Bacteroides thetaiotaomicron fosters the growth of butyrate-producing anaerostipes caccae in the presence of lactose and total human milk carbohydrates

Loo Wee Chia, Marko Mank, Bernadet Blijenberg, Steven Aalvink, Roger S. Bongers, Bernd Stahl, Jan Knol, Clara Belzer*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The development of infant gut microbiota is strongly influenced by nutrition. Human milk oligosaccharides (HMOSs) in breast milk selectively promote the growth of glycan-degrading microbes, which lays the basis of the microbial network. In this study, we investigated the trophic interaction between Bacteroides thetaiotaomicron and the butyrate-producing Anaerostipes caccae in the presence of early-life carbohydrates. Anaerobic bioreactors were set up to study the monocultures of B. thetaiotaomicron and the co-cultures of B. thetaiotaomicron with A. caccae in minimal media supplemented with lactose or a total human milk carbohydrate fraction. Bacterial growth (qPCR), metabolites (HPLC), and HMOS utilization (LC-ESI-MS2) were monitored. B. thetaiotaomicron displayed potent glycan catabolic capability with differential preference in degrading specific low molecular weight HMOSs, including the neutral trioses (2-FL and 3-FL), neutral tetraoses (DFL, LNT, LNnT), neutral pentaoses (LNFP I, II, III, V), and acidic trioses (3-SL and 6-SL). In contrast, A. caccae was not able to utilize lactose and HMOSs. However, the signature metabolite of A. caccae, butyrate, was detected in co-culture with B. thetaiotaomicron. As such, A. caccae cross-fed on B. thetaiotaomicron-derived monosaccharides, acetate, and d-lactate for growth and concomitant butyrate production. This study provides a proof of concept that B. thetaiotaomicron could drive the butyrogenic metabolic network in the infant gut.

Original languageEnglish
Article number1513
Pages (from-to)1-13
Number of pages13
JournalMicroorganisms
Volume8
Issue number10
DOIs
Publication statusPublished - Oct 2020

Keywords

  • Bifidobacteria
  • Cross-feeding
  • D-lactate
  • Human milk oligosaccharides
  • Lactose

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