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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 the presence of Entamoeba (Ent- or Ent+) and fecal microbiome composition.(a) Multidimensional Scaling plot of unweighted UniFrac distances colored by Entamoeba presence or absence. The first two principal components (PC1 and PC2 are shown). (b) Summary of the relative abundance of taxa (> = 0.1% in at least 4 individuals) for Ent- and Ent+ individuals color coded 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. (c) Normalized relative abundance of four taxa significantly associated with Entamoeba presence/absence in an ANOVA as well as in the random forest classifier model (q < 0.05).
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pgen.1005658.g002: Relationship between the presence of Entamoeba (Ent- or Ent+) and fecal microbiome composition.(a) Multidimensional Scaling plot of unweighted UniFrac distances colored by Entamoeba presence or absence. The first two principal components (PC1 and PC2 are shown). (b) Summary of the relative abundance of taxa (> = 0.1% in at least 4 individuals) for Ent- and Ent+ individuals color coded 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. (c) Normalized relative abundance of four taxa significantly associated with Entamoeba presence/absence in an ANOVA as well as in the random forest classifier model (q < 0.05).

Mentions: We used PERMANOVA analysis to separately test for associations between microbiome composition (OTU abundances) and age, sex, BMI, parasitism, location, subsistence, and ancestry, the latter three being nested (see S2 Table). We found that the presence of Entamoeba, location, subsistence, and ancestry were each significantly associated with variation in microbiome composition (p = 0.0001, 0.01, 0.003 and 0.01, respectively; S2 Table), whereas the other factors were not. To further characterize patterns of variation that account for phylogenetic relationships of community taxa, we also performed a PERMANOVA analysis on both weighted and unweighted UniFrac distance matrices. Congruent with our previous results, we found that the presence of Entamoeba was the most significant variable for both weighted and unweighted UniFrac distances (p = 0.007 and 0.0001, respectively; S2 Table). Entamoeba infection also provided the strongest separation along the primary axis of variation of the multidimensional scaling plots (Fig 2a and S4a Fig). Subsistence and location were both determined to be significant based on unweighted UniFrac distances (p = 0.0003 and p = 0.002, respectively), but not weighted (p = 0.14 and p = 0.29, respectively). Because unweighted UniFrac distances assign increased weight to rare taxa, this suggests that less abundant taxa are more important in describing differences between the microbiomes across subsistence modes and locations. Furthermore, subsistence provided only weak visual separation along the first two axes of variation for both metrics (S4b and S4c Fig).


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 the presence of Entamoeba (Ent- or Ent+) and fecal microbiome composition.(a) Multidimensional Scaling plot of unweighted UniFrac distances colored by Entamoeba presence or absence. The first two principal components (PC1 and PC2 are shown). (b) Summary of the relative abundance of taxa (> = 0.1% in at least 4 individuals) for Ent- and Ent+ individuals color coded 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. (c) Normalized relative abundance of four taxa significantly associated with Entamoeba presence/absence in an ANOVA as well as in the random forest classifier model (q < 0.05).
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pgen.1005658.g002: Relationship between the presence of Entamoeba (Ent- or Ent+) and fecal microbiome composition.(a) Multidimensional Scaling plot of unweighted UniFrac distances colored by Entamoeba presence or absence. The first two principal components (PC1 and PC2 are shown). (b) Summary of the relative abundance of taxa (> = 0.1% in at least 4 individuals) for Ent- and Ent+ individuals color coded 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. (c) Normalized relative abundance of four taxa significantly associated with Entamoeba presence/absence in an ANOVA as well as in the random forest classifier model (q < 0.05).
Mentions: We used PERMANOVA analysis to separately test for associations between microbiome composition (OTU abundances) and age, sex, BMI, parasitism, location, subsistence, and ancestry, the latter three being nested (see S2 Table). We found that the presence of Entamoeba, location, subsistence, and ancestry were each significantly associated with variation in microbiome composition (p = 0.0001, 0.01, 0.003 and 0.01, respectively; S2 Table), whereas the other factors were not. To further characterize patterns of variation that account for phylogenetic relationships of community taxa, we also performed a PERMANOVA analysis on both weighted and unweighted UniFrac distance matrices. Congruent with our previous results, we found that the presence of Entamoeba was the most significant variable for both weighted and unweighted UniFrac distances (p = 0.007 and 0.0001, respectively; S2 Table). Entamoeba infection also provided the strongest separation along the primary axis of variation of the multidimensional scaling plots (Fig 2a and S4a Fig). Subsistence and location were both determined to be significant based on unweighted UniFrac distances (p = 0.0003 and p = 0.002, respectively), but not weighted (p = 0.14 and p = 0.29, respectively). Because unweighted UniFrac distances assign increased weight to rare taxa, this suggests that less abundant taxa are more important in describing differences between the microbiomes across subsistence modes and locations. Furthermore, subsistence provided only weak visual separation along the first two axes of variation for both metrics (S4b and S4c Fig).

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