Bacteroidetes bacteria in the soil: Glycan acquisition, enzyme secretion, and gliding motility

Larsbrink, Johan; McKee, Lauren S.

doi:10.1016/bs.aambs.2019.11.001

Cited by 145 publications

(78 citation statements)

References 165 publications

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“…PULs are efficient systems that have been argued to give Bacteroidetes bacteria a competitive edge in nutrient scavenging, whether the organisms reside in the gut or in other environments (18,56), and the importance of both acetyl xylan esterase and feruloyl esterase activities are mirrored by the number of PULs encoding the corresponding CE families (14). Multicatalytic CEs, i.e., comprising two or more CE domains, have to our knowledge only been characterized in our own recent work where two different enzymes composed of CE6-CE1 fusions were investigated (32).…”

Section: Discussionmentioning

confidence: 99%

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

Kmezik

Mazurkewich

Meents

et al. 2021

Journal of Biological Chemistry

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The gut microbiota plays a central role in human health by enzymatically degrading dietary fiber and concomitantly excreting short chain fatty acids that are associated with manifold health benefits. The polysaccharide xylan is abundant in dietary fiber but noncarbohydrate decorations hinder efficient cleavage by glycoside hydrolases (GHs) and need to be addressed by carbohydrate esterases (CEs). Enzymes from carbohydrate esterase families 1 and 6 (CE1 and 6) perform key roles in xylan degradation by removing feruloyl and acetate decorations, yet little is known about these enzyme families especially with regard to their diversity in activity. Bacteroidetes bacteria are dominant members of the microbiota and often encode their carbohydrate-active enzymes in multigene polysaccharide utilization loci (PULs). Here we present the characterization of three CEs found in a PUL encoded by the gut Bacteroidete Dysgonomonas mossii . We demonstrate that the CEs are functionally distinct, with one highly efficient CE6 acetyl esterase and two CE1 enzymes with feruloyl esterase activities. One multidomain CE1 enzyme contains two CE1 domains: an N-terminal domain feruloyl esterase, and a C-terminal domain with minimal activity on model substrates. We present the structure of the C-terminal CE1 domain with the carbohydrate-binding module that bridges the two CE1 domains, as well as a complex of the same protein fragment with methyl ferulate. The investment of D. mossii in producing multiple CEs suggests that improved accessibility of xylan for GHs and cleavage of covalent polysaccharide-polysaccharide and lignin-polysaccharide bonds are important enzyme activities in the gut environment.

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Section: Discussionmentioning

confidence: 99%

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

Kmezik

Mazurkewich

Meents

et al. 2021

Journal of Biological Chemistry

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“…The presumed biological role of GEs would indicate that the target substrate(s) of Be CE15A is found in large LCCs that are unlikely to be imported into the periplasm. Conversely, the Rex activity of Be Rex8A would be more in keeping with how final degradation of poly- and oligosaccharides in PULs is believed to mainly occur in the periplasm to prevent “leakage” of metabolizable sugars to surrounding cells 8 , 9 , 18 , 19 . The low GE activity of the enzyme and atypical active site setup might indicate that GlcA in xylan can be esterified with as of yet unidentified moieties that are hydrolyzed in the periplasm by B. eggerthii .…”

Section: Resultsmentioning

confidence: 99%

“…To facilitate the complete degradation of recalcitrant dietary fiber, many Bacteroidetes species utilize polysaccharide utilization loci (PULs) 7 , which are discrete gene clusters encoding all proteins necessary to metabolize a specific polysaccharide 8 , 9 . The starch utilization system (Sus) from the anaerobic human gut symbiont Bacteroides thetaiotaomicron was the first PUL described and serves as a template for the identification and description of new PULs 10 , 11 .…”

Section: Introductionmentioning

confidence: 99%

Characterization of a novel multidomain CE15-GH8 enzyme encoded by a polysaccharide utilization locus in the human gut bacterium Bacteroides eggerthii

