Polysaccharide Utilization Loci: Fueling Microbial Communities

Abstract

The complex carbohydrates of terrestrial and marine biomass represent a rich nutrient source for free-living and mutualistic microbes alike. The enzymatic saccharification of these diverse substrates is of critical importance for fueling a variety of complex microbial communities, including marine, soil, ruminant, and monogastric microbiota. Consequently, highly specific carbohydrate-active enzymes, recognition proteins, and transporters are enriched in the genomes of certain species and are of critical importance in competitive environments. In Bacteroidetes bacteria, these systems are organized as polysaccharide utilization loci (PULs), which are strictly regulated, colocalized gene clusters that encode enzyme and protein ensembles required for the saccharification of complex carbohydrates. This review provides historical perspectives and summarizes key findings in the study of these systems, highlighting a critical shift from sequence-based PUL discovery to systems-based analyses combining reverse genetics, biochemistry, enzymology, and structural biology to precisely illuminate the molecular mechanisms underpinning PUL function. The ecological implications of dynamic PUL deployment by key species in the human gastrointestinal tract are explored, as well as the wider distribution of these systems in other gut, terrestrial, and marine environments.

Molecular Mechanism by which Prominent Human Gut Bacteroidetes Utilize Mixed-Linkage Beta-Glucans, Major Health-Promoting Cereal Polysaccharides

“…6), analogous to that of other PUL-encoded systems (Grondin et al, 2017). Thus, BoGH16 MLG is anchored to the outer membrane where it plays a leading role in fragmenting large MLG polysaccharide chains (typical d.p.…”

“…Analogous to the archetypal Bacteroides thetaiotaomicron starch utilization system (Sus), a hallmark of all Bacteroidetes PULs is the organization of genes clustered around tandem susC / susD homologs (encoding a TonB dependent transporter, TBDT, and a cell-surface glycan-binding protein, SGBP, respectively) (Martens et al, 2009). Additional co-localized and co-regulated SGBP(s), a cohort of enzymes, and a transcriptional regulator typically make up a machinery that acts in concert to sense, break down, and import complex glycans (Grondin et al, 2017; Hemsworth et al, 2016). Many such PULs, each targeting specific glycan structures, have been identified by genomics and transcriptomics (see, e.g.…”

“…Many such PULs, each targeting specific glycan structures, have been identified by genomics and transcriptomics (see, e.g. , the seminal study by (Martens et al, 2011), but detailed functional characterization lags severely behind (reviewed in (Grondin et al, 2017; Martens et al, 2014)). Developing a precise understanding of the molecular details of complex glycan utilization by individual members of the microbiota is essential to designing targeted therapies based on prebiotics, probiotics, and synbiotics (Ciorba, 2012; Slavin, 2013), as well as novel therapeutic interventions.…”

Receptor uptake arrays for vitamin B12, siderophores, and glycans shape bacterial communities

“…I limit my discussion to a few specific challenges of receptor array design, broadening my prior discussions of corrinoids and siderophores. Many excellent reviews of glycan catabolism have been published recently (e.g., Grondin et al., ; Hamaker & Tuncil, ; Martens, Kelly, Tauzin, & Brumer, ).…”

“…In habitats with diverse glycan sources, such as the mammalian gut, bacteria often express broad glycan receptor arrays. For example, many species of Bacteroidetes have diverse Polysaccharide Utilization Loci (PUL) gene clusters (Flint, Scott, Duncan, Louis, & Forano, ; Grondin, Tamura, Déjean, Abbott, & Brumer, ; Martens, Koropatkin, Smith, & Gordon, ). Each cluster typically encodes cell surface glycan‐binding proteins that capture specific glycans to initiate catabolism.…”