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Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence.

Morton ER, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M, Blekhman R, Ségurel L - PLoS Genet. (2015)

Bottom Line: Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity.We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders.We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, Cell Biology, and Development, Department of Ecology, Evolution, and Behavior, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
The human gut microbiota is impacted by host nutrition and health status and therefore represents a potentially adaptive phenotype influenced by metabolic and immune constraints. Previous studies contrasting rural populations in developing countries to urban industrialized ones have shown that industrialization is strongly correlated with patterns in human gut microbiota; however, we know little about the relative contribution of factors such as climate, diet, medicine, hygiene practices, host genetics, and parasitism. Here, we focus on fine-scale comparisons of African rural populations in order to (i) contrast the gut microbiota of populations inhabiting similar environments but having different traditional subsistence modes and either shared or distinct genetic ancestry, and (ii) examine the relationship between gut parasites and bacterial communities. Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity. We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders. We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon.

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Relationship between subsistence modes and fecal microbiome composition.(a) Summary of the relative abundance of taxa (occurring at > = 0.1% in at least 4 individuals) for individuals across subsistence. Taxa are colored by phylum (Actinobacteria (Act.) = red, Bacteroidetes (Bact.) = green, Cyanobacteria (Cyan.) = black, Elusimicrobia (Elus.) = gold, Firmicutes (Firm.) = blue, Fusobacteria (Fus.) = pink, Lentisphaerae (Lent.) = yellow, Proteobacteria (Prot.) = purple, Spirochaetes (Spir.) = orange, and Tenericutes (Ten.) = gray). The number of individuals (N) in each population is indicated below the bars. (b) Relative abundance of four taxa significantly associated with subsistence based on an ANOVA, q < 0.05. Fis = Fishing population; Far(S) = Farmers from the South; Far(N) = Farmers from the North; HG = Hunter-gatherers.
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pgen.1005658.g005: Relationship between subsistence modes and fecal microbiome composition.(a) Summary of the relative abundance of taxa (occurring at > = 0.1% in at least 4 individuals) for individuals across subsistence. Taxa are colored by phylum (Actinobacteria (Act.) = red, Bacteroidetes (Bact.) = green, Cyanobacteria (Cyan.) = black, Elusimicrobia (Elus.) = gold, Firmicutes (Firm.) = blue, Fusobacteria (Fus.) = pink, Lentisphaerae (Lent.) = yellow, Proteobacteria (Prot.) = purple, Spirochaetes (Spir.) = orange, and Tenericutes (Ten.) = gray). The number of individuals (N) in each population is indicated below the bars. (b) Relative abundance of four taxa significantly associated with subsistence based on an ANOVA, q < 0.05. Fis = Fishing population; Far(S) = Farmers from the South; Far(N) = Farmers from the North; HG = Hunter-gatherers.

