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Subsistence strategies in traditional societies distinguish gut microbiomes.

Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, Zech Xu Z, Van Treuren W, Knight R, Gaffney PM, Spicer P, Lawson P, Marin-Reyes L, Trujillo-Villarroel O, Foster M, Guija-Poma E, Troncoso-Corzo L, Warinner C, Ozga AT, Lewis CM - Nat Commun (2015)

Bottom Line: We find that in addition to taxonomic and metabolic differences between urban and traditional lifestyles, hunter-gatherers form a distinct sub-group among traditional peoples.As observed in previous studies, we find that Treponema are characteristic of traditional gut microbiomes.Moreover, through genome reconstruction (2.2-2.5 MB, coverage depth × 26-513) and functional potential characterization, we discover these Treponema are diverse, fall outside of pathogenic clades and are similar to Treponema succinifaciens, a known carbohydrate metabolizer in swine.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Anthropology, University of Oklahoma, Dale Hall Tower, 521 Norman, Oklahoma 73019, USA [2] Universidad Científica del Sur, Lima 18, Perú [3] City of Hope, NCI-designated Comprehensive Cancer Center, Duarte, California 91010, USA.

ABSTRACT
Recent studies suggest that gut microbiomes of urban-industrialized societies are different from those of traditional peoples. Here we examine the relationship between lifeways and gut microbiota through taxonomic and functional potential characterization of faecal samples from hunter-gatherer and traditional agriculturalist communities in Peru and an urban-industrialized community from the US. We find that in addition to taxonomic and metabolic differences between urban and traditional lifestyles, hunter-gatherers form a distinct sub-group among traditional peoples. As observed in previous studies, we find that Treponema are characteristic of traditional gut microbiomes. Moreover, through genome reconstruction (2.2-2.5 MB, coverage depth × 26-513) and functional potential characterization, we discover these Treponema are diverse, fall outside of pathogenic clades and are similar to Treponema succinifaciens, a known carbohydrate metabolizer in swine. Gut Treponema are found in non-human primates and all traditional peoples studied to date, suggesting they are symbionts lost in urban-industrialized societies.

No MeSH data available.


Phylogenetic trees showing relationship of Matses Treponema strains to reference Treponema species.(a) Maximum likelihood tree constructed using 16S rRNA sequences from de novo assemblies of shotgun data. (b) Maximum likelihood tree constructed using concatenated amino acid sequences from 35 single copy marker loci, retrieved from de novo assemblies of shotgun data. Both trees show similar topology, with the Matses Treponema strains grouping with Treponema succinifaciens, a known carbohydrate metabolizer in the swine gut microbiome.
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f6: Phylogenetic trees showing relationship of Matses Treponema strains to reference Treponema species.(a) Maximum likelihood tree constructed using 16S rRNA sequences from de novo assemblies of shotgun data. (b) Maximum likelihood tree constructed using concatenated amino acid sequences from 35 single copy marker loci, retrieved from de novo assemblies of shotgun data. Both trees show similar topology, with the Matses Treponema strains grouping with Treponema succinifaciens, a known carbohydrate metabolizer in the swine gut microbiome.

Mentions: To further characterize the phylogenetic and functional relationships of the Matses gut Treponema to other currently available reference strains from this genus, we retrieved contigs matching Treponema from metagenomes assembled de novo (Methods) from four Matses samples. These samples were selected based on high frequencies of Treponema observed in their taxonomic profiles. Samples from Tunapuco were not included in this analysis as they had lower sequencing coverage and often contained multiple Treponema strains leading to poor assemblies. Phylogenetic analysis using 16S rRNA gene sequences retrieved from these contigs confirmed the presence of two distinct strains of Treponema within these samples, one with ~99% sequence similarity to T. succinifaciens (found in all four samples, referred to as Strain 1) and the other with ~90% sequence similarity to T. succinifaciens (found in two samples, referred to as Strain 2) (Fig. 6a). A second phylogenetic tree constructed using concatenated amino acid sequences from 35 single copy marker loci22 (predominantly composed of ribosomal small and large subunit proteins) showed similar topology, confirming the presence of two distinct strains of Treponema within our samples (Fig. 6b). Overall, we retrieved between 2.19 and 2.46 Mb of genome sequence data for the Treponema strains through a combination of methods, including sequence identity to the reference T. succinifaciens, GC% and coverage statistics (Methods). We annotated these partial assemblies using the ‘prokka’ pipeline23, followed by evaluation of metabolic potential using MAPLE24. We then performed hierarchical clustering using metabolic Module Completion Ratio (MCR) data obtained from the MAPLE24 pipeline (Fig. 7). Based on predicted metabolic potential, the reconstructed Treponema strains cluster most closely with T. succinifaciens and are nested with other gut-associated treponemes reported from termites (T. azotonutricium and T. primitia)25 and a digital dermatitis associated Treponema reported from cattle (T. brennaborense)26. In addition, these strains functionally cluster with gut-associated members of the Brachyspira clade of Spirochaetes, along with several gut-associated bacteria from other phyla, including Ruminococcus, Eubacterium and Butyrivibrio. In contrast several pathogenic Spirochaetes including T. pallidum (syphilis), Borrellia burgdorferi (Lyme disease) and T. denticola (periodontal disease), form a functionally separate clade outside of the gut-associated bacteria. Overall, these results give further support for a potential metabolic role for the Treponema strains observed in the gut microbiomes of traditional human populations.


