Published May 9, 2023 | Version v1
Journal article Open

Universal gut microbial relationships in the gut microbiome of wild baboons

  • 1. Duke University
  • 2. University of Groningen
  • 3. University of Notre Dame
  • 4. University of British Columbia-Okanagan Campus
  • 5. University of Minnesota
  • 6. University of Chicago
  • 7. University of California, San Diego

Description

Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships is essential to learn how ecology scales up to affect microbiome assembly, dynamics, and host health. However, whether bacterial relationships are generalizable across hosts or personalized to individual hosts is debated. Here, we apply a robust, multinomial logistic-normal modeling framework to extensive time series data (5534 samples from 56 baboon hosts over 13 years) to infer thousands of correlations in bacterial abundance in individual baboons and test the degree to which bacterial abundance correlations are 'universal'. We also compare these patterns to two human data sets. We find that, most bacterial correlations are weak, negative, and universal across hosts, such that shared correlation patterns dominate over host-specific correlations by almost twofold. Further, taxon pairs that had inconsistent correlation signs (either positive or negative) in different hosts always had weak correlations within hosts. From the host perspective, host pairs with the most similar bacterial correlation patterns also had similar microbiome taxonomic compositions and tended to be genetic relatives. Compared to humans, universality in baboons was similar to that in human infants, and stronger than one data set from human adults. Bacterial families that showed universal correlations in human infants were often universal in baboons. Together, our work contributes new tools for analyzing the universality of bacterial associations across hosts, with implications for microbiome personalization, community assembly, and stability, and for designing microbiome interventions to improve host health.

Data availability

16S rRNA gene sequences are available on EBI-ENA (project 590 ERP119849) and Qiita (study 12949). Analyzed data and code are available on GitHub at: https://github.com/kimberlyroche/rulesoflife

The following data sets were generated:
University of California San Diego Microbiome Initiative (2021) European Nucleotide Archive ID ERP119849. 16S rRNA gene sequencing data from baboon gut microbiomes collected between 2000 and 2014.
https://www.ebi.ac.uk/ena/browser/view/ERP119849
Grieneisen L Dasari M Gould TJ Björk JR Grenier J Yotova V Jansen D Gottel N Gordon JB Learn NH Gesquiere LR Wango TL Mututua RS Warutere JK Siodi L Gilbert JA Barreiro LB Alberts SC Tung J Archie EA Blekhman R (2021) Qiita ID 12949. Gut microbiome heritability is nearly universal but environmentally contingent.
https://qiita.ucsd.edu/public/?study_id=12949

The following previously published data sets were used :
Vatanen T Kostic A d'Hennezel E (2016) NCBI BioProject ID PRJNA290380. DIABIMMUNE three country cohort. https://www.ncbi.nlm.nih.gov/bioproject/PRJNA290380
Johnson AJ (2019) European Nucleotide Archive ID PRJEB29065. Johnson et al. dietary cohort.
https://www.ebi.ac.uk/ena/browser/view/PRJEB29065

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Additional details

Identifiers

DOI
10.7554/eLife.83152
Other
oai:uchicago.tind.io:6622

Funding

National Science Foundation
DEB1840223
National Institute on Aging
R01AG071684
National Institute on Aging
R21AG055777
National Institute on Aging
R01AG053330
National Institute of General Medical Sciences
R35GM128716
Duke University
Population Research Institute
University of Notre Dame
Eck Institute for Global Health
Notre Dame Environmental Change Initiative
National Science Foundation
IOS 1456832
National Science Foundation
IOS 1053461
National Science Foundation
DEB 1405308
National Science Foundation
DEB 0846532
National Science Foundation
IBN 0322781
National Science Foundation
IBN 0322613
National Science Foundation
BCS 0323553
National Science Foundation
BCS 0323596
National Institutes of Health
P01AG031719
National Institutes of Health
R21AG049936
National Institutes of Health
R03AG045459
National Institutes of Health
R01HD088558
National Institutes of Health
P30AG024361

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Genetics, Genomics, and Systems Biology, Immunology, Medicine