Comprehensive analysis of the gut microbiome and post-translational modifications elucidates the route involved in microbiota-host interactions

Hai-Yang Wang; Lan-Xiang Liu; Xue-Yi Chen; Yang-Dong Zhang; Wen-Xia Li; Wen-Wen Li; Lian Wang; Xiao-Long Mo; Hong Wei; Ping Ji; Peng Xie

doi:10.24272/j.issn.2095-8137.2023.008

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Hai-Yang Wang, Lan-Xiang Liu, Xue-Yi Chen, Yang-Dong Zhang, Wen-Xia Li, Wen-Wen Li, Lian Wang, Xiao-Long Mo, Hong Wei, Ping Ji, Peng Xie. Comprehensive analysis of the gut microbiome and post-translational modifications elucidates the route involved in microbiota-host interactions. Zoological Research, 2024, 45(1): 95-107. doi: 10.24272/j.issn.2095-8137.2023.008

Citation:

Hai-Yang Wang, Lan-Xiang Liu, Xue-Yi Chen, Yang-Dong Zhang, Wen-Xia Li, Wen-Wen Li, Lian Wang, Xiao-Long Mo, Hong Wei, Ping Ji, Peng Xie. Comprehensive analysis of the gut microbiome and post-translational modifications elucidates the route involved in microbiota-host interactions. Zoological Research, 2024, 45(1): 95-107. doi: 10.24272/j.issn.2095-8137.2023.008

Citation:

Hai-Yang Wang, Lan-Xiang Liu, Xue-Yi Chen, Yang-Dong Zhang, Wen-Xia Li, Wen-Wen Li, Lian Wang, Xiao-Long Mo, Hong Wei, Ping Ji, Peng Xie. Comprehensive analysis of the gut microbiome and post-translational modifications elucidates the route involved in microbiota-host interactions. Zoological Research, 2024, 45(1): 95-107. doi: 10.24272/j.issn.2095-8137.2023.008

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Comprehensive analysis of the gut microbiome and post-translational modifications elucidates the route involved in microbiota-host interactions

doi: 10.24272/j.issn.2095-8137.2023.008

Hai-Yang Wang^{1, 2, 3, #},
Lan-Xiang Liu^{4, #},
Xue-Yi Chen^{5, #},
Yang-Dong Zhang^{6, #},
Wen-Xia Li¹,
Wen-Wen Li⁵,
Lian Wang¹,
Xiao-Long Mo^{1, 6},
Hong Wei^{7
,
,},
Ping Ji^{2, 3
,
,},
Peng Xie^{1, 2, 6
,
,}

1.
NHC Key Laboratory of Diagnosis and Treatment on Brain Functional Diseases, First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
2.
College of Stomatology and Affiliated Stomatological Hospital of Chongqing Medical University, Chongqing 401147, China
3.
Chongqing Key Laboratory for Oral Diseases and Biomedical Sciences, Chongqing 401147, China
4.
Department of Neurology, Yongchuan Hospital of Chongqing Medical University, Chongqing 402160, China
5.
Department of Pathology, Faculty of Basic Medicine, Chongqing Medical University, Chongqing 400016, China
6.
Department of Neurology, First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China
7.
Yu-Yue Pathology Scientific Research Center, Chongqing 401329, China

The raw metagenomics sequencing reads can be downloaded from the NCBI (PRJNA1003305), China National Center for Bioinformation (PRJCA018916), and Science Data Bank databases (DOI: 10.57760/sciencedb.j00139.00058).
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
H.W., P.J., and P.X. conceived and designed the study, H.Y.W. and L.X.L. wrote the manuscript, X.Y.C. and Y.D.Z. analyzed the data, W.W.L., W.X.L., L.W., and X.L.M. revised the manuscript. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work

Funds: This work was supported by the Natural Science Foundation Project of China (81820108015, 82201683), China Postdoctoral Science Foundation (2021M693926, 2020TQ0393, 2020M683634XB), Chongqing Science & Technology Commission (cstc2021jcyj-bshX0150, cstc2021jcyj-bshX0201), and Special Funding for Chongqing Postdoctoral Research Projects (2021XMT001)

More Information

Corresponding author: E-mail: Weihong63528@163.com; jiping@hospital.cqmu.edu.cn; xiepeng@cqmu.edu.cn
Received Date: 2023-04-06
Accepted Date: 2023-04-21

Published Online: 2023-09-09

Abstract

Abstract

The gut microbiome interacts with the host to maintain body homeostasis, with gut microbial dysbiosis implicated in many diseases. However, the underlying mechanisms of gut microbe regulation of host behavior and brain functions remain unclear. This study aimed to elucidate the influence of gut microbiota on brain functions via post-translational modification mechanisms in the presence or absence of bacteria without any stimulation. We conducted succinylome analysis of hippocampal proteins in germ-free (GF) and specific pathogen-free (SPF) mice and metagenomic analysis of feces from SPF mice. These results were integrated with previously reported hippocampal acetylome and phosphorylome data from the same batch of mice. Subsequent bioinformatics analyses revealed 584 succinylation sites on 455 proteins, including 54 up-regulated succinylation sites on 91 proteins and 99 down-regulated sites on 51 proteins in the GF mice compared to the SPF mice. We constructed a panoramic map of gut microbiota-regulated succinylation, acetylation, and phosphorylation, and identified cross-talk and relative independence between the different types of post-translational modifications in modulating complicated intracellular pathways. Pearson correlation analysis indicated that 13 taxa, predominantly belonging to the Bacteroidetes phylum, were correlated with the biological functions of post-translational modifications. Positive correlations between these taxa and succinylation and negative correlations between these taxa and acetylation were identified in the modulation of intracellular pathways. This study highlights the hippocampal physiological changes induced by the absence of gut microbiota, and proteomic quantification of succinylation, phosphorylation, and acetylation, contributing to our understanding of the role of the gut microbiome in brain function and behavioral phenotypes.
- Gut microbiota,
- Hippocampal protein,
- Post-translational modifications,
- Succinylation,
- Acetylation,
- Phosphorylation

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References(70)

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