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Human gut microbiome viewed across age and geography.

Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI - Nature (2012)

Bottom Line: Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the genes involved in vitamin biosynthesis and metabolism.These distinctive features are evident in early infancy as well as adulthood.Our findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations and the impact of westernization.

View Article: PubMed Central - PubMed

Affiliation: Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St Louis, Missouri 63108, USA.

ABSTRACT
Gut microbial communities represent one source of human genetic and metabolic diversity. To examine how gut microbiomes differ among human populations, here we characterize bacterial species in fecal samples from 531 individuals, plus the gene content of 110 of them. The cohort encompassed healthy children and adults from the Amazonas of Venezuela, rural Malawi and US metropolitan areas and included mono- and dizygotic twins. Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the genes involved in vitamin biosynthesis and metabolism. Pronounced differences in bacterial assemblages and functional gene repertoires were noted between US residents and those in the other two countries. These distinctive features are evident in early infancy as well as adulthood. Our findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations and the impact of westernization.

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Differences in the fecal microbial communities of Malawians, Amerindians and residents of the USA at different ages(a) UniFrac distances between children and adults decrease with increasing age of children in each population. Each point shows an average distance between a child and all adults unrelated to that child but from the same country. Results are derived from bacterial V4-16S rRNA datasets. (b) Large interpersonal variations are observed in the phylogenetic configurations of fecal microbial communities at early ages. Malawian and Amerindian children and adults are more similar to one another than to USA children and adults. UniFrac distances were defined from bacterial V4-16S rRNA data generated from the microbiota of 181 unrelated adults (≥18 years old) and 204 unrelated children (n=31 Malawians 0.03–3 years old, 21 3–17 years old; 30 Amerindians 0.08–3 years old, 29 3–17 years old; 31 residents of the USA 0.08–3 years old, 62 sampled at 3–17 years of age). Abbreviations: * p<0.05; **p<0.005 (Student’s t-test with 1000 Monte Carlo simulations). See Table S3 for a complete description of the statistical significance of all comparisons shown in the Figure. (c) PCoA of unweighted UniFrac distances for the fecal microbiota of adults.
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Figure 1: Differences in the fecal microbial communities of Malawians, Amerindians and residents of the USA at different ages(a) UniFrac distances between children and adults decrease with increasing age of children in each population. Each point shows an average distance between a child and all adults unrelated to that child but from the same country. Results are derived from bacterial V4-16S rRNA datasets. (b) Large interpersonal variations are observed in the phylogenetic configurations of fecal microbial communities at early ages. Malawian and Amerindian children and adults are more similar to one another than to USA children and adults. UniFrac distances were defined from bacterial V4-16S rRNA data generated from the microbiota of 181 unrelated adults (≥18 years old) and 204 unrelated children (n=31 Malawians 0.03–3 years old, 21 3–17 years old; 30 Amerindians 0.08–3 years old, 29 3–17 years old; 31 residents of the USA 0.08–3 years old, 62 sampled at 3–17 years of age). Abbreviations: * p<0.05; **p<0.005 (Student’s t-test with 1000 Monte Carlo simulations). See Table S3 for a complete description of the statistical significance of all comparisons shown in the Figure. (c) PCoA of unweighted UniFrac distances for the fecal microbiota of adults.

Mentions: We collected bacterial V4-16S rRNA data from 326 individuals aged 0–17 years (83 Malawian, 65 Amerindian and 178 residents of the USA) plus 202 adults aged 18–70 years (31 Malawians, 35 Amerindians, and 136 residents of the USA). 16S rRNA datasets were first analyzed using UniFrac, an algorithm that measures similarity between microbial communities based on the degree to which their component taxa share branch length on a bacterial tree of life16. There were several notable findings. First, the phylogenetic composition of the bacterial community evolved towards an adult-like configuration within the 3-year period following birth in all three populations (Fig. 1a, Fig. S1). Second, interpersonal variation is significantly greater between children than between adults; this finding is robust to geography (Fig. 1b; also see ref. 4). Third, there were significant differences in the phylogenetic composition of fecal microbiota between individuals living in the different countries, with especially pronounced separation occurring between USA compared to Malawian and Amerindian gut communities; this was true for individuals aged 0–3 years, 3–17 years, and for adults (Fig. 1b, Table S3). Unsupervised clustering using Principal Coordinates Analysis (PCoA) of UniFrac distance matrices indicated that age and geography/cultural traditions primarily explain the variation in our dataset, where USA microbiota clustered separately from non-USA along principal coordinate 1 (Fig. 1c, S2). However, within the non-USA populations, separation between Malawians and Amerindians was also observed (along principal coordinate 3 in the case of adults, Fig. S2f). We did not find any significant clustering by a village for Malawians and Amerindians or by region within the USA. Fourth, bacterial diversity increased with age in all three populations (Fig. 2a,b). The fecal microbiota of USA adults was the least diverse compared to the two other populations (Fig. 2c, p<0.005, ANOVA with Bonferroni post-hoc test): these differences were evident in children older than 3 years of age (p<0.005, ANOVA with Bonferroni post-hoc test), but not in younger subjects.


