Human microbiome variation is linked to the incidence, prevalence, and mortality of many diseases and associates with race and ethnicity in the United States. However, the age at which microbiome ...variability emerges between these groups remains a central gap in knowledge. Here, we identify that gut microbiome variation associated with race and ethnicity arises after 3 months of age and persists through childhood. One-third of the bacterial taxa that vary across caregiver-identified racial categories in children are taxa reported to also vary between adults. Machine learning modeling of childhood microbiomes from 8 cohort studies (2,756 samples from 729 children) distinguishes racial and ethnic categories with 87% accuracy. Importantly, predictive genera are also among the top 30 most important taxa when childhood microbiomes are used to predict adult self-identified race and ethnicity. Our results highlight a critical developmental window at or shortly after 3 months of age when social and environmental factors drive race and ethnicity-associated microbiome variation and may contribute to adult health and health disparities.
Mammalian gut microbial communities are frequently found to be host‐specific—microbial community compositions are more similar within than between host species—and some individual microbial taxa ...consistently associate with a single or small set of host species. The ecoevolutionary dynamics that result in this pattern of phylosymbiosis or host specificity have been proposed, but robust tests of the mechanisms driving these relationships are lacking. In this issue of Molecular Ecology, Mazel et al. (2023) combine large amplicon sequencing data sets with bacterial phenotypic traits to test whether microbial dispersal patterns contribute to the host specificity of the gut microbiome. They find that both transmission mode and oxygen tolerance are predictive of how specialized a microbe is. Horizontally transmitted, oxygen‐tolerant microbes are more likely to be generalists, and vertically transmitted anaerobes are more likely to be limited to a few host species. This creative use of publicly available data provides a roadmap for testing hypotheses about the mechanisms underlying phylosymbiosis.
Host specificity of the gut microbiome Mallott, Elizabeth K; Amato, Katherine R
Nature reviews. Microbiology,
10/2021, Letnik:
19, Številka:
10
Journal Article
Recenzirano
Developing general principles of host-microorganism interactions necessitates a robust understanding of the eco-evolutionary processes that structure microbiota. Phylosymbiosis, or patterns of ...microbiome composition that can be predicted by host phylogeny, is a unique framework for interrogating these processes. Identifying the contexts in which phylosymbiosis does and does not occur facilitates an evaluation of the relative importance of different ecological processes in shaping the microbial community. In this Review, we summarize the prevalence of phylosymbiosis across the animal kingdom on the basis of the current literature and explore the microbial community assembly processes and related host traits that contribute to phylosymbiosis. We find that phylosymbiosis is less prevalent in taxonomically richer microbiomes and hypothesize that this pattern is a result of increased stochasticity in the assembly of complex microbial communities. We also note that despite hosting rich microbiomes, mammals commonly exhibit phylosymbiosis. We hypothesize that this pattern is a result of a unique combination of mammalian traits, including viviparous birth, lactation and the co-evolution of haemochorial placentas and the eutherian immune system, which compound to ensure deterministic microbial community assembly. Examining both the individual and the combined importance of these traits in driving phylosymbiosis provides a new framework for research in this area moving forward.
Many diseases linked with ethnic health disparities associate with changes in microbial communities in the United States, but the causes and persistence of ethnicity-associated microbiome variation ...are not understood. For instance, microbiome studies that strictly control for diet across ethnically diverse populations are lacking. Here, we performed multiomic profiling over a 9-day period that included a 4-day controlled vegetarian diet intervention in a defined geographic location across 36 healthy Black and White females of similar age, weight, habitual diets, and health status. We demonstrate that individuality and ethnicity account for roughly 70% to 88% and 2% to 10% of taxonomic variation, respectively, eclipsing the effects a short-term diet intervention in shaping gut and oral microbiomes and gut viromes. Persistent variation between ethnicities occurs for microbial and viral taxa and various metagenomic functions, including several gut KEGG orthologs, oral carbohydrate active enzyme categories, cluster of orthologous groups of proteins, and antibiotic-resistant gene categories. In contrast to the gut and oral microbiome data, the urine and plasma metabolites tend to decouple from ethnicity and more strongly associate with diet. These longitudinal, multiomic profiles paired with a dietary intervention illuminate previously unrecognized associations of ethnicity with metagenomic and viromic features across body sites and cohorts within a single geographic location, highlighting the importance of accounting for human microbiome variation in research, health determinants, and eventual therapies. Trial Registration: ClinicalTrials.gov ClinicalTrials.gov Identifier: NCT03314194.
