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Trait-based community assembly and succession of the infant gut microbiome.

ABSTRACT: The human gut microbiome develops over early childhood and aids in food digestion and immunomodulation, but the mechanisms driving its development remain elusive. Here we use data curated from literature and online repositories to examine trait-based patterns of gut microbiome succession in 56 infants over their first three years of life. We also develop a new phylogeny-based approach of inferring trait values that can extend readily to other microbial systems and questions. Trait-based patterns suggest that infant gut succession begins with a functionally variable cohort of taxa, adept at proliferating rapidly within hosts, which gradually matures into a more functionally uniform cohort of taxa adapted to thrive in the anoxic gut and disperse between anoxic patches as oxygen-tolerant spores. Trait-based composition stabilizes after the first year, while taxonomic turnover continues unabated, suggesting functional redundancy in the traits examined. Trait-based approaches powerfully complement taxonomy-based approaches to understanding the mechanisms of microbial community assembly and succession.

SUBMITTER: Guittar J

PROVIDER: S-EPMC6358638 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Trait-based community assembly and succession of the infant gut microbiome.

Guittar John J Shade Ashley A Litchman Elena E

Nature communications 20190201 1

The human gut microbiome develops over early childhood and aids in food digestion and immunomodulation, but the mechanisms driving its development remain elusive. Here we use data curated from literature and online repositories to examine trait-based patterns of gut microbiome succession in 56 infants over their first three years of life. We also develop a new phylogeny-based approach of inferring trait values that can extend readily to other microbial systems and questions. Trait-based patterns ...[more]

PMID: 30710083

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Project description:Background - Prepregnancy overweight and obesity promote deleterious health impacts on both mothers during pregnancy and the offspring. Significant changes in the maternal peripheral blood mononuclear cells (PBMCs) gene expression due to obesity are well-known. However, during pregnancy the impact of overweight on immune cell gene expression and its association with maternal and infant outcomes is not well explored. Methods – Blood samples were collected from healthy normal weight (NW, BMI 18.5-24.9) or overweight (OW, BMI 25-29.9) 2nd parity pregnant women at 12, 24 and 36 weeks of pregnancy. PBMCs were isolated from the blood and subjected to mRNA sequencing. Maternal and infant microbiota were analyzed by 16S rRNA gene sequencing. Integrative multi-omics data analysis was performed to evaluate the association of gene expression with maternal diet, gut microbiota, milk composition, and infant gut microbiota. Results - Gene expression analysis revealed that 453 genes were differentially expressed in the OW women compared to NW women at 12 weeks of pregnancy, out of which 354 were upregulated and 99 were downregulated. Several up-regulated genes in the OW group were enriched in inflammatory, chemokine-mediated signaling and regulation of interleukin-8 production-related pathways. At 36 weeks of pregnancy healthy eating index score was positively associated with several genes that include, DTD1, ELOC, GALNT8, ITGA6-AS1, KRT17P2, NPW, POT1-AS1 and RPL26. In addition, at 36 weeks of pregnancy, genes involved in adipocyte functions, such as NG2 and SMTNL1, were negatively correlated to human milk 2’FL and total fucosylated oligosaccharides content collected at 1 month postnatally. Furthermore, infant Akkermansia was positively associated with maternal PBMC anti-inflammatory genes that include CPS1 and RAB7B, at 12 and 36 weeks of pregnancy. Conclusions – These findings suggest that prepregnancy overweight impacts the immune cell gene expression profile, particularly at 12 weeks of pregnancy. Further, deciphering the complex association of PBMC’s gene expression levels with maternal gut microbiome and milk composition and infant gut microbiome may aid in developing strategies to mitigate obesity-mediated effects.

Project description:UnlabelledDespite its importance to the host, the flower microbiome is poorly understood. We report a culture-independent, community-level assessment of apple flower microbial diversity and dynamics. We collected flowers from six apple trees at five time points, starting before flowers opened and ending at petal fall. We applied streptomycin to half of the trees when flowers opened. Assessment of microbial diversity using tag pyrosequencing of 16S rRNA genes revealed that the apple flower communities were rich and diverse and dominated by members of TM7 and Deinococcus-Thermus, phyla about which relatively little is known. From thousands of taxa, we identified six successional groups with coherent dynamics whose abundances peaked at different times before and after bud opening. We designated the groups Pioneer, Early, Mid, Late, Climax, and Generalist communities. The successional pattern was attributed to a set of prevalent taxa that were persistent and gradually changing in abundance. These taxa had significant associations with other community members, as demonstrated with a cooccurrence network based on local similarity analysis. We also detected a set of less-abundant, transient taxa that contributed to general tree-to-tree variability but not to the successional pattern. Communities on trees sprayed with streptomycin had slightly lower phylogenetic diversity than those on unsprayed trees but did not differ in structure or succession. Our results suggest that changes in apple flower microbial community structure are predictable over the life of the flower, providing a basis for ecological understanding and disease management.ImportanceFlowering plants (angiosperms) represent a diverse group of an estimated 400,000 species, and their successful cultivation is essential to agriculture. Yet fundamental knowledge of flower-associated microbiotas remains largely unknown. Even less well understood are the changes that flower microbial communities experience through time. Flowers are particularly conducive to comprehensive temporal studies because they are, by nature, ephemeral organs. Here, we present the first culture-independent time series of bacterial and archaeal communities associated with the flowers of apple, an economically important crop. We found unexpected diversity on apple flowers, including a preponderance of taxa affiliated with Deinococcus-Thermus and TM7, phyla that are understudied but thought to be tolerant to an array of environmental stresses. Our results also suggest that changes in microbial community structure on the apple flower may be predictable over the life of the flower, providing the basis for ecological understanding and disease management.

Dataset Information

Trait-based community assembly and succession of the infant gut microbiome.

Publications

Trait-based community assembly and succession of the infant gut microbiome.

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