The human gut microbiota is an important metabolic organ. However, little is known about how its individual species interact, establish dominant positions, and respond to changes in environmental factors such as diet. In the current study, gnotobiotic mice colonized with a simplified model microbiota composed of 12 sequenced human gut bacterial species were fed oscillating diets of disparate composition. Rapid, reproducible and reversible changes in community structure were observed. Time series microbial RNA-Seq analyses revealed staggered functional responses to diet shifts throughout the community that were heavily focused on carbohydrate and amino acid metabolism. High-resolution shotgun metaproteomics confirmed many of these responses at a protein level. One member, Bacteroides cellulosilyticus WH2, proved exceptionally fit regardless of diet. Its genome encoded more carbohydrate active enzymes than any known Bacteroidetes. Transcriptional profiling indicated that B. cellulosilyticus WH2 is an adaptive forager that tailors its versatile carbohydrate utilization strategy to available dietary polysaccharides, with a strong emphasis on plant-derived xylans abundant in dietary staples like cereal grains. Two highly expressed, diet-specific polysaccharide utilization loci (PULs) in B. cellulosilyticus WH2 were identified, one with characteristics of xylan utilization systems. Introduction of a B. cellulosilyticus WH2 library comprising 26,750 isogenic transposon mutants into gnotobiotic mice along with other model community members confirmed that these loci represent critical diet-specific fitness determinants. The specific carbohydrates that trigger overexpression of these two loci and many of the organism's 111 other predicted PULs were identified by RNA-Seq during in vitro growth on 31 distinct carbohydrate substrates, allowing us to better interpret in vivo RNA-Seq and proteomics data. These results offer insight into how gut microbes adapt to dietary perturbations, both at a community level and from the perspective of a well-adapted symbiont with exceptional saccharolytic capabilities, and illustrate the value of studying defined models of the human gut microbiota.