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. 2014 Jun;8(6):1323-35.
doi: 10.1038/ismej.2014.14. Epub 2014 Feb 20.

Phylogenetic Distribution of Three Pathways for Propionate Production Within the Human Gut Microbiota

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Phylogenetic Distribution of Three Pathways for Propionate Production Within the Human Gut Microbiota

Nicole Reichardt et al. ISME J. .
Free PMC article

Erratum in

  • ISME J. 2014 Jun;8(6):1352

Abstract

Propionate is produced in the human large intestine by microbial fermentation and may help maintain human health. We have examined the distribution of three different pathways used by bacteria for propionate formation using genomic and metagenomic analysis of the human gut microbiota and by designing degenerate primer sets for the detection of diagnostic genes for these pathways. Degenerate primers for the acrylate pathway (detecting the lcdA gene, encoding lactoyl-CoA dehydratase) together with metagenomic mining revealed that this pathway is restricted to only a few human colonic species within the Lachnospiraceae and Negativicutes. The operation of this pathway for lactate utilisation in Coprococcus catus (Lachnospiraceae) was confirmed using stable isotope labelling. The propanediol pathway that processes deoxy sugars such as fucose and rhamnose was more abundant within the Lachnospiraceae (based on the pduP gene, which encodes propionaldehyde dehydrogenase), occurring in relatives of Ruminococcus obeum and in Roseburia inulinivorans. The dominant source of propionate from hexose sugars, however, was concluded to be the succinate pathway, as indicated by the widespread distribution of the mmdA gene that encodes methylmalonyl-CoA decarboxylase in the Bacteroidetes and in many Negativicutes. In general, the capacity to produce propionate or butyrate from hexose sugars resided in different species, although two species of Lachnospiraceae (C. catus and R. inulinivorans) are now known to be able to switch from butyrate to propionate production on different substrates. A better understanding of the microbial ecology of short-chain fatty acid formation may allow modulation of propionate formation by the human gut microbiota.

Figures

Figure 1
Figure 1
Known pathways for propionate formation in human gut bacteria. (P1), Succinate pathway; (P2), acrylate pathway; (P3), propanediol pathway. Substrates utilised are shown in boxes. Genes targeted as molecular markers for the specific pathways are indicated. DHAP, dihydroxyacetonephosphate; PEP, phosphoenolpyruvate.
Figure 2
Figure 2
Fermentation acid profiles for C. catus GD/7 grown (24 h) on basal YCFA medium with 30 mM acetate, supplemented with either lactate (25 mM), fructose (10 mM) or both substrates (average and s.d. of triplicate experiments).
Figure 3
Figure 3
Phylogenetic tree of deduced protein sequence of lactoyl-CoA dehydratase gene lcdA. Database matches to C. propionicum (AEM62994) of at least 60% as well as the top hit below this cutoff (Desulfosporosinus orientis YP_004972292, 41%) are shown. The lcdA gene fragment of C. lactatifermentans DSM 14214 was sequenced in this study. The number of hits within the metagenomic data set of Qin et al. (2010) with at least 50% identity is indicated to the right (sequences with at least 95% identity were grouped; for a list of all hits see Supplementary Table S5). Sequences from clone library analysis of a human faecal sample (⩾95% identity grouped) are shaded. Grey tree branches indicate genes with lower identity to C. propionicum assumed not to be bona fide lcdA genes.
Figure 4
Figure 4
Phylogenetic tree of deduced protein sequence of CoA-dependent propionaldehyde dehydrogenase pduP. Database matches to R. inulinivorans (ABC25528) of at least 60% as well as the top hits below this cutoff (Clostridium methylpentosum ZP_03705305, 57% Geobacillus thermoglucosidasius YP_004587980, 54%) are shown. The number of hits within the metagenomic data set of Qin et al. (2010) with at least 55% identity is indicated to the right (sequences with at least 95% identity were grouped; for a list of all hits see Supplementary Table S6). Numbers of sequences from clone library analysis of a human faecal sample (⩾95% identity grouped) are shaded. Grey tree branches indicate gene with lower identity to R. inulinivorans assumed not to be bona fide pduP genes.
Figure 5
Figure 5
Distribution of different pathways for propionate and butyrate formation in dominant human gut bacteria, based on genome searches of corresponding genes (Table 2; note that no sequence information is currently available for C. lactatifermentans), metagenomic mining (Figures 3 and 4) and validation of degenerate primers (Supplementary Table S1). C. lactatifermentans and M elsdenii originate from animal hosts (chicken and sheep, respectively). They are included as closely related bacteria are carriers of the acrylate pathway based on human metagenome mining (Figure 3). 16S rRNA sequences were obtained from the Ribosomal Database Project (Cole et al., 2009). Phylogenetic assignment—Lach.: Lachnospiraceae, Rum.: Ruminococcaceae, Neg.: Negativicutes, Ver.: Verrucomicrobia, Bact.: Bacteroidetes. P1–P3, B1–B2: Propionate and butyrate pathways as per Table 2. Question marks indicate the presence of genes with ⩾50% sequence identity (Table 2). As M. elsdenii is known to produce butyrate and A. munciniphila propionate, this has been taken into consideration for the assignment of pathways.

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