Microbiome and Human Health: Current Understanding, Engineering, and Enabling Technologies

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Abstract

The human microbiome is composed of a collection of dynamic microbial communities that inhabit various anatomical locations in the body. Accordingly, the coevolution of the microbiome with the host has resulted in these communities playing a profound role in promoting human health. Consequently, perturbations in the human microbiome can cause or exacerbate several diseases. In this Review, we present our current understanding of the relationship between human health and disease development, focusing on the microbiomes found across the digestive, respiratory, urinary, and reproductive systems as well as the skin. We further discuss various strategies by which the composition and function of the human microbiome can be modulated to exert a therapeutic effect on the host. Finally, we examine technologies such as multiomics approaches and cellular reprogramming of microbes that can enable significant advancements in microbiome research and engineering.

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An obesity-associated gut microbiome with increased capacity for energy harvest.

Peter J Turnbaugh, Ruth E Ley, Michael A Mahowald … (2006)

The worldwide obesity epidemic is stimulating efforts to identify host and environmental factors that affect energy balance. Comparisons of the distal gut microbiota of genetically obese mice and their lean littermates, as well as those of obese and lean human volunteers have revealed that obesity is associated with changes in the relative abundance of the two dominant bacterial divisions, the Bacteroidetes and the Firmicutes. Here we demonstrate through metagenomic and biochemical analyses that these changes affect the metabolic potential of the mouse gut microbiota. Our results indicate that the obese microbiome has an increased capacity to harvest energy from the diet. Furthermore, this trait is transmissible: colonization of germ-free mice with an 'obese microbiota' results in a significantly greater increase in total body fat than colonization with a 'lean microbiota'. These results identify the gut microbiota as an additional contributing factor to the pathophysiology of obesity.

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Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors

Bo Qu, Gladys Ferrere, Céline Clemenson … (2018)

Immune checkpoint inhibitors (ICI) targeting the PD-1/PD-L1 axis induce sustained clinical responses in a sizeable minority of cancer patients. Here, we show that primary resistance to ICI can be due to abnormal gut microbiome composition. Antibiotics (ATB) inhibited the clinical benefit of ICI in patients with advanced cancer. Fecal microbiota transplantation (FMT) from cancer patients who responded to ICI (but not from non-responding patients) into germ-free or ATB-treated mice ameliorated the antitumor effects of PD-1 blockade. Metagenomics of patient stools at diagnosis revealed correlations between clinical responses to ICI and the relative abundance of Akkermansia muciniphila. Oral supplementation with A. muciniphila post-FMT with non-responder feces restored the efficacy of PD-1 blockade in an IL-12-dependent manner, by increasing the recruitment of CCR9+CXCR3+CD4+ T lymphocytes into tumor beds.

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Human gut microbiome viewed across age and geography

Tanya Yatsunenko, Federico E Rey, Mark Manary … (2012)

Gut microbial communities represent one source of human genetic and metabolic diversity. To examine how gut microbiomes differ between human populations when viewed from the perspective of component microbial lineages, encoded metabolic functions, stage of postnatal development, and environmental exposures, we characterized bacterial species present in fecal samples obtained from 531 individuals representing healthy Amerindians from the Amazonas of Venezuela, residents of rural Malawian communities, and inhabitants of USA metropolitan areas, as well as the gene content of 110 of their microbiomes. This cohort encompassed infants, children, teenagers and adults, parents and offspring, and included mono- and dizygotic twins. Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the representation of genes involved in vitamin biosynthesis and metabolism. Pronounced differences in bacterial species assemblages and functional gene repertoires were noted between individuals residing in the USA compared to the other two countries. These distinctive features are evident in early infancy as well as adulthood. In addition, the similarity of fecal microbiomes among family members extends across cultures. These findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations, and the impact of Westernization.

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Author and article information

Journal

Journal ID (nlm-ta): Chem Rev

Journal ID (iso-abbrev): Chem Rev

Journal ID (publisher-id): cr

Journal ID (coden): chreay

Title: Chemical Reviews

Publisher: American Chemical Society

ISSN (Print): 0009-2665

ISSN (Electronic): 1520-6890

Publication date (Electronic): 01 November 2022

Publication date Collection: 11 January 2023

Volume: 123

Issue: 1

Pages: 31-72

Affiliations

[† ]NUS Synthetic Biology for Clinical and Technological Innovation (SynCTI), National University of Singapore , Singapore 117456, Singapore

[‡ ]Synthetic Biology Translational Research Programme, Yong Loo Lin School of Medicine, National University of Singapore , Singapore 117456, Singapore

[§ ]Wilmar-NUS (WIL@NUS) Corporate Laboratory, National University of Singapore , Singapore 117599, Singapore

[∥ ]Wilmar International Limited , Singapore 138568, Singapore

[⊥ ]Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore , Singapore 117596, Singapore

[# ]Singapore Institute of Technology , Singapore 138683, Singapore

Author notes

[* ]E-mail: bchcmw@ 123456nus.edu.sg .

Author information

Sandra Kittelmann https://orcid.org/0000-0002-6019-9854

Matthew Wook Chang https://orcid.org/0000-0001-6448-6319

Article

DOI: 10.1021/acs.chemrev.2c00431

PMC ID: 9837825

PubMed ID: 36317983

SO-VID: 792ff537-e665-46c2-9ca7-b7174afb918a

License:

Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained ( https://creativecommons.org/licenses/by/4.0/).

History

Date received : 22 June 2022

Funding

Funded by: U.S. Department of Defense, doi 10.13039/100000181;

Award ID: FA2386-18-1- 4058

Funded by: Ministry of Education - Singapore, doi 10.13039/501100001459;

Award ID: NUHSRO/2020/046/T1/3

Funded by: Economic Development Board - Singapore, doi 10.13039/501100001446;

Award ID: S18-139S-IPP-1I

Funded by: National Research Foundation Singapore, doi 10.13039/501100001381;

Award ID: NRF2019-NRF-ISF003-3208

Funded by: National Research Foundation Singapore, doi 10.13039/501100001381;

Award ID: NRF-NRFI05-2019-0004

Funded by: National University of Singapore, doi 10.13039/501100001352;

Award ID: NUHSRO/2020/077/MSC/02/SB

Funded by: National University of Singapore, doi 10.13039/501100001352;

Award ID: NUHSRO/2016/053/SRP/05

Funded by: National University of Singapore, doi 10.13039/501100001352;

Award ID: DPRT/943/09/14

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document-id-new-14 cr2c00431

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ScienceOpen disciplines: Chemistry

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Most cited references 475

An obesity-associated gut microbiome with increased capacity for energy harvest.

Gut microbiome influences efficacy of PD-1–based immunotherapy against epithelial tumors

Human gut microbiome viewed across age and geography

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Cited by 70

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