Temporal dynamics of gut microbiomes in non-industrialized urban Amazonia.

Eric J Alm, Mathieu Groussin, Mathilde Poyet, Ana Paula Schaan, Amanda Vidal, An-Ni Zhang, Ândrea Ribeiro-Dos-Santos

Journal: mSystems 2024;9(3):e0070723

PMID: 38376180

Abstract

Increasing levels of industrialization have been associated with changes in gut microbiome structure and loss of features thought to be crucial for maintaining gut ecological balance. The stability of gut microbial communities over time within individuals seems to be largely affected by these changes but has been overlooked among transitioning populations from low- to middle-income countries. Here, we used metagenomic sequencing to characterize the temporal dynamics in gut microbiomes of 24 individuals living an urban non-industrialized lifestyle in the Brazilian Amazon. We further contextualized our data with 165 matching longitudinal samples from an urban industrialized and a rural non-industrialized population. We show that gut microbiome composition and diversity have greater variability over time among non-industrialized individuals when compared to industrialized counterparts and that taxa may present diverse temporal dynamics across human populations. Enterotype classifications show that community types are generally stable over time despite shifts in microbiome structure. Furthermore, by tracking genomes over time, we show that levels of bacterial population replacements are more frequent among Amazonian individuals and that non-synonymous variants accumulate in genes associated with degradation of host dietary polysaccharides. Taken together, our results suggest that the stability of gut microbiomes is influenced by levels of industrialization and that tracking microbial population dynamics is important to understand how the microbiome will adapt to these transitions.IMPORTANCEThe transition from a rural or non-industrialized lifestyle to urbanization and industrialization has been linked to changes in the structure and function of the human gut microbiome. Understanding how the gut microbiomes changes over time is crucial to define healthy states and to grasp how the gut microbiome interacts with the host environment. Here, we investigate the temporal dynamics of gut microbiomes from an urban and non-industrialized population in the Amazon, as well as metagenomic data sets from urban United States and rural Tanzania. We showed that healthy non-industrialized microbiomes experience greater compositional shifts over time compared to industrialized individuals. Furthermore, bacterial strain populations are more frequently replaced in non-industrialized microbiomes, and most non-synonymous mutations accumulate in genes associated with the degradation of host dietary components. This indicates that microbiome stability is affected by transitions to industrialization, and that strain tracking can elucidate the ecological dynamics behind such transitions.

Address: Genetics and Molecular Biology Program, Universidade Federal do Pará, Belém, Pará, Brazil.; Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.; Schleswig-Holstein University Clinic, Kiel, Germany.; Instituto Tecnológico Vale, Belém, Pará, Brazil.; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Schleswig-Holstein University Clinic, Kiel, Germany.; Instituto Tecnológico Vale, Belém, Pará, Brazil.; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Institute of Experimental Medicine, Christian-Albrecht University of Kiel, Kiel, Germany.; The Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; The Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.; Institute of Clinical Molecular Biology, Christian-Albrecht University of Kiel, Kiel, Germany.; Schleswig-Holstein University Clinic, Kiel, Germany.; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; The Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.; The Global Microbiome Conservancy, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.; Genetics and Molecular Biology Program, Universidade Federal do Pará, Belém, Pará, Brazil.; Center for Oncology Research, Universidade Federal do Pará, Belém, Pará, Brazil.

DOI: 10.1128/msystems.00707-23

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MeSH Terms: Humans, Gastrointestinal Microbiome, Brazil, Microbiota, Bacteria, Urbanization