Abstract

The various ecological habitats in the human body provide microbes a wide array of nutrient sources and survival challenges. Advances in technology such as DNA sequencing have allowed a deeper perspective into the molecular function of the human microbiota than has been achievable in the past. Here we aimed to examine the enzymes that cleave complex carbohydrates (CAZymes) in the human microbiome in order to determine (i) whether the CAZyme profiles of bacterial genomes are more similar within body sites or bacterial families and (ii) the sugar degradation and utilization capabilities of microbial communities inhabiting various human habitats. Upon examination of 493 bacterial references genomes from 12 human habitats, we found that sugar degradation capabilities of taxa are more similar to others in the same bacterial family than to those inhabiting the same habitat. Yet, the analysis of 520 metagenomic samples from five major body sites show that even when the community composition varies the CAZyme profiles are very similar within a body site, suggesting that the observed functional profile and microbial habitation have adapted to the local carbohydrate composition. When broad sugar utilization was compared within the five major body sites, the gastrointestinal track contained the highest potential for total sugar degradation, while dextran and peptidoglycan degradation were highest in oral and vaginal sites respectively. Our analysis suggests that the carbohydrate composition of each body site has a profound influence and probably constitutes one of the major driving forces that shapes the community composition and therefore the CAZyme profile of the local microbial communities, which in turn reflects the microbiome fitness to a body site.

Highlights

  • Carbohydrates in the form of glycoconjugates, oligo- and polysaccharides represent one of the most diverse sets of molecules on Earth

  • The selective assembly of glycoconjugates and complex carbohydrates is catalyzed by glycosyltransferases (GTs) while the deconstruction of the resulting structures is achieved by specific glycoside hydrolases (GHs) and polysaccharide lyases (PLs)

  • When we compare the mean number of sugar-cleaving enzymes, GHs and PLs, encoded by genomes within a bacterial family, the abundance of these enzymes varies greatly (Table S4)

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Summary

Introduction

Carbohydrates in the form of glycoconjugates, oligo- and polysaccharides represent one of the most diverse sets of molecules on Earth. The selective assembly of glycoconjugates and complex carbohydrates is catalyzed by glycosyltransferases (GTs) while the deconstruction of the resulting structures is achieved by specific glycoside hydrolases (GHs) and polysaccharide lyases (PLs). These enzymes have been termed ‘‘Carbohydrateactive enzymes’’ (CAZymes), which are classified in a number of sequence-based families in the CAZy database (www.cazy.org) [6,7,8,9,10]. Examination of the human genome reveals that it encodes 97 GHs, with only 17 enzymes to breakdown carbohydrate nutrients, nine of which are not yet fully characterized (Table S2) This is a tiny number compared to some of the gut bacteria such as Bacteroides thetaiotaomicron [12], which, alone, encodes over 260 GHs (see www.cazy.org/b135.html)

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