Dietary fiber intake, gut microbiome, and chronic systemic inflamation

Background: Higher intake of dietary fiber is associated with decreased risk of chronic inflammatory diseases. Dietary fiber may abrogate chronic systemic inflammation induced by factors including dysbiotic gut communities. Data regarding the detailed influences of long-term and recent intake of differing fiber sources in human populations are lacking.

Methods: We collected longitudinal stool samples from 307 healthy men in the Health Professionals Follow-up Study (up to 4 stools over 6 months, in 2012-2013) totaling 913 metagenomes and 341 metatranscriptomes with concurrent measurement of the circulating inflammatory biomarker, high- sensitivity C-reactive protein (CRP). We captured recent dietary fiber intake using a 7-day dietary record at the time of stool collection and long-term intake using validated semi-quantitative food frequency questionnaires (FFQs) every 4 years since 1986. Dietary fiber captured by FFQ was further subclassified into their food sources (fruit, cereal, and vegetable). We used transformed generalized linear mixed models via MaAsLin2 to examine the relationship between dietary fiber and microbial features with adjustment for covariates.

Results: Both recent and long-term higher dietary fiber intake were associated with shifts in Clostridiales, including increases of Eubacterium eligens, Faecalibacterium prausnitzii, and genus Roseburia, but also decreases in Clostridium, Lachnospiraceae, and Ruminococcus. Greater fiber intake was also associated with greater relative abundances of Haemophilus parainfluenzae and Bacteroides species, including B. cellulosilyticus. In addition to taxonomic composition, dietary fiber intake was associated with a large number of functional genomic features. Microbial influences were varying according to fiber sources, with predominant effects deriving from pectin and fruit fiber. For instance, abundances of E. eligens and F. prausnitzii as well as their functions in the degradation of polysaccharides as represented by polysaccharide lyase family 9 were enriched in participants with greater dietary fiber and pectin intake. Higher CRP was associated with enrichment of Bacteroides uniformis and Barnesiella intestinihominis and depletion of Lachnospiraceae_bacterium_3_1_46faa, E. eligens, and Bifidobacterium bifidum. The association between recent fiber intake and plasma levels of CRP was significantly modified by gut microbial composition and specifically presence/absence of Prevotella copri (P-interaction=0.01). A stronger inverse association was observed among participants who did not have P. copri.

Conclusions: Our findings offer evidence supporting a fiber-gut microbiome interaction relevant to human chronic systemic inflammation. The differential effects of fiber according to its food source may inform personalized approaches to gut microbial modulation.