Abstract

Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (H2S), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and H2S production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of H2S in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions.

Highlights

  • Dietary habits largely modulate the highly personalized composition and temporal dynamics of the human intestinal microbiota and influence disease risk [1,2,3]

  • SQ is cooperatively metabolized in fimo mainly by E. rectale and B. wadsworthia to acetate and H2S

  • To investigate SQ degradation by human gut microbiota, we constructed triplicate anoxic microcosms with fecal slurries mixed from eight vegetarians and incubated them with SQ (10 mM) or control substrates (Fig. S1A)

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Summary

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Dietary habits largely modulate the highly personalized composition and temporal dynamics of the human intestinal microbiota and influence disease risk [1,2,3]. Studies on the catabolism of dietary SQDG by animals are scarce; in guinea pigs SQDG is deacylated via host-derived lipases to sulfoquinovosyl glycerol (SQG) [11]. It is not known whether host tissues are able to metabolize SQG or SQ. Because SQDG is a frequent compound in a vegetarian diet and some gut bacteria have the catabolic potential for complete degradation of SQ to H2S via interspecies cross-feeding of 3-sulfolactate or DHPS, SQ could be a so far overlooked green-dietderived source of H2S in the gut. By targeted physiological experiments with human fecal microcosms and monoand co-cultures and by re-analysis of large metagenome and metatranscriptome datasets from human fecal samples, we reveal the identity of bacteria involved in complete degradation of SQ to H2S, the activity of the underlying pathways, and provide evidence for their importance for the microbial processes in the gut

Materials and methods
Results and discussion
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