Xylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymes

Zhang, Meiling; Chekan, Jonathan R.; Dodd, Dylan; Hong, Pei‐Ying; Radlinski, Lauren C.; Revindran, Vanessa; Nair, Satish K.; Mackie, Roderick I.; Cann, Isaac

doi:10.1073/pnas.1406156111

Cited by 135 publications

(143 citation statements)

References 55 publications

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“…However, this interrupted domain structure was first noted in rumen Prevotella ruminicola GH10 xylanases [64] and more recently in the GH10 xylanases from B. ovatus [34] and B. intestinalis [65]. While the full-length protein structures of these GH10 enzymes have not been determined we hypothesize that like SusG, the CBMs are simply appended from the catalytic domain with minimal disruption of the GH10 protein fold.…”

Section: Susg Is a Novel Gh13 Amylase Required For Starch Utilizationmentioning

confidence: 84%

The Sus operon: a model system for starch uptake by the human gut Bacteroidetes

Foley

Cockburn

Koropatkin

2016

Cell. Mol. Life Sci.

200

157

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Resident bacteria in the densely populated human intestinal tract must efficiently compete for carbohydrate nutrition. The Bacteroidetes, a dominant bacterial phylum in the mammalian gut, encode a plethora of discrete polysaccharide utilization loci (PULs) that are selectively activated to facilitate glycan capture at the cell surface. The most well-studied PUL-encoded glycan-up-take system is the starch utilization system (Sus) of Bacteroides thetaiotaomicron. The Sus includes the requisite proteins for binding and degrading starch at the surface of the cell preceding oligosaccharide transport across the outer membrane for further depolymerization to glucose in the periplasm. All mammalian gut Bacteroidetes possess analogous Sus-like systems that target numerous diverse glycans. In this review, we discuss what is known about the eight Sus proteins of B. thetaiotaomicron that define the Sus-like paradigm of nutrient acquisition that is exclusive to the Gram-negative Bacteroidetes. We emphasize the well-characterized outer membrane proteins SusDEF and the α-amylase SusG, each of which have unique structural features that allow them to interact with starch on the cell surface. Despite the apparent redundancy in starch-binding sites among these proteins, each has a distinct role during starch catabolism. Additionally, we consider what is known about how these proteins dynamically interact and cooperate in the membrane and propose a model for the formation of the Sus outer membrane complex.

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Section: Susg Is a Novel Gh13 Amylase Required For Starch Utilizationmentioning

confidence: 84%

The Sus operon: a model system for starch uptake by the human gut Bacteroidetes

Foley

Cockburn

Koropatkin

2016

Cell. Mol. Life Sci.

200

157

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“…Different models were built from the X-ray coordinates of the carbohydrate-binding module (CBM) of the glycoside hydrolase family 10 protein from Prevotella bryantii B14 (PDB code 4MGQ) and Bacteroides intestinalis (PDB code 4QPW) (Zhang et al, 2014), and the CBM4-2 of the xylanase from Rhodothermus marinus (PDB code 1K42) (Simpson et al, 2002). Finally, a hybrid model of the proteins was built using the different previous models.…”

Section: Molecular Modellingmentioning

confidence: 99%

Evolution and structural diversification ofNictaba-like lectin genes in food crops with a focus on soybean (Glycine max)

Holle¹,

Rougé²,

Damme³

2017

Ann Bot

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Background and Aims The Nictaba family groups all proteins that show homology to Nictaba, the tobacco lectin. So far, Nictaba and an Arabidopsis thaliana homologue have been shown to be implicated in the plant stress response. The availability of more than 50 sequenced plant genomes provided the opportunity for a genome-wide identification of Nictaba-like genes in 15 species, representing members of the Fabaceae, Poaceae, Solanaceae, Musaceae, Arecaceae, Malvaceae and Rubiaceae. Additionally, phylogenetic relationships between the different species were explored. Furthermore, this study included domain organization analysis, searching for orthologous genes in the legume family and transcript profiling of the Nictaba-like lectin genes in soybean.Methods Using a combination of BLASTp, InterPro analysis and hidden Markov models, the genomes of Medicago truncatula, Cicer arietinum, Lotus japonicus, Glycine max, Cajanus cajan, Phaseolus vulgaris, Theobroma cacao, Solanum lycopersicum, Solanum tuberosum, Coffea canephora, Oryza sativa, Zea mays, Sorghum bicolor, Musa acuminata and Elaeis guineensis were searched for Nictaba-like genes. Phylogenetic analysis was performed using RAxML and additional protein domains in the Nictaba-like sequences were identified using InterPro. Expression analysis of the soybean Nictaba-like genes was investigated using microarray data.Key Results Nictaba-like genes were identified in all studied species and analysis of the duplication events demonstrated that both tandem and segmental duplication contributed to the expansion of the Nictaba gene family in angiosperms. The single-domain Nictaba protein and the multi-domain F-box Nictaba architectures are ubiquitous among all analysed species and microarray analysis revealed differential expression patterns for all soybean Nictaba-like genes.Conclusions Taken together, the comparative genomics data contributes to our understanding of the Nictaba-like gene family in species for which the occurrence of Nictaba domains had not yet been investigated. Given the ubiquitous nature of these genes, they have probably acquired new functions over time and are expected to take on various roles in plant development and defence.

