Pectins are a major dietary nutrient source for the human gut microbiota (HGM). The prominent gut microbe Bacteroides thetaiotaomicron was recently shown to encode the founding member (BT1017) of a new family of pectin methylesterases (PMEs) essential for the metabolism of the complex pectin rhamnogalacturonan-II (RG-II). However, biochemical and structural knowledge of this family is lacking. Here, we showed that BT1017 is critical for the metabolism of an RG-II-derived oligosaccharide ?BT1017oligoB generated by a BT1017 deletion mutant (?BT1017) during growth on carbohydrate extract from apple juice. Structural analyses of ?BT1017oligoB using a combination of enzymatic, mass spectrometric and nuclear magnetic resonance approaches revealed that it is a bi-methylated nona-oligosaccharide GlcA-ß1,4-(2-O-Me-Xyl-a1,3)-Fuc-a1,4-(GalA-ß1,3)-Rha-a1,3-Api-ß1,2-(Araf-a1,3)-(GalA-a1,4)-GalA containing components of the RG-II backbone and its side chains. We showed that the catalytic module of BT1017 adopts an alpha/beta (a/ß) hydrolase fold, consisting of a central twisted 10-stranded ß-sheet sandwiched by several a-helices. This constitutes a new fold for PMEs, which are predominantly right-handed ß-helical proteins. Bioinformatics analyses revealed that the family is dominated by sequences from the prominent genera of the HGM, including Bacteroides and Prevotella Our results not only highlight the critical role played by this family of enzymes in pectin metabolism but provide new insights into the molecular basis of the adaptation of B. thetaiotaomicron to the human gut.