Abstract
ABSTRACTThe aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut. Hence, different Fe availabilities were mimicked in an in vitro colonic fermentation model (the polyfermenter intestinal model called PolyFermS) inoculated with immobilized gut microbiota from a child and in batch cultures of the butyrate producer Roseburia intestinalis. Shifts in the microbial community (16S rRNA sequencing and quantitative PCR), metabolic activity (high-performance liquid chromatography), and expression of genes involved in butyrate production were assessed. In the PolyFermS, moderate Fe deficiency resulted in a 1.4-fold increase in butyrate production and a 5-fold increase in butyryl-coenzyme A (CoA):acetate CoA-transferase gene expression, while very strong Fe deficiency significantly decreased butyrate concentrations and butyrate-producing bacteria compared with the results under normal Fe conditions. Batch cultures of R. intestinalis grown in a low-Fe environment preferentially produced lactate and had reduced butyrate and hydrogen production, in parallel with upregulation of the lactate dehydrogenase gene and downregulation of the pyruvate:ferredoxin-oxidoreductase gene. In contrast, under high-Fe conditions, R. intestinalis cultures showed enhanced butyrate and hydrogen production, along with increased expression of the corresponding genes, compared with the results under normal-Fe conditions. Our data reveal the strong regulatory effect of Fe on gut microbiota butyrate producers and on the concentrations of butyrate, which contributes to the maintenance of host gut health.
Highlights
The aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut
The gut microbiota compositions in the control reactor (CR) and TRs under different Fe conditions were determined by 16S rRNA gene sequencing analysis of the combined samples from the last 3 days of each of the 3 fermentation periods (Fig. 2a) and by quantitative PCR (qPCR) analysis of specific bacterial groups
After an initial stabilization period of feeding normal-Fe medium to all reactors for 6 days, the gut microbiota compositions were highly similar in the inoculum reactor (IR), CR, TR1, and TR2 as assessed by qPCR, and the composition was stable over time in the CR, where the Fe concentration of the medium was not changed (Fig. 2a; see Table S1)
Summary
The aim of this study was to investigate the effect of iron (Fe) availability on butyrate production in the complex bacterial ecosystem of the human gut. IMPORTANCE Fe deficiency is one of the most common nutritional deficiencies worldwide and can be corrected by Fe supplementation In this in vitro study, we show that environmental Fe concentrations in a continuous gut fermentation model closely mimicking a child’s gut microbiota strongly affect the composition of the gut microbiome and its metabolic activity, butyrate production. Using a combination of in vivo and in vitro models and human trials, we recently showed strong effects of Fe supplementation and low-Fe conditions on the microbial ecosystem of the gut and, on the production of the short-chain fatty acids (SCFA) acetate, propionate, and butyrate [14,15,16,17]. The degradation of indigestible fibers from the diet by the gut microbiota and the resulting metabolites can contribute an additional 10% of daily dietary energy to the host [18]
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