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Maternal Breast Milk and Fecal Microbes Guide the Spatiotemporal Development of Mucosa-Associated Microbiota and Barrier Function in the Neonatal Gut

29 Pages Posted: 15 Jun 2019

See all articles by Hongbin Liu

Hongbin Liu

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Xiangfang Zeng

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Guolong Zhang

Oklahoma State University - Stillwater

Chengli Hou

Chinese Academy of Agricultural Sciences (CAAS)

Ning Li

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Haitao Yu

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Lijun Shang

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Xiaoya Zhang

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Paolo Trevisi

University of Bologna

Feiyun Yang

Chongqing Academy of Animal Science

Zuohua Liu

Chongqing Academy of Animal Science

Shiyan Qiao

China Agricultural University - State Key Laboratory of Animal Nutrition; China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

More...

Abstract

Background: The early-life microbiota exerts a profound impact on host health. However, most human gut microbiome studies are based on the analysis of fecal samples. Early development of mucosa-associated intestinal microbiota and its impact on gut function remain poorly understood.

Methods: Using piglets as a model for human infants, we assessed the origin and succession of mucosa-associated microbiota across the intestinal tract in the first 35 days after birth.

Findings: Although sharing a similar composition at birth, the mucosa-associated microbiome in the small intestine (jejunum and ileum) remained relatively stable, while those in the large intestine (cecum and colon) quickly expanded and diversified by day 35. Among the microbial sources from mother and the birth environment, maternal breast milk and fecal microbes were primarily responsible for initial colonization of the neonatal gut. Importantly, we revealed a strong correlation between the relative abundance of mucosa-associated microbes, particularly those transferred from mother, and the expression levels of multiple intestinal immune and barrier function genes in different segments of the intestinal tract.

Interpretation: This study represents a significant expansion from the current understanding on the source and development of the gut microbiota in early life that were based largely on the fecal analysis. It provided new insights into the role of maternal microbiota in the development of gut function in the offspring, laying an important foundation for improving neonatal health through manipulation of maternal microbiota.

Funding Statement: National Natural Science Foundation of China (No. 31420103908), and H2020 European Research Council (Feed-a-Gene, No. 633531).

Declaration of Interests: The authors declare that they have no conflict of interest.

Ethics Approval Statement: All animal procedures reported in this study were approved by the China Agricultural University Institutional Animal Care and Use Committee under Protocol number CAU20161110-2.

Keywords: Mucosal microbiota; Spatiotemporal colonization; Early life; Maternal microbial transmission; Immunologic maturation; Microbiota-host interactions

Suggested Citation

Liu, Hongbin and Zeng, Xiangfang and Zhang, Guolong and Hou, Chengli and Li, Ning and Yu, Haitao and Shang, Lijun and Zhang, Xiaoya and Trevisi, Paolo and Yang, Feiyun and Liu, Zuohua and Qiao, Shiyan, Maternal Breast Milk and Fecal Microbes Guide the Spatiotemporal Development of Mucosa-Associated Microbiota and Barrier Function in the Neonatal Gut (June 13, 2019). Available at SSRN: https://ssrn.com/abstract=3403346 or http://dx.doi.org/10.2139/ssrn.3403346

Hongbin Liu

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Xiangfang Zeng

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Guolong Zhang

Oklahoma State University - Stillwater

Stillwater, OK 74078-0555
United States

Chengli Hou

Chinese Academy of Agricultural Sciences (CAAS)

No.12 Zhongguancun South St.
Beijing, 100081
China

Ning Li

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Haitao Yu

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Lijun Shang

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Xiaoya Zhang

China Agricultural University - State Key Laboratory of Animal Nutrition

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives

Beijing
China

Paolo Trevisi

University of Bologna

Piazza Scaravilli 2
Bologna, 40100
Italy

Feiyun Yang

Chongqing Academy of Animal Science

Chongqing
China

Zuohua Liu

Chongqing Academy of Animal Science

Chongqing
China

Shiyan Qiao (Contact Author)

China Agricultural University - State Key Laboratory of Animal Nutrition ( email )

Beijing
China

China Agricultural University - Beijing Key Laboratory of Bio-Feed Additives ( email )

Beijing
China

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