Subsistence strategies in traditional societies distinguish gut microbiomes.

Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, Zech Xu Z, Van Treuren W, Knight R, Gaffney PM, Spicer P, Lawson P, Marin-Reyes L, Trujillo-Villarroel O, Foster M, Guija-Poma E, Troncoso-Corzo L, Warinner C, Ozga AT, Lewis CM - Nat Commun (2015)

Phylogenetic trees showing relationship of Matses Treponema strains to reference Treponema species.(a) Maximum likelihood tree constructed using 16S rRNA sequences from de novo assemblies of shotgun data. (b) Maximum likelihood tree constructed using concatenated amino acid sequences from 35 single copy marker loci, retrieved from de novo assemblies of shotgun data. Both trees show similar topology, with the Matses Treponema strains grouping with Treponema succinifaciens, a known carbohydrate metabolizer in the swine gut microbiome.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4386023&req=5

f6: Phylogenetic trees showing relationship of Matses Treponema strains to reference Treponema species.(a) Maximum likelihood tree constructed using 16S rRNA sequences from de novo assemblies of shotgun data. (b) Maximum likelihood tree constructed using concatenated amino acid sequences from 35 single copy marker loci, retrieved from de novo assemblies of shotgun data. Both trees show similar topology, with the Matses Treponema strains grouping with Treponema succinifaciens, a known carbohydrate metabolizer in the swine gut microbiome.
Mentions: To further characterize the phylogenetic and functional relationships of the Matses gut Treponema to other currently available reference strains from this genus, we retrieved contigs matching Treponema from metagenomes assembled de novo (Methods) from four Matses samples. These samples were selected based on high frequencies of Treponema observed in their taxonomic profiles. Samples from Tunapuco were not included in this analysis as they had lower sequencing coverage and often contained multiple Treponema strains leading to poor assemblies. Phylogenetic analysis using 16S rRNA gene sequences retrieved from these contigs confirmed the presence of two distinct strains of Treponema within these samples, one with ~99% sequence similarity to T. succinifaciens (found in all four samples, referred to as Strain 1) and the other with ~90% sequence similarity to T. succinifaciens (found in two samples, referred to as Strain 2) (Fig. 6a). A second phylogenetic tree constructed using concatenated amino acid sequences from 35 single copy marker loci22 (predominantly composed of ribosomal small and large subunit proteins) showed similar topology, confirming the presence of two distinct strains of Treponema within our samples (Fig. 6b). Overall, we retrieved between 2.19 and 2.46 Mb of genome sequence data for the Treponema strains through a combination of methods, including sequence identity to the reference T. succinifaciens, GC% and coverage statistics (Methods). We annotated these partial assemblies using the ‘prokka’ pipeline23, followed by evaluation of metabolic potential using MAPLE24. We then performed hierarchical clustering using metabolic Module Completion Ratio (MCR) data obtained from the MAPLE24 pipeline (Fig. 7). Based on predicted metabolic potential, the reconstructed Treponema strains cluster most closely with T. succinifaciens and are nested with other gut-associated treponemes reported from termites (T. azotonutricium and T. primitia)25 and a digital dermatitis associated Treponema reported from cattle (T. brennaborense)26. In addition, these strains functionally cluster with gut-associated members of the Brachyspira clade of Spirochaetes, along with several gut-associated bacteria from other phyla, including Ruminococcus, Eubacterium and Butyrivibrio. In contrast several pathogenic Spirochaetes including T. pallidum (syphilis), Borrellia burgdorferi (Lyme disease) and T. denticola (periodontal disease), form a functionally separate clade outside of the gut-associated bacteria. Overall, these results give further support for a potential metabolic role for the Treponema strains observed in the gut microbiomes of traditional human populations.

Bottom Line: We find that in addition to taxonomic and metabolic differences between urban and traditional lifestyles, hunter-gatherers form a distinct sub-group among traditional peoples.As observed in previous studies, we find that Treponema are characteristic of traditional gut microbiomes.Moreover, through genome reconstruction (2.2-2.5 MB, coverage depth × 26-513) and functional potential characterization, we discover these Treponema are diverse, fall outside of pathogenic clades and are similar to Treponema succinifaciens, a known carbohydrate metabolizer in swine.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Anthropology, University of Oklahoma, Dale Hall Tower, 521 Norman, Oklahoma 73019, USA [2] Universidad Científica del Sur, Lima 18, Perú [3] City of Hope, NCI-designated Comprehensive Cancer Center, Duarte, California 91010, USA.

ABSTRACT
Recent studies suggest that gut microbiomes of urban-industrialized societies are different from those of traditional peoples. Here we examine the relationship between lifeways and gut microbiota through taxonomic and functional potential characterization of faecal samples from hunter-gatherer and traditional agriculturalist communities in Peru and an urban-industrialized community from the US. We find that in addition to taxonomic and metabolic differences between urban and traditional lifestyles, hunter-gatherers form a distinct sub-group among traditional peoples. As observed in previous studies, we find that Treponema are characteristic of traditional gut microbiomes. Moreover, through genome reconstruction (2.2-2.5 MB, coverage depth × 26-513) and functional potential characterization, we discover these Treponema are diverse, fall outside of pathogenic clades and are similar to Treponema succinifaciens, a known carbohydrate metabolizer in swine. Gut Treponema are found in non-human primates and all traditional peoples studied to date, suggesting they are symbionts lost in urban-industrialized societies.

No MeSH data available.