Bacteroidota polysaccharide utilization system for branched dextran exopolysaccharides from lactic acid bacteria

Nakamura, Shuntaro; Kurata, Rikuya; Tonozuka, Takashi; Funane, Kazumi; Park, Enoch Y.; Miyazaki, Takatsugu

doi:10.1016/j.jbc.2023.104885

Cited by 7 publications

(4 citation statements)

References 89 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…BT4581 produced glucose as the sole degradation product, consistent with another previously characterized Bt protein that belongs to GH97, SusB of the Sus-like system ( 42 ). On the other hand, BT3086 produced glucose and isomaltose as major degradation products, which is again consistent with products formed by exodextranases (GH31) as described previously ( 33 ). Finally, BT3087 treatment of dextran produced not only glucose and isomaltose as major degradation products but also other higher MW oligosaccharides, consistent with previous observations of studies involving GH66 endodextranases ( 33 , 35 ) ( Fig.…”

Section: Resultssupporting

confidence: 90%

“…Like starch, dextran is a polyglucan consisting of two unique glycosidic linkages: an α-1,6-linked backbone along with α-1,3 branches ( 32 ). It is known that the degradation of dextran involves the enzyme dextranase, where they may be further classified into two separate classes: endodextranase or exodextranase ( 33 ). Endodextranases (GH families 31, 49, and 66) act by randomly hydrolyzing the α-(1→6) linkages of dextran, which leads to the formation of isomaltooligosaccharides of various degrees of polymerization, whereas exodextranases (GH families 13, 15, 27, and 49) act on the non-reducing end of dextran, forming glucose, isomaltose, or isomaltotriose as the main degradation products ( 33 ).…”

Section: Introductionmentioning

confidence: 99%

“…It is known that the degradation of dextran involves the enzyme dextranase, where they may be further classified into two separate classes: endodextranase or exodextranase ( 33 ). Endodextranases (GH families 31, 49, and 66) act by randomly hydrolyzing the α-(1→6) linkages of dextran, which leads to the formation of isomaltooligosaccharides of various degrees of polymerization, whereas exodextranases (GH families 13, 15, 27, and 49) act on the non-reducing end of dextran, forming glucose, isomaltose, or isomaltotriose as the main degradation products ( 33 ). Previous works have identified the upregulation of PUL48 in Bt under dextran growth ( 30 , 34 ), which is structurally very similar to a PUL dedicated to the utilization of dextran in the Gram-negative soil bacterium Flavobacterium johnsoniae ( 33 ).…”

Section: Introductionmentioning

confidence: 99%

“…Endodextranases (GH families 31, 49, and 66) act by randomly hydrolyzing the α-(1→6) linkages of dextran, which leads to the formation of isomaltooligosaccharides of various degrees of polymerization, whereas exodextranases (GH families 13, 15, 27, and 49) act on the non-reducing end of dextran, forming glucose, isomaltose, or isomaltotriose as the main degradation products ( 33 ). Previous works have identified the upregulation of PUL48 in Bt under dextran growth ( 30 , 34 ), which is structurally very similar to a PUL dedicated to the utilization of dextran in the Gram-negative soil bacterium Flavobacterium johnsoniae ( 33 ). Both PULs featured a GH66 and a GH31, which likely serve as endodextranase and exodextranase for the hydrolysis of dextran, respectively.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Bacteroides thetaiotaomicron metabolic activity decreases with polysaccharide molecular weight

Wong,

Chillier,

Fischer-Stettler

et al. 2024

mBio

View full text Add to dashboard Cite

The human colon hosts hundreds of commensal bacterial species, many of which ferment complex dietary carbohydrates. To transform these fibers into metabolically accessible compounds, microbes often express a series of dedicated enzymes homologous to the starch utilization system (Sus) encoded in polysaccharide utilization loci (PULs). The genome of Bacteroides thetaiotaomicron ( Bt ), a common member of the human gut microbiota, encodes nearly 100 PULs, conferring a strong metabolic versatility. While the structures and functions of individual enzymes within the PULs have been investigated, little is known about how polysaccharide complexity impacts the function of Sus-like systems. We here show that the activity of Sus-like systems depends on polysaccharide size, ultimately impacting bacterial growth. We demonstrate the effect of size-dependent metabolism in the context of dextran metabolism driven by the specific utilization system PUL48. We find that as the molecular weight of dextran increases, Bt growth rate decreases and lag time increases. At the enzymatic level, the dextranase BT3087, a glycoside hydrolase (GH) belonging to the GH family 66, is the main GH for dextran utilization, and BT3087 and BT3088 contribute to Bt dextran metabolism in a size-dependent manner. Finally, we show that the polysaccharide size-dependent metabolism of Bt impacts its metabolic output in a way that modulates the composition of a producer-consumer community it forms with Bacteroides fragilis . Altogether, our results expose an overlooked aspect of Bt metabolism that can impact the composition and diversity of microbiota. IMPORTANCE Polysaccharides are complex molecules that are commonly found in our diet. While humans lack the ability to degrade many polysaccharides, their intestinal microbiota contain bacterial commensals that are versatile polysaccharide utilizers. The gut commensal Bacteroides thetaiotaomicron dedicates roughly 20% of their genomes to the expression of polysaccharide utilization loci for the broad range utilization of polysaccharides. Although it is known that different polysaccharide utilization loci are dedicated to the degradation of specific polysaccharides with unique glycosidic linkages and monosaccharide compositions, it is often overlooked that specific polysaccharides may also exist in various molecular weights. These different physical attributes may impact their processability by starch utilization system-like systems, leading to differing growth rates and nutrient-sharing properties at the community level. Therefore, understanding how molecular weight impacts utilization by gut microbe may lead to the potential design of novel precision prebiotics.

show abstract