Human gut microbiome viewed across age and geography.

Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI - Nature (2012)

Differences in the fecal microbial communities of Malawians, Amerindians and residents of the USA at different ages(a) UniFrac distances between children and adults decrease with increasing age of children in each population. Each point shows an average distance between a child and all adults unrelated to that child but from the same country. Results are derived from bacterial V4-16S rRNA datasets. (b) Large interpersonal variations are observed in the phylogenetic configurations of fecal microbial communities at early ages. Malawian and Amerindian children and adults are more similar to one another than to USA children and adults. UniFrac distances were defined from bacterial V4-16S rRNA data generated from the microbiota of 181 unrelated adults (≥18 years old) and 204 unrelated children (n=31 Malawians 0.03–3 years old, 21 3–17 years old; 30 Amerindians 0.08–3 years old, 29 3–17 years old; 31 residents of the USA 0.08–3 years old, 62 sampled at 3–17 years of age). Abbreviations: * p<0.05; **p<0.005 (Student’s t-test with 1000 Monte Carlo simulations). See Table S3 for a complete description of the statistical significance of all comparisons shown in the Figure. (c) PCoA of unweighted UniFrac distances for the fecal microbiota of adults.
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Related In: Results  -  Collection

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Figure 1: Differences in the fecal microbial communities of Malawians, Amerindians and residents of the USA at different ages(a) UniFrac distances between children and adults decrease with increasing age of children in each population. Each point shows an average distance between a child and all adults unrelated to that child but from the same country. Results are derived from bacterial V4-16S rRNA datasets. (b) Large interpersonal variations are observed in the phylogenetic configurations of fecal microbial communities at early ages. Malawian and Amerindian children and adults are more similar to one another than to USA children and adults. UniFrac distances were defined from bacterial V4-16S rRNA data generated from the microbiota of 181 unrelated adults (≥18 years old) and 204 unrelated children (n=31 Malawians 0.03–3 years old, 21 3–17 years old; 30 Amerindians 0.08–3 years old, 29 3–17 years old; 31 residents of the USA 0.08–3 years old, 62 sampled at 3–17 years of age). Abbreviations: * p<0.05; **p<0.005 (Student’s t-test with 1000 Monte Carlo simulations). See Table S3 for a complete description of the statistical significance of all comparisons shown in the Figure. (c) PCoA of unweighted UniFrac distances for the fecal microbiota of adults.
Mentions: We collected bacterial V4-16S rRNA data from 326 individuals aged 0–17 years (83 Malawian, 65 Amerindian and 178 residents of the USA) plus 202 adults aged 18–70 years (31 Malawians, 35 Amerindians, and 136 residents of the USA). 16S rRNA datasets were first analyzed using UniFrac, an algorithm that measures similarity between microbial communities based on the degree to which their component taxa share branch length on a bacterial tree of life16. There were several notable findings. First, the phylogenetic composition of the bacterial community evolved towards an adult-like configuration within the 3-year period following birth in all three populations (Fig. 1a, Fig. S1). Second, interpersonal variation is significantly greater between children than between adults; this finding is robust to geography (Fig. 1b; also see ref. 4). Third, there were significant differences in the phylogenetic composition of fecal microbiota between individuals living in the different countries, with especially pronounced separation occurring between USA compared to Malawian and Amerindian gut communities; this was true for individuals aged 0–3 years, 3–17 years, and for adults (Fig. 1b, Table S3). Unsupervised clustering using Principal Coordinates Analysis (PCoA) of UniFrac distance matrices indicated that age and geography/cultural traditions primarily explain the variation in our dataset, where USA microbiota clustered separately from non-USA along principal coordinate 1 (Fig. 1c, S2). However, within the non-USA populations, separation between Malawians and Amerindians was also observed (along principal coordinate 3 in the case of adults, Fig. S2f). We did not find any significant clustering by a village for Malawians and Amerindians or by region within the USA. Fourth, bacterial diversity increased with age in all three populations (Fig. 2a,b). The fecal microbiota of USA adults was the least diverse compared to the two other populations (Fig. 2c, p<0.005, ANOVA with Bonferroni post-hoc test): these differences were evident in children older than 3 years of age (p<0.005, ANOVA with Bonferroni post-hoc test), but not in younger subjects.

Bottom Line: Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the genes involved in vitamin biosynthesis and metabolism.These distinctive features are evident in early infancy as well as adulthood.Our findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations and the impact of westernization.

View Article: PubMed Central - PubMed

Affiliation: Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St Louis, Missouri 63108, USA.

ABSTRACT
Gut microbial communities represent one source of human genetic and metabolic diversity. To examine how gut microbiomes differ among human populations, here we characterize bacterial species in fecal samples from 531 individuals, plus the gene content of 110 of them. The cohort encompassed healthy children and adults from the Amazonas of Venezuela, rural Malawi and US metropolitan areas and included mono- and dizygotic twins. Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the genes involved in vitamin biosynthesis and metabolism. Pronounced differences in bacterial assemblages and functional gene repertoires were noted between US residents and those in the other two countries. These distinctive features are evident in early infancy as well as adulthood. Our findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations and the impact of westernization.

Show MeSH