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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

Phylogeny and individual statistics of the microbe selection. The cladogram shows the taxonomic relationships among the 301 microbes. In the four outer layers, the bars represent the relative individual genome size, number of genes, number of reactions, and in silico growth rate. The different colors represent the various bacterial classes. The leaf colors and shapes symbolize whether a microbe is a probiotic (green triangle), a pathogen (red diamond), an opportunistic pathogen (red circles), or a non-pathogenic bacterium (white triangles)
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Fig1: Phylogeny and individual statistics of the microbe selection. The cladogram shows the taxonomic relationships among the 301 microbes. In the four outer layers, the bars represent the relative individual genome size, number of genes, number of reactions, and in silico growth rate. The different colors represent the various bacterial classes. The leaf colors and shapes symbolize whether a microbe is a probiotic (green triangle), a pathogen (red diamond), an opportunistic pathogen (red circles), or a non-pathogenic bacterium (white triangles)

Mentions: In order to answer ecological and evolutionary questions relevant for human health and disease, we selected 301 commonly found gut microbes based on their reported occurrence in the healthy gut microbiome [1, 3] and the availability of sequenced isolate genomes (Fig. 1). We used the Model SEED platform [19] to generate automated draft genome-scale metabolic reconstructions for each microbe. To enable growth under anaerobic conditions, which are predominant in the human gut [23], we added specific reactions, if necessary (Additional file 1: Table S2). A comparison of our draft reconstructions with a set of published manually refined high-quality metabolic reconstructions taken from [24] revealed that most of the metabolic functionalities were captured in the refined draft reconstructions (Additional file 2: Figure S1). Reactions absent in the refined draft reconstruction belonged mostly to the category of transport and exchange reactions, whose addition requires experimental and physiological data, as substrate specificity and transport mechanism is difficult to automatically annotate in microbial genomes [25].Fig. 1


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

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

Phylogeny and individual statistics of the microbe selection. The cladogram shows the taxonomic relationships among the 301 microbes. In the four outer layers, the bars represent the relative individual genome size, number of genes, number of reactions, and in silico growth rate. The different colors represent the various bacterial classes. The leaf colors and shapes symbolize whether a microbe is a probiotic (green triangle), a pathogen (red diamond), an opportunistic pathogen (red circles), or a non-pathogenic bacterium (white triangles)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Phylogeny and individual statistics of the microbe selection. The cladogram shows the taxonomic relationships among the 301 microbes. In the four outer layers, the bars represent the relative individual genome size, number of genes, number of reactions, and in silico growth rate. The different colors represent the various bacterial classes. The leaf colors and shapes symbolize whether a microbe is a probiotic (green triangle), a pathogen (red diamond), an opportunistic pathogen (red circles), or a non-pathogenic bacterium (white triangles)
Mentions: In order to answer ecological and evolutionary questions relevant for human health and disease, we selected 301 commonly found gut microbes based on their reported occurrence in the healthy gut microbiome [1, 3] and the availability of sequenced isolate genomes (Fig. 1). We used the Model SEED platform [19] to generate automated draft genome-scale metabolic reconstructions for each microbe. To enable growth under anaerobic conditions, which are predominant in the human gut [23], we added specific reactions, if necessary (Additional file 1: Table S2). A comparison of our draft reconstructions with a set of published manually refined high-quality metabolic reconstructions taken from [24] revealed that most of the metabolic functionalities were captured in the refined draft reconstructions (Additional file 2: Figure S1). Reactions absent in the refined draft reconstruction belonged mostly to the category of transport and exchange reactions, whose addition requires experimental and physiological data, as substrate specificity and transport mechanism is difficult to automatically annotate in microbial genomes [25].Fig. 1

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