Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan

Attia, Mohamed Adel; Brumer, Harry

doi:10.1016/j.sbi.2016.07.005

Cited by 35 publications

(29 citation statements)

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“…The present model for XyG utilization by C. japonicus involves a xyloglucan utilization locus (XyGUL) (Fig. ) that encodes three periplasmic, side‐chain‐cleaving GHs (a GH31 α‐xylosidase, a GH35 β‐galactosidase and a GH95 α‐ l ‐fucosidase) and a predicted outer‐membrane TonB dependent transporter (TBDT) for periplasmic uptake and saccharification of XyGOs produced by extracellular endo‐xyloglucanases (Larsbrink et al ., ; Attia and Brumer, ; Attia et al ., ). Despite extensive efforts illuminating the concerted action of these players, the identity of the β‐glucosidase(s) necessary for the complete deconstruction of the β(1→4)‐linked XyGO backbone was heretofore unknown.…”

Section: Discussionmentioning

confidence: 99%

Comprehensive functional characterization of the glycoside hydrolase family 3 enzymes from Cellvibrio japonicus reveals unique metabolic roles in biomass saccharification

Nelson

Attia

Rogowski

et al. 2017

Environmental Microbiology

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SUMMARY Lignocellulose degradation is central to the carbon cycle and renewable biotechnologies. The xyloglucan (XyG), β(1→3)/β(1→4) mixed-linkage glucan (MLG), and β(1→3) glucan components of lignocellulose represent significant carbohydrate energy sources for saprophytic microorganisms. The bacterium Cellvibrio japonicus has a robust capacity for plant polysaccharide degradation, due to a genome encoding a large contingent of Carbohydrate-Active Enzymes (CAZymes), many of whose specific functions remain unknown. Using a comprehensive genetic and biochemical approach we have delineated the physiological roles of the four C. japonicus Glycoside Hydrolase Family 3 (GH3) members on diverse β-glucans. Despite high protein sequence similarity and partially overlapping activity profiles on disaccharides, these β-glucosidases are not functionally equivalent. Bgl3A has a major role in MLG and sophorose utilization, and supports β(1→3) glucan utilization, while Bgl3B underpins cellulose utilization and supports MLG utilization. Bgl3C drives β(1→3) glucan utilization. Finally, Bgl3D is the crucial β-glucosidase for XyG utilization. This study not only sheds the light on the metabolic machinery of C. japonicus, but also expands the repertoire of characterized CAZymes for future deployment in biotechnological applications. In particular, the precise functional analysis provided here serves as a reference for informed bioinformatics on the genomes of other Cellvibrio and related species.

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Section: Discussionmentioning

confidence: 99%

Comprehensive functional characterization of the glycoside hydrolase family 3 enzymes from Cellvibrio japonicus