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. 2006 May;72(5):3593-9.
doi: 10.1128/AEM.72.5.3593-3599.2006.

Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut

Alvaro Belenguer  1 , Sylvia H Duncan, A Graham Calder, Grietje Holtrop, Petra Louis, Gerald E Lobley, Harry J Flint
Affiliations

Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut

Alvaro Belenguer et al. Appl Environ Microbiol. 2006 May.

Abstract

Dietary carbohydrates have the potential to influence diverse functional groups of bacteria within the human large intestine. Of 12 Bifidobacterium strains of human gut origin from seven species tested, four grew in pure culture on starch and nine on fructo-oligosaccharides. The potential for metabolic cross-feeding between Bifidobacterium adolescentis and lactate-utilizing, butyrate-producing Firmicute bacteria related to Eubacterium hallii and Anaerostipes caccae was investigated in vitro. E. hallii L2-7 and A. caccae L1-92 failed to grow on starch in pure culture, but in coculture with B. adolescentis L2-32 butyrate was formed, indicating cross-feeding of metabolites to the lactate utilizers. Studies with [(13)C]lactate confirmed carbon flow from lactate, via acetyl coenzyme A, to butyrate both in pure cultures of E. hallii and in cocultures with B. adolescentis. Similar results were obtained in cocultures involving B. adolescentis DSM 20083 with fructo-oligosaccharides as the substrate. Butyrate formation was also stimulated, however, in cocultures of B. adolescentis L2-32 grown on starch or fructo-oligosaccharides with Roseburia sp. strain A2-183, which produces butyrate but does not utilize lactate. This is probably a consequence of the release by B. adolescentis of oligosaccharides that are available to Roseburia sp. strain A2-183. We conclude that two distinct mechanisms of metabolic cross-feeding between B. adolescentis and butyrate-forming bacteria may operate in gut ecosystems, one due to consumption of fermentation end products (lactate and acetate) and the other due to cross-feeding of partial breakdown products from complex substrates.

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Figures

FIG. 1.
FIG. 1.
Schematic representation of the model used for the C2 flows. Fbl, flow of C2 from lactate to butyrate via acetyl-CoA without exchange with exogenous acetate; Fal, flow of C2 from lactate to acetate; Fba, flow of C2 from acetate to butyrate.
FIG. 2.
FIG. 2.
Changes in butyrate (closed symbols) and lactate (open symbols) concentrations during incubation of monocultures of B. adolescentis L2-32 (circles), E. hallii L2-7 (triangles), and their cocultures (squares) on potato starch at either pH 5.7 (A) or 6.5 (B).
FIG. 3.
FIG. 3.
Enrichments of lactate (circles), acetate (triangles), and butyrate (squares) in cocultures of Bifidobacterium adolescentis L2-32 and Eubacterium hallii L2-7 on starch at pH 5.7 following [3-13C]lactate (A) or [1-13C]acetate (B) injection.
FIG. 4.
FIG. 4.
Changes in butyrate (closed symbols) and lactate (open symbols) concentrations during incubation of monocultures of B. adolescentis L2-32 (circles), A. caccae L1-92 (triangles), and their cocultures (squares) on fructo-oligosaccharides at pH 5.7.
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