Kmezik

Krska

Mazurkewich

et al. 2021

Sci Rep

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Bacteroidetes are efficient degraders of complex carbohydrates, much thanks to their use of polysaccharide utilization loci (PULs). An integral part of PULs are highly specialized carbohydrate-active enzymes, sometimes composed of multiple linked domains with discrete functions—multicatalytic enzymes. We present the biochemical characterization of a multicatalytic enzyme from a large PUL encoded by the gut bacterium Bacteroides eggerthii. The enzyme, BeCE15A-Rex8A, has a rare and novel architecture, with an N-terminal carbohydrate esterase family 15 (CE15) domain and a C-terminal glycoside hydrolase family 8 (GH8) domain. The CE15 domain was identified as a glucuronoyl esterase (GE), though with relatively poor activity on GE model substrates, attributed to key amino acid substitutions in the active site compared to previously studied GEs. The GH8 domain was shown to be a reducing-end xylose-releasing exo-oligoxylanase (Rex), based on having activity on xylooligosaccharides but not on longer xylan chains. The full-length BeCE15A-Rex8A enzyme and the Rex domain were capable of boosting the activity of a commercially available GH11 xylanase on corn cob biomass. Our research adds to the understanding of multicatalytic enzyme architectures and showcases the potential of discovering novel and atypical carbohydrate-active enzymes from mining PULs.

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“…Bacteroidota were also an active and frequently infected bacterial phylum that increased in abundance through time; of this group, all the infected MAGs shared taxonomic affiliation to the order Bacteroidales. Most of these bacteria are obligate anaerobes and known for their diverse arrays of carbohydrate-active enzymes arranged into polysaccharide utilization loci and fermentation [87, 88]. Many active MAGs within this group had the genomic capacity for polysaccharide degradation (e.g., ICE 1 encoded pectin degradation protein KdgF) and all encoded genes for lactate fermentation (Table S8).…”

Section: Discussionmentioning

confidence: 99%

Ecology of active viruses and their bacterial hosts in frozen Arctic peat soil revealed with H₂¹⁸O stable isotope probing metagenomics

Trubl

Kimbrel

Liquet-Gonzalez

et al. 2021

Preprint

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Winter soil processes are critical to the carbon balance of northern ecosystems, yet the microbial ecology governing biogeochemical cycling in frozen soils is largely unknown. We used stable isotope probing targeted metagenomics to reveal the genomic potential of active microbial populations, with an emphasis on viruses, in soils. Peat soils were incubated under simulated winter conditions (subzero and anoxic) with H218O or natural abundance water for 184 and 370 days. Isotope incorporation revealed 46 active bacterial populations (MAGs; spanning 9 bacterial phyla) and 243 active viral populations (vOTUs). Active hosts were predicted for 33% of the active vOTUs and were some of the most abundant MAGs, having capacity for fermentation and carbohydrate utilization. Additionally, almost one-third of vOTUs carried auxiliary metabolic genes spanning five functional categories, highlighting the potential impact of viruses in microbial biogeochemistry. CO2 production throughout the incubation supports our evidence of microbial activities under winter conditions. Our results revealed a multi-trophic and changing microbial community in tandem with a changing viral community targeting dominant active bacteria consistent with the “kill-the-winner” hypothesis. These data have important implications for low-temperature soil processes in northern peatlands and reveal active host-linked soil viral ecology, with potential multifaceted biogeochemical impacts.

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Bacteroidetes bacteria in the soil: Glycan acquisition, enzyme secretion, and gliding motility

Cited by 145 publications

References 165 publications

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

Characterization of a novel multidomain CE15-GH8 enzyme encoded by a polysaccharide utilization locus in the human gut bacterium Bacteroides eggerthii

Ecology of active viruses and their bacterial hosts in frozen Arctic peat soil revealed with H₂¹⁸O stable isotope probing metagenomics

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Bacteroidetes bacteria in the soil: Glycan acquisition, enzyme secretion, and gliding motility

Cited by 145 publications

References 165 publications

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

A polysaccharide utilization locus from the gut bacterium Dysgonomonas mossii encodes functionally distinct carbohydrate esterases

Characterization of a novel multidomain CE15-GH8 enzyme encoded by a polysaccharide utilization locus in the human gut bacterium Bacteroides eggerthii

Ecology of active viruses and their bacterial hosts in frozen Arctic peat soil revealed with H218O stable isotope probing metagenomics

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Ecology of active viruses and their bacterial hosts in frozen Arctic peat soil revealed with H₂¹⁸O stable isotope probing metagenomics