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Phenotypic differentiation of gastrointestinal microbes is reflected in their encoded metabolic repertoires.

Bauer E, Laczny CC, Magnusdottir S, Wilmes P, Thiele I - Microbiome (2015)

Bottom Line: Based on the global metabolic differences, we found that energy metabolism and membrane synthesis play important roles in delineating different taxonomic groups.Furthermore, we found an exponential relationship between phylogeny and the reaction composition, meaning that closely related microbes of the same genus can exhibit pronounced differences with respect to their metabolic capabilities while at the family level only marginal metabolic differences can be observed.These results have important implications in our understanding of the ecological and evolutionary complexity of the human gastrointestinal microbiome.

View Article: PubMed Central - PubMed

Affiliation: Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg. eugen.bauer@uni.lu.

ABSTRACT

Background: The human gastrointestinal tract harbors a diverse microbial community, in which metabolic phenotypes play important roles for the human host. Recent developments in meta-omics attempt to unravel metabolic roles of microbes by linking genotypic and phenotypic characteristics. This connection, however, still remains poorly understood with respect to its evolutionary and ecological context.

Results: We generated automatically refined draft genome-scale metabolic models of 301 representative intestinal microbes in silico. We applied a combination of unsupervised machine-learning and systems biology techniques to study individual and global differences in genomic content and inferred metabolic capabilities. Based on the global metabolic differences, we found that energy metabolism and membrane synthesis play important roles in delineating different taxonomic groups. Furthermore, we found an exponential relationship between phylogeny and the reaction composition, meaning that closely related microbes of the same genus can exhibit pronounced differences with respect to their metabolic capabilities while at the family level only marginal metabolic differences can be observed. This finding was further substantiated by the metabolic divergence within different genera. In particular, we could distinguish three sub-type clusters based on membrane and energy metabolism within the Lactobacilli as well as two clusters within the Bifidobacteria and Bacteroides.

Conclusions: We demonstrate that phenotypic differentiation within closely related species could be explained by their metabolic repertoire rather than their phylogenetic relationships. These results have important implications in our understanding of the ecological and evolutionary complexity of the human gastrointestinal microbiome.

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Related in: MedlinePlus

Global differences within metabolic models and their most divergent reactions. Biplot of the principle coordinate analysis based on the metabolic distance determined by the presence/absence of specific reactions in the metabolic models. Taxonomic groups are represented by different colors. The 200 reactions most associated with the point separation are indicated as arrows pointing from the coordinate origin to the contributing direction. The arrow shading represents reactions overlapping in their direction of contribution. The complete set of 2272 reactions sorted by their relevance can be found in Additional file 4: Table S3
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Fig2: Global differences within metabolic models and their most divergent reactions. Biplot of the principle coordinate analysis based on the metabolic distance determined by the presence/absence of specific reactions in the metabolic models. Taxonomic groups are represented by different colors. The 200 reactions most associated with the point separation are indicated as arrows pointing from the coordinate origin to the contributing direction. The arrow shading represents reactions overlapping in their direction of contribution. The complete set of 2272 reactions sorted by their relevance can be found in Additional file 4: Table S3

Mentions: To assess the differences within the metabolic reconstructions, we tested whether they could recapitulate the taxonomy of the studied microbes. We therefore computed a metabolic distance between the reconstructions based on the reaction presence [32] and subsequently used principle coordinate analysis (PCoA) [33]. This analysis revealed clusters, which correspond to known taxonomic groups (Fig. 2). More specifically, with more than 30 % of explained variance, the first principle coordinate (Fig. 2) was able to discriminate between Gram-negative and Gram-positive bacteria, which is in concordance to traditional measures of broad taxonomic groups, assigned based on the phylogeny of the 16S rRNA gene, the production of fatty acids, and corresponding membrane lipid composition [34]. In our PCoA (Fig. 2), members of the class Negativicutes were closely associated with Gram-negative bacteria rather than their phylogenetically close Gram-positive relatives, which is in accordance to their unusual membrane composition including two membrane layers [35].Fig. 2


Phenotypic differentiation of gastrointestinal microbes is reflected in their encoded metabolic repertoires.