Mentions: Controlling for the effect of Entamoeba, subsistence mode was significantly correlated with patterns of gut microbiota (p = 0.004; PERMANOVA). To investigate the relationship between subsistence and microbiome community composition, we summarized microbial taxonomic composition across the four subsistence groups and their geographic locations (Fig 5a, S13 Fig). At the phylum level, we found a moderately significant difference in the relative contribution of Proteobacteria across subsistence (q = 0.067, Table 1; ANOVA), with hunter-gatherers having a higher frequency than the fishing population, farmers from the South and the North (23% versus 12.4%, 7.2% and 8.3%, respectively), mirroring the higher frequency observed in the Hadza hunter-gatherers compared to Italians [18] and the higher frequency observed in traditional Peruvian groups (both hunter-gatherers and farmers) compared to US individuals. Based on an ANOVA, we also found that 8 of the most abundant taxa differed significantly across subsistence modes (see Fig 5b and S3 and S5 Tables). Of particular interest is the genus Bifidobacterium, both B. uncl and B. adolescentis, which were found at higher abundance in the fishing population (means 0.30% and 0.51%, respectively) relative to all other populations (≤ to 0.11% and 0.07%, respectively; q = 0.0003 and q = 0.008; ANOVA). This genus is associated with a higher consumption of dairy products, a pattern also observed in a comparison of Italians to Hadza hunter-gatherers [18] and consistent with the occasional consumption of yogurt in the fishing population. We also found Bacteroidales uncl to occur at significantly lower relative abundance in the fishing population relative to the other three populations (0.7% vs. ≥ 2.4%; q = 0.003; ANOVA), an order of bacteria also identified as being less abundant in the Italians versus the Hadza [18]. In contrast with other Firmicutes genera that tend to be in lower frequency in hunter-gatherers, we found the genus Sarcina, a synthesizer of microbial cellulose, to be only present in the hunter-gatherers (means of 0.69% compared to ≤ 0.07% in the other subsistence groups; q = 0.007; ANOVA). This genus was also found in higher frequency in traditional farming populations from Papua New Guinea as compared to US individuals [26]. Finally, we found three members of the Lachnospiraceae family to be significantly different among populations, with Ruminococcus uncl and Ruminococcus gnavus being in lower frequency in hunter-gatherers (0.34% and 0.19%, respectively) compared to other populations (0.46–0.86% and 0.41–0.99%, respectively; q = 0.030 and 0.006; ANOVA). This family has been linked to obesity [51] in addition to protection from colon cancer attributable to their production of butyric acid [52]. Importantly, although BMI did differ across subsistence modes (p = 0.026, reflecting a BMI significantly higher in fishers; linear regression model), we did not find a significant relationship between BMI and microbiota composition or diversity patterns (see S2 Table).


Variation in Rural African Gut Microbiota Is Strongly Correlated with Colonization by Entamoeba and Subsistence.

Morton ER, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M, Blekhman R, Ségurel L - PLoS Genet. (2015)

Relationship between subsistence modes and fecal microbiome composition.(a) Summary of the relative abundance of taxa (occurring at > = 0.1% in at least 4 individuals) for individuals across subsistence. Taxa are colored by phylum (Actinobacteria (Act.) = red, Bacteroidetes (Bact.) = green, Cyanobacteria (Cyan.) = black, Elusimicrobia (Elus.) = gold, Firmicutes (Firm.) = blue, Fusobacteria (Fus.) = pink, Lentisphaerae (Lent.) = yellow, Proteobacteria (Prot.) = purple, Spirochaetes (Spir.) = orange, and Tenericutes (Ten.) = gray). The number of individuals (N) in each population is indicated below the bars. (b) Relative abundance of four taxa significantly associated with subsistence based on an ANOVA, q < 0.05. Fis = Fishing population; Far(S) = Farmers from the South; Far(N) = Farmers from the North; HG = Hunter-gatherers.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4664238&req=5

