skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.
Attention:The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 7:00 AM ET to 7:30 AM ET on Friday, April 24 due to maintenance. We apologize for the inconvenience.


Title: Gene-specific selective sweeps are pervasive across human gut microbiomes
Abstract The human gut microbiome is composed of a highly diverse consortia of species that are continually evolving within and across hosts1,2. The ability to identify adaptations common to many human gut microbiomes would show not only shared selection pressures across hosts but also key drivers of functional differentiation of the microbiome that may affect community structure and host traits. However, the extent to which adaptations have spread across human gut microbiomes is relatively unknown. Here we develop a new selection scan statistic named the integrated linkage disequilibrium score (iLDS) that can detect sweeps of adaptive alleles spreading across host microbiomes by migration and horizontal gene transfer. Specifically, iLDS leverages signals of hitchhiking of deleterious variants with a beneficial variant. Application of the statistic to around 30 of the most prevalent commensal gut species from 24 human populations around the world showed more than 300 selective sweeps across species. We find an enrichment for selective sweeps at loci involved in carbohydrate metabolism, indicative of adaptation to host diet, and we find that the targets of selection differ significantly between industrialized populations and non-industrialized populations. One of these sweeps is at a locus known to be involved in the metabolism of maltodextrin—a synthetic starch that has recently become a widespread component of industrialized diets. In summary, our results indicate that recombination between strains fuels pervasive adaptive evolution among human gut commensal bacteria, and strongly implicate host diet and lifestyle as critical selection pressures.  more » « less
Award ID(s):
2240098
PAR ID:
10654869
Author(s) / Creator(s):
;
Publisher / Repository:
Nature
Date Published:
Journal Name:
Nature
ISSN:
0028-0836
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype. 
    more » « less
  2. Diet selection is a fundamental aspect of animal behavior with numerous ecological and evolutionary implications. While the underlying mechanisms are complex, the availability of essential dietary nutrients can strongly influence diet selection behavior. The gut microbiome has been shown to metabolize many of these same nutrients, leading to the untested hypothesis that intestinal microbiota may influence diet selection. Here, we show that germ-free mice colonized by gut microbiota from three rodent species with distinct foraging strategies differentially selected diets that varied in macronutrient composition. Specifically, we found that herbivore-conventionalized mice voluntarily selected a higher protein:carbohydrate (P:C) ratio diet, while omnivore- and carnivore-conventionalized mice selected a lower P:C ratio diet. In support of the long-standing hypothesis that tryptophan—the essential amino acid precursor of serotonin—serves as a peripheral signal regulating diet selection, bacterial genes involved in tryptophan metabolism and plasma tryptophan availability prior to the selection trial were significantly correlated with subsequent voluntary carbohydrate intake. Finally, herbivore-conventionalized mice exhibited larger intestinal compartments associated with microbial fermentation, broadly reflecting the intestinal morphology of their donor species. Together, these results demonstrate that gut microbiome can influence host diet selection behavior, perhaps by mediating the availability of essential amino acids, thereby revealing a mechanism by which the gut microbiota can influence host foraging behavior. 
    more » « less
  3. Kormas, Konstantinos Aristomenis (Ed.)
    ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution. 
    more » « less
  4. null (Ed.)
    Freshwater mussels perform essential ecosystem functions, yet we have no information on how their microbiomes fluctuate over time. In this study, we examined temporal variation in the microbiome of six mussel species (Lampsilis ornata, Obovaria unicolor, Elliptio arca, Fusconaia cerina, Cyclonaias asperata, and Tritogonia verrucosa) sampled from the same river in 2016 and 2019. We examined the taxonomic, phylogenetic, and inferred functional (from 16S rRNA sequences) facets of their microbiome diversity. Significant differences between the two years were identified in five of the six species sampled. However, not all species that exhibited a temporally variable microbiome were functionally distinct across years, indicating functional redundancy within the mussel gut microbiome. Inferred biosynthesis pathways showed temporal variation in pathways involved in degradation, while pathways involved in cellular metabolism were stable. There was no evidence for phylosymbiosis across any facet of microbiome biodiversity. These results indicate that temporal variation is an important factor in the assembly of the gut microbiomes of freshwater mussels and provides further support that the mussel gut microbiome is involved in host development and activity. 
    more » « less
  5. ABSTRACT Organisms inhabiting extreme environments must tolerate a variety of physiochemical stressors. In some cases, host‐associated microbial communities facilitate the survival of their hosts in extreme environments, but extremophile symbioses have not been identified in vertebrates. We used 16S rRNA amplicon sequencing to investigate commonalities and differences in the gut bacterial communities of livebearing fishes (Poecilia mexicanaspecies complex, Poeciliidae) that have repeatedly colonised toxic sulfide streams in southern Mexico. We found shared gut microbial taxa across habitat types and drainages but also differences in the microbiomes between sulfidic and nonsulfidic populations, both in terms of patterns of diversity and community composition. Most importantly, we documented convergent changes in microbiome composition across evolutionarily independent sulfide spring lineages. These patterns were consistent when we analysed the gut microbiomes as well as primarily host‐associated microbiomes that excluded taxa that are commonly found in the environment. Our analyses also revealed several microbial taxa associated with sulfide spring coloniation that have previously been implicated in symbioses and may influence the host's tolerance to the extreme environmental conditions. Our study sheds light on how shared environmental pressures can give rise to convergent host‐microbiome associations in fishes, and it provides a foundation for investigating the role of host‐microbiome interactions in vertebrate adaptation to extreme environments. 
    more » « less