Bauer E, Laczny CC, Magnusdottir S, Wilmes P, Thiele I - Microbiome (2015)

Global differences within metabolic models and their most divergent reactions. Biplot of the principle coordinate analysis based on the metabolic distance determined by the presence/absence of specific reactions in the metabolic models. Taxonomic groups are represented by different colors. The 200 reactions most associated with the point separation are indicated as arrows pointing from the coordinate origin to the contributing direction. The arrow shading represents reactions overlapping in their direction of contribution. The complete set of 2272 reactions sorted by their relevance can be found in Additional file 4: Table S3
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4663747&req=5

Fig2: Global differences within metabolic models and their most divergent reactions. Biplot of the principle coordinate analysis based on the metabolic distance determined by the presence/absence of specific reactions in the metabolic models. Taxonomic groups are represented by different colors. The 200 reactions most associated with the point separation are indicated as arrows pointing from the coordinate origin to the contributing direction. The arrow shading represents reactions overlapping in their direction of contribution. The complete set of 2272 reactions sorted by their relevance can be found in Additional file 4: Table S3
Mentions: To assess the differences within the metabolic reconstructions, we tested whether they could recapitulate the taxonomy of the studied microbes. We therefore computed a metabolic distance between the reconstructions based on the reaction presence [32] and subsequently used principle coordinate analysis (PCoA) [33]. This analysis revealed clusters, which correspond to known taxonomic groups (Fig. 2). More specifically, with more than 30 % of explained variance, the first principle coordinate (Fig. 2) was able to discriminate between Gram-negative and Gram-positive bacteria, which is in concordance to traditional measures of broad taxonomic groups, assigned based on the phylogeny of the 16S rRNA gene, the production of fatty acids, and corresponding membrane lipid composition [34]. In our PCoA (Fig. 2), members of the class Negativicutes were closely associated with Gram-negative bacteria rather than their phylogenetically close Gram-positive relatives, which is in accordance to their unusual membrane composition including two membrane layers [35].Fig. 2

Bottom Line: Based on the global metabolic differences, we found that energy metabolism and membrane synthesis play important roles in delineating different taxonomic groups.Furthermore, we found an exponential relationship between phylogeny and the reaction composition, meaning that closely related microbes of the same genus can exhibit pronounced differences with respect to their metabolic capabilities while at the family level only marginal metabolic differences can be observed.These results have important implications in our understanding of the ecological and evolutionary complexity of the human gastrointestinal microbiome.

View Article: PubMed Central - PubMed

Affiliation: Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg. eugen.bauer@uni.lu.

ABSTRACT

Background: The human gastrointestinal tract harbors a diverse microbial community, in which metabolic phenotypes play important roles for the human host. Recent developments in meta-omics attempt to unravel metabolic roles of microbes by linking genotypic and phenotypic characteristics. This connection, however, still remains poorly understood with respect to its evolutionary and ecological context.

Results: We generated automatically refined draft genome-scale metabolic models of 301 representative intestinal microbes in silico. We applied a combination of unsupervised machine-learning and systems biology techniques to study individual and global differences in genomic content and inferred metabolic capabilities. Based on the global metabolic differences, we found that energy metabolism and membrane synthesis play important roles in delineating different taxonomic groups. Furthermore, we found an exponential relationship between phylogeny and the reaction composition, meaning that closely related microbes of the same genus can exhibit pronounced differences with respect to their metabolic capabilities while at the family level only marginal metabolic differences can be observed. This finding was further substantiated by the metabolic divergence within different genera. In particular, we could distinguish three sub-type clusters based on membrane and energy metabolism within the Lactobacilli as well as two clusters within the Bifidobacteria and Bacteroides.

Conclusions: We demonstrate that phenotypic differentiation within closely related species could be explained by their metabolic repertoire rather than their phylogenetic relationships. These results have important implications in our understanding of the ecological and evolutionary complexity of the human gastrointestinal microbiome.

Show MeSH
Related in: MedlinePlus