DNA metabarcoding is a powerful tool for assessing the diets of wild animals, but there is no clear consensus on which proposed plant barcoding marker is most suitable for dietary analysis. This ...study compares two DNA plant barcoding markers that are commonly used for dietary analyses from degraded DNA, rbcL and trnL, to detailed dietary observations of wild white-faced capuchins (Cebus capucinus). Observational dietary data and fecal samples (n = 170) were collected for one year from a group of individually recognizable monkeys at La Suerte Biological Field Station, Costa Rica. DNA was extracted and portions of the rbcL and trnL chloroplast were amplified and sequenced on the Illumina MiSeq platform. Sequences were analyzed using obitools. Of the two barcoding markers tested, trnL yielded greater numbers of sequences with equal sequencing effort, higher resolution taxonomic identifications (albeit with a larger reference database), and identified a greater number of families also found in the observed diet. There was no relationship between observed capuchin feeding behavior and dietary composition based on either sequence occurrence or relative abundance of sequences using rbcL as a marker. However, dietary composition based on the relative abundance of trnL sequences was significantly positively associated with the observed percentage of feeding and foraging time capuchins' spent on each plant species. Additionally, in 35% of cases, the relative abundance of trnL sequences assigned to particular plant families in fecal samples was highly positively correlated with time spent consuming plants from those same families. Our results indicate that trnL is a more robust DNA metabarcoding marker for plant dietary analysis and may potentially be used to quantitatively assess differences in diet within or between species.
Studies in multiple host species have shown that gut microbial diversity and composition change during pregnancy and lactation. However, the specific mechanisms underlying these shifts are not well ...understood. Here, we use longitudinal data from wild Phayre's leaf monkeys to test the hypothesis that fluctuations in reproductive hormone concentrations contribute to gut microbial shifts during pregnancy. We described the microbial taxonomic composition of 91 fecal samples from 15 females (n = 16 cycling, n = 36 pregnant, n = 39 lactating) using 16S rRNA gene amplicon sequencing and assessed whether the resulting data were better explained by overall reproductive stage or by fecal estrogen (fE) and progesterone (fP) concentrations. Our results indicate that while overall reproductive stage affected gut microbiome composition, the observed patterns were driven by reproductive hormones. Females had lower gut microbial diversity during pregnancy and fP concentrations were negatively correlated with diversity. Additionally, fP concentrations predicted both unweighted and weighted UniFrac distances, while reproductive state only predicted unweighted UniFrac distances. Seasonality (rainfall and periods of phytoprogestin consumption) additionally influenced gut microbial diversity and composition. Our results indicate that reproductive hormones, specifically progestagens, contribute to the shifts in the gut microbiome during pregnancy and lactation.
Abstract
Background
Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that ...differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates.
Results
Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates.
Conclusions
Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.
Abstract
Over the course of human evolution, shifts in dietary practices such as meat-eating and cooking, have resulted in reduced fiber intake, a trend that has been exaggerated more recently in ...industrialized populations. Reduced fiber consumption is associated with a loss of gut microbial taxa that degrade fiber, particularly butyrate. Therefore, this dietary shift in humans may have altered the abundance of microbial genes involved in butyrate production. This study uses a gene-targeted alignment approach to quantify the abundance of butyrate production pathway genes from published wild nonhuman primate and human gut metagenomes. Surprisingly, humans have higher diversity and relative abundances of butyrate production pathways compared with all groups of nonhuman primates except cercopithecoids. Industrialized populations of humans also differ only slightly in butyrate pathway abundance from nonindustrialized populations. This apparent resilience of butyrate production pathways to shifts in human diet across both evolutionary and modern populations may signal an evolutionary shift in host–microbe interactions in humans that increased SCFA production. Such a shift could have contributed to meeting the increased energy requirements of humans relative to nonhuman primates.
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