Phylogenetic distribution of three pathways for propionate production within the human gut microbiota

Nicole Reichardt, Sylvia Helen Duncan, Pauline Young, Alvaro Belenguer, Carol McWilliam Leitch, Karen Patricia Scott, Harry J Flint, Petra Louis

Research output: Contribution to journalArticlepeer-review

736 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)1323-1335
Number of pages13
JournalThe ISME Journal
Volume8
Issue number6
Early online date20 Feb 2014
DOIs
Publication statusPublished - Jun 2014

Bibliographical note

Acknowledgements: The Rowett Institute of Nutrition and Health receives financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services. Alvaro Belenguer received financial support from the Spanish Ministry of Education and Science. Nicole Reichardt is funded by a Scottish Government Strategic Partnership on Food and Drink Science. We thank Wolfgang Buckel, Douglas Morrison, Tom Preston, Graeme Milligan, Lynda Williams and Janice Drew for helpful discussions, Freda Farquharson for help with bacterial cultures and supply of genomic DNA, Graham Calder and Gerald Lobley for help with stable isotope analysis and Tony Travis for help with bioinformatic analysis

Correction to: The ISME Journal (2014) 8, 1323–1335; doi:10.1038/ismej.2014.14; published online 20 February 2014

Keywords

  • acrylate pathway
  • gut microbiota
  • propanediol pathway
  • propionate
  • succinate pathway

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