Review

Vulnerability of the industrialized microbiota

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Science  25 Oct 2019:
Vol. 366, Issue 6464, eaaw9255
DOI: 10.1126/science.aaw9255

Figures

  • Industrialization affects the human gut microbiota.

    Aspects of lifestyle, including those associated with industrialization, such as processed foods, infant formula, modern medicines, and sanitation, can change the gut microbiota. Major questions include whether microbiota changes associated with industrialization are important for human health, if they are reversible, and what steps should be taken to prevent further change while information is acquired to enable an informed cost-versus-benefit analysis. It is possible that a diet rich in whole foods and low in processed foods, along with increased exposure to nonpathogenic microbes, may be beneficial to industrial populations.

    ILLUSTRATION: KELLIE HOLOSKI/SCIENCE
  • Fig. 1 The gut microbiota mirrors lifestyle across traditional and industrial populations.

    (A) Aggregation of gut microbiota composition from multiple studies separated by principal component analysis of Bray–Curtis dissimilarity of 16S rRNA enumerations [adapted from Smits et al. (33)]. Top panel: The first principal component explains 22% of the variation in the data from 18 populations living lifestyles spanning from uncontacted Amerindians in Venezuela (top) to fully industrialized populations in Australia, the United States, Canada, and Ireland (bottom). Bottom panel: Mapping the relative abundance of bacterial families on PCo1 reveals global patterns in the VANISH taxa, which are associated negatively with industrialized societies, and BloSSUM taxa (bloom or selected in societies of urbanization/modernization), such as the Bacteroidaceae and Verrucomicrobia. (B) Heat map adapted from Jha et al. (31) displaying taxa that change across lifestyles in one geographic location (Nepal) of individuals living as foragers (Chepang), settled foragers (Raute, Raji), or agriculturalists (Tharu) versus industrialized individuals in the United States. (C) Model adapted from Jha et al. (31) of strain loss and/or reduction versus gain and/or increase across a lifestyle gradient. Different patterns of changing abundance correspond with specific aspects of lifestyle that change as populations move away from foraging and toward urbanization. The model could also reflect the historical progression of industrialized humans from foraging (Homo sapiens arose ~200,000 to 300,000 years ago) to agriculture (starting 10,000 to 20,000 years ago) to industrialization (starting 100 to 200 years ago).

  • Fig. 2 Interaction networks in Yellowstone and the gut microbiota.

    (A) Gray wolves were introduced into Yellowstone National Park in 1995 to control the swelling elk population (105). The rewilding of Yellowstone set off a trophic cascade that resulted in a decreasing elk population (thereby promoting new growth in aspens), an increase in berries available to bears, and stream morphology changes caused by increased woody plants (64). This provides an example of how wildlife management can be used to restore a more diverse and perhaps functional ecosystem, as well as how reintroduction of species into a habitat can lead to unanticipated changes to that ecosystem. (B) Rewilding of a C. difficile–infected microbiota by FMT results in largely predictable outcomes in host health, but the specifics of the resulting microbiota composition are difficult to predict. (C) Long-term strategies for managing the microbiota include precision approaches of adding defined cocktails of microbes, engineered bacterial species, and improving ecosystem habitat quality. For example, increasing dietary MACs encourages commensal growth and provides fermentation end products such as butyrate to the epithelium, which can help keep oxygen tensions lower in the gut and prevent the growth of facultative anaerobes with pathogenic potential (106).

  • Fig. 3 Ecosystem services of the gut microbiota.

    Identifying the benefits provided by the gut microbiome to human health is one way to determine when the ecosystem is functioning well. (A) List of benefits provided by the gut microbiota. This list is not intended to be comprehensive, and the categorization is only one of many possibilities, but it is presented as a potentially useful framework for conceptualizing how to value specific features of microbiota. (B) Current data suggest that, along with the shift in the composition of the industrialized microbiota, certain services may be lost or out of balance, resulting in suboptimal states of host physiology or disease. A more nuanced understanding of which services are beneficial and in what context will be enabled by longitudinal high-dimensional profiling of microbiome and host biology combined with long-term monitoring of health in humans.

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