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“…Bacteroides ovatus is a common human gut bacterium capable of degrading and growing on several complex plant cell wall polysaccharides, such as hemicellulosic xylan- (8–10) and β-mannan-based dietary fibers (11). A study by Martens et al (10) highlighted the metabolic diversity among Bacteroides species showing that, in contrast to the mucin-degrading Bacteroides thetaiotaomicron, the B. ovatus type strain ATCC 8483 harbors several PULs for utilization of hemicellulosic polysaccharides.…”

Section: Introductionmentioning

confidence: 99%

“…B. ovatus has been shown to have cell-associated β-mannanase activity (12), although the identity of the corresponding enzyme(s) is not known. Some of the proteins encoded within the Bacteroides PULs dedicated to α-mannan (13), xylan (9, 14, 15), and xyloglucan utilization (16) have recently been characterized, demonstrating the diversity in the proteins and enzymes encoded within distinct PULs. The functional mechanisms of β-mannan PULs are, however, much less understood.…”

Section: Introductionmentioning

confidence: 99%

Galactomannan Catabolism Conferred by a Polysaccharide Utilization Locus of Bacteroides ovatus

Bågenholm

Reddy

Bouraoui

et al. 2017

Journal of Biological Chemistry

156

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A recently identified polysaccharide utilization locus (PUL) from Bacteroides ovatus ATCC 8483 is transcriptionally up-regulated during growth on galacto- and glucomannans. It encodes two glycoside hydrolase family 26 (GH26) β-mannanases, BoMan26A and BoMan26B, and a GH36 α-galactosidase, BoGal36A. The PUL also includes two glycan-binding proteins, confirmed by β-mannan affinity electrophoresis. When this PUL was deleted, B. ovatus was no longer able to grow on locust bean galactomannan. BoMan26A primarily formed mannobiose from mannan polysaccharides. BoMan26B had higher activity on galactomannan with a high degree of galactosyl substitution and was shown to be endo-acting generating a more diverse mixture of oligosaccharides, including mannobiose. Of the two β-mannanases, only BoMan26B hydrolyzed galactoglucomannan. A crystal structure of BoMan26A revealed a similar structure to the exo-mannobiohydrolase CjMan26C from Cellvibrio japonicus, with a conserved glycone region (−1 and −2 subsites), including a conserved loop closing the active site beyond subsite −2. Analysis of cellular location by immunolabeling and fluorescence microscopy suggests that BoMan26B is surface-exposed and associated with the outer membrane, although BoMan26A and BoGal36A are likely periplasmic. In light of the cellular location and the biochemical properties of the two characterized β-mannanases, we propose a scheme of sequential action by the glycoside hydrolases encoded by the β-mannan PUL and involved in the β-mannan utilization pathway in B. ovatus. The outer membrane-associated BoMan26B initially acts on the polysaccharide galactomannan, producing comparably large oligosaccharide fragments. Galactomanno-oligosaccharides are further processed in the periplasm, degalactosylated by BoGal36A, and subsequently hydrolyzed into mainly mannobiose by the β-mannanase BoMan26A.

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Xylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymes

Cited by 135 publications

References 55 publications

The Sus operon: a model system for starch uptake by the human gut Bacteroidetes

The Sus operon: a model system for starch uptake by the human gut Bacteroidetes

Evolution and structural diversification ofNictaba-like lectin genes in food crops with a focus on soybean (Glycine max)

Galactomannan Catabolism Conferred by a Polysaccharide Utilization Locus of Bacteroides ovatus

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