pgen.1005658.g005: Relationship between subsistence modes and fecal microbiome composition.(a) Summary of the relative abundance of taxa (occurring at > = 0.1% in at least 4 individuals) for individuals across subsistence. Taxa are colored by phylum (Actinobacteria (Act.) = red, Bacteroidetes (Bact.) = green, Cyanobacteria (Cyan.) = black, Elusimicrobia (Elus.) = gold, Firmicutes (Firm.) = blue, Fusobacteria (Fus.) = pink, Lentisphaerae (Lent.) = yellow, Proteobacteria (Prot.) = purple, Spirochaetes (Spir.) = orange, and Tenericutes (Ten.) = gray). The number of individuals (N) in each population is indicated below the bars. (b) Relative abundance of four taxa significantly associated with subsistence based on an ANOVA, q < 0.05. Fis = Fishing population; Far(S) = Farmers from the South; Far(N) = Farmers from the North; HG = Hunter-gatherers.
Mentions: Controlling for the effect of Entamoeba, subsistence mode was significantly correlated with patterns of gut microbiota (p = 0.004; PERMANOVA). To investigate the relationship between subsistence and microbiome community composition, we summarized microbial taxonomic composition across the four subsistence groups and their geographic locations (Fig 5a, S13 Fig). At the phylum level, we found a moderately significant difference in the relative contribution of Proteobacteria across subsistence (q = 0.067, Table 1; ANOVA), with hunter-gatherers having a higher frequency than the fishing population, farmers from the South and the North (23% versus 12.4%, 7.2% and 8.3%, respectively), mirroring the higher frequency observed in the Hadza hunter-gatherers compared to Italians [18] and the higher frequency observed in traditional Peruvian groups (both hunter-gatherers and farmers) compared to US individuals. Based on an ANOVA, we also found that 8 of the most abundant taxa differed significantly across subsistence modes (see Fig 5b and S3 and S5 Tables). Of particular interest is the genus Bifidobacterium, both B. uncl and B. adolescentis, which were found at higher abundance in the fishing population (means 0.30% and 0.51%, respectively) relative to all other populations (≤ to 0.11% and 0.07%, respectively; q = 0.0003 and q = 0.008; ANOVA). This genus is associated with a higher consumption of dairy products, a pattern also observed in a comparison of Italians to Hadza hunter-gatherers [18] and consistent with the occasional consumption of yogurt in the fishing population. We also found Bacteroidales uncl to occur at significantly lower relative abundance in the fishing population relative to the other three populations (0.7% vs. ≥ 2.4%; q = 0.003; ANOVA), an order of bacteria also identified as being less abundant in the Italians versus the Hadza [18]. In contrast with other Firmicutes genera that tend to be in lower frequency in hunter-gatherers, we found the genus Sarcina, a synthesizer of microbial cellulose, to be only present in the hunter-gatherers (means of 0.69% compared to ≤ 0.07% in the other subsistence groups; q = 0.007; ANOVA). This genus was also found in higher frequency in traditional farming populations from Papua New Guinea as compared to US individuals [26]. Finally, we found three members of the Lachnospiraceae family to be significantly different among populations, with Ruminococcus uncl and Ruminococcus gnavus being in lower frequency in hunter-gatherers (0.34% and 0.19%, respectively) compared to other populations (0.46–0.86% and 0.41–0.99%, respectively; q = 0.030 and 0.006; ANOVA). This family has been linked to obesity [51] in addition to protection from colon cancer attributable to their production of butyric acid [52]. Importantly, although BMI did differ across subsistence modes (p = 0.026, reflecting a BMI significantly higher in fishers; linear regression model), we did not find a significant relationship between BMI and microbiota composition or diversity patterns (see S2 Table).

Bottom Line: Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity.We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders.We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, Cell Biology, and Development, Department of Ecology, Evolution, and Behavior, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
The human gut microbiota is impacted by host nutrition and health status and therefore represents a potentially adaptive phenotype influenced by metabolic and immune constraints. Previous studies contrasting rural populations in developing countries to urban industrialized ones have shown that industrialization is strongly correlated with patterns in human gut microbiota; however, we know little about the relative contribution of factors such as climate, diet, medicine, hygiene practices, host genetics, and parasitism. Here, we focus on fine-scale comparisons of African rural populations in order to (i) contrast the gut microbiota of populations inhabiting similar environments but having different traditional subsistence modes and either shared or distinct genetic ancestry, and (ii) examine the relationship between gut parasites and bacterial communities. Characterizing the fecal microbiota of Pygmy hunter-gatherers as well as Bantu individuals from both farming and fishing populations in Southwest Cameroon, we found that the gut parasite Entamoeba is significantly correlated with microbiome composition and diversity. We show that across populations, colonization by this protozoa can be predicted with 79% accuracy based on the composition of an individual's gut microbiota, and that several of the taxa most important for distinguishing Entamoeba absence or presence are signature taxa for autoimmune disorders. We also found gut communities to vary significantly with subsistence mode, notably with some taxa previously shown to be enriched in other hunter-gatherers groups (in Tanzania and Peru) also discriminating hunter-gatherers from neighboring farming or fishing populations in Cameroon.

Show MeSH
Related in: MedlinePlus