Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures

doi:10.1038/s43587-023-00389-y

. 2023 Apr;3(4):436-449.

doi: 10.1038/s43587-023-00389-y. Epub 2023 Apr 6.

Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures

Shifu Pang^#¹, Xiaodong Chen^#^{1

2}, Zhilong Lu³, Lili Meng¹, Yu Huang¹, Xiuqi Yu¹, Lianfei Huang^{1

4}, Pengpeng Ye¹, Xiaochun Chen¹, Jian Liang⁵, Tao Peng⁶, Weifei Luo^{7

8

9}, Shuai Wang^{10

11}

Affiliations

¹ AIage Life Science Corporation Ltd., Guangxi Free Trade Zone Aisheng Biotechnology Corporation Ltd., Nanning, China.
² The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China.
³ State Key Laboratory of Non-food Biomass and Enzyme Technology, Guangxi Academy of Sciences, Nanning, China.
⁴ State Key Laboratory of Veterinary Etiological Biology, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China.
⁵ Medical College, Guangxi University, Nanning, China.
⁶ Guangxi Key Laboratory of Enhanced Recovery after Surgery for Gastrointestinal Cancer, Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning, China.
⁷ AIage Life Science Corporation Ltd., Guangxi Free Trade Zone Aisheng Biotechnology Corporation Ltd., Nanning, China. [email protected].
⁸ The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China. [email protected].
⁹ State Key Laboratory of Non-food Biomass and Enzyme Technology, Guangxi Academy of Sciences, Nanning, China. [email protected].
¹⁰ The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China. [email protected].
¹¹ State Key Laboratory of Veterinary Etiological Biology, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China. [email protected].

^# Contributed equally.

PMID: 37117794
DOI: 10.1038/s43587-023-00389-y

Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures

Shifu Pang et al. Nat Aging. 2023 Apr.

. 2023 Apr;3(4):436-449.

doi: 10.1038/s43587-023-00389-y. Epub 2023 Apr 6.

Authors

Affiliations

¹ AIage Life Science Corporation Ltd., Guangxi Free Trade Zone Aisheng Biotechnology Corporation Ltd., Nanning, China.
² The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China.
³ State Key Laboratory of Non-food Biomass and Enzyme Technology, Guangxi Academy of Sciences, Nanning, China.
⁴ State Key Laboratory of Veterinary Etiological Biology, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China.
⁵ Medical College, Guangxi University, Nanning, China.
⁶ Guangxi Key Laboratory of Enhanced Recovery after Surgery for Gastrointestinal Cancer, Department of Hepatobiliary Surgery, The First Affiliated Hospital of Guangxi Medical University, Nanning, China.
⁷ AIage Life Science Corporation Ltd., Guangxi Free Trade Zone Aisheng Biotechnology Corporation Ltd., Nanning, China. [email protected].
⁸ The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China. [email protected].
⁹ State Key Laboratory of Non-food Biomass and Enzyme Technology, Guangxi Academy of Sciences, Nanning, China. [email protected].
¹⁰ The Grand Health Industry Research Institute, Guangxi Academy of Sciences, Nanning, China. [email protected].
¹¹ State Key Laboratory of Veterinary Etiological Biology, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China. [email protected].

^# Contributed equally.

PMID: 37117794
DOI: 10.1038/s43587-023-00389-y

Abstract

Centenarians are an excellent model to study the relationship between the gut microbiome and longevity. To characterize the gut microbiome signatures of aging, we conducted a cross-sectional investigation of 1,575 individuals (20-117 years) from Guangxi province of China, including 297 centenarians (n = 45 with longitudinal sampling). Compared to their old adult counterparts, centenarians displayed youth-associated features in the gut microbiome characterized by an over-representation of a Bacteroides-dominated enterotype, increase in species evenness, enrichment of potentially beneficial Bacteroidetes and depletion of potential pathobionts. Health status stratification in older individuals did not alter the directional trends for these signature comparisons but revealed more apparent associations in less healthy individuals. Importantly, longitudinal analysis of centenarians across a 1.5-year period indicated that the youth-associated gut microbial signatures were enhanced with regard to increased evenness, reduction in interindividual variation and stability of Bacteroides, and that centenarians with low microbial evenness were prone to large microbiome instability during aging. These results together highlight a youth-related aging pattern of the gut microbiome for long-lived individuals.

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References

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[1] Dato, S. et al. The genetics of human longevity: an intricacy of genes, environment, culture and microbiome. Mech. Ageing Dev. 165, 147–155 (2017). - PubMed - DOI

[2] Dato, S. et al. The genetics of human longevity: an intricacy of genes, environment, culture and microbiome. Mech. Ageing Dev. 165, 147–155 (2017). - PubMed - DOI

[3] Cani, P. D. Human gut microbiome: hopes, threats and promises. Gut 67, 1716–1725 (2018). - PubMed - DOI

[4] Cani, P. D. Human gut microbiome: hopes, threats and promises. Gut 67, 1716–1725 (2018). - PubMed - DOI

[5] de Vos, W. M., Tilg, H., Van Hul, M. & Cani, P. D. Gut microbiome and health: mechanistic insights. Gut 71, 1020–1032 (2022). - PubMed - DOI

[6] de Vos, W. M., Tilg, H., Van Hul, M. & Cani, P. D. Gut microbiome and health: mechanistic insights. Gut 71, 1020–1032 (2022). - PubMed - DOI

[7] DeJong, E. N., Surette, M. G. & Bowdish, D. M. E. The gut microbiota and unhealthy aging: disentangling cause from consequence. Cell Host Microbe 28, 180–189 (2020). - PubMed - DOI

[8] DeJong, E. N., Surette, M. G. & Bowdish, D. M. E. The gut microbiota and unhealthy aging: disentangling cause from consequence. Cell Host Microbe 28, 180–189 (2020). - PubMed - DOI

[9] Kim, S. & Jazwinski, S. M. The gut microbiota and healthy aging: a mini-review. Gerontology 64, 513–520 (2018). - PubMed - DOI

[10] Kim, S. & Jazwinski, S. M. The gut microbiota and healthy aging: a mini-review. Gerontology 64, 513–520 (2018). - PubMed - DOI

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Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures

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Longevity of centenarians is reflected by the gut microbiome with youth-associated signatures

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