolon@okstate.edu. *E-mail: maxi@cau.edu.cn. Phone: 86-13811794292. Fax: 86-10-62733688. ORCID Jie Zhang: 0000-0001-5010-0833 Ping Liu: 0000-0002-8298-6576 Xi Ma: 0000-0002-2856-9501 Author Contributions □These authors contributed equally to this work. Author Contributions The work was mainly conceived and designed by X.M. and G.L.Z. Experimental data were collected and analyzed by J.Z., X.Y.C., P.L., and J.B.Z. The manuscript was mainly written by J.Z. and X.Y.C. with revisions of the draft assisted by J.S., W.Y.G., and P.X.F. and edited by L.J.J., C.L.L., T.H., and X.M; X.M. resourced the project. All of the authors contributed to, read, and approved of the final manuscript. Funding This work was supported by grants from the National Key R&D Program of China (2017YFD0500501), the National Basic Research Program of China (973 Program, 2013CB117301), the National Natural Science Foundation of China (31722054, 31472101, and 31528018), the College of Animal Science and Technology “Young Talents Program” in China Agricultural University (2017DKA001), the 111 Project (B16044), National Department Public Benefit Research Foundation (201403047), the developmental fund for animal science by Shenzhen Jinxinnong Feed Co., Ltd., and the Beijing Nova Programme Interdisciplinary Cooperation Project (xxjc201804). Notes The authors declare no competing financial interest.",

year = "2018",

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doi = "10.1021/acs.jafc.8b01253",

language = "English (US)",

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T1 - Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model

AU - Zhang, Jie

AU - Chen, Xiyue

AU - Liu, Ping

AU - Zhao, Jinbiao

AU - Sun, Jian

AU - Guan, Wenyi

AU - Johnston, Lee J.

AU - Levesque, Crystal L.

AU - Fan, Peixin

AU - He, Ting

AU - Zhang, Guolong

AU - Ma, Xi

N1 - Funding Information: *E-mail: zguolon@okstate.edu. *E-mail: maxi@cau.edu.cn. Phone: 86-13811794292. Fax: 86-10-62733688. ORCID Jie Zhang: 0000-0001-5010-0833 Ping Liu: 0000-0002-8298-6576 Xi Ma: 0000-0002-2856-9501 Author Contributions □These authors contributed equally to this work. Author Contributions The work was mainly conceived and designed by X.M. and G.L.Z. Experimental data were collected and analyzed by J.Z., X.Y.C., P.L., and J.B.Z. The manuscript was mainly written by J.Z. and X.Y.C. with revisions of the draft assisted by J.S., W.Y.G., and P.X.F. and edited by L.J.J., C.L.L., T.H., and X.M; X.M. resourced the project. All of the authors contributed to, read, and approved of the final manuscript. Funding This work was supported by grants from the National Key R&D Program of China (2017YFD0500501), the National Basic Research Program of China (973 Program, 2013CB117301), the National Natural Science Foundation of China (31722054, 31472101, and 31528018), the College of Animal Science and Technology “Young Talents Program” in China Agricultural University (2017DKA001), the 111 Project (B16044), National Department Public Benefit Research Foundation (201403047), the developmental fund for animal science by Shenzhen Jinxinnong Feed Co., Ltd., and the Beijing Nova Programme Interdisciplinary Cooperation Project (xxjc201804). Notes The authors declare no competing financial interest.

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N2 - Clostridium butyricum is known as a butyrate producer and a regulator of gut health, but whether it exerts a beneficial effect as a dietary supplement via modulating the intestinal microbiota remains elusive. This study investigated the impact of C. butyricum on the fecal microbiota composition and their metabolites 14 and 28 days after weaning with 10 g/kg dietary supplementation of C. butyricum. Dynamic changes of microbial compositions showed dramatically increasing Selenomonadales and decreasing Clostridiales on days 14 and 28. Within Selenomonadales, Megasphaera became the main responder by increasing from 3.79 to 11.31%. Following the prevalence of some acetate producers (Magasphaera) and utilizers (Eubacterium-hallii) at the genus level and even with a significant decrease in fecal acetate on day 28, the present data suggested that C. butyricum influenced microbial metabolism by optimizing the structure of microbiota and enhancing acetate production and utilization for butyrate production.

AB - Clostridium butyricum is known as a butyrate producer and a regulator of gut health, but whether it exerts a beneficial effect as a dietary supplement via modulating the intestinal microbiota remains elusive. This study investigated the impact of C. butyricum on the fecal microbiota composition and their metabolites 14 and 28 days after weaning with 10 g/kg dietary supplementation of C. butyricum. Dynamic changes of microbial compositions showed dramatically increasing Selenomonadales and decreasing Clostridiales on days 14 and 28. Within Selenomonadales, Megasphaera became the main responder by increasing from 3.79 to 11.31%. Following the prevalence of some acetate producers (Magasphaera) and utilizers (Eubacterium-hallii) at the genus level and even with a significant decrease in fecal acetate on day 28, the present data suggested that C. butyricum influenced microbial metabolism by optimizing the structure of microbiota and enhancing acetate production and utilization for butyrate production.

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KW - acetate production

KW - fecal microbiota

KW - phased shift

KW - short chain fatty acid

KW - weaned piglet

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Dietary Clostridium butyricum Induces a Phased Shift in Fecal Microbiota Structure and Increases the Acetic Acid-Producing Bacteria in a Weaned Piglet Model

Abstract

Bibliographical note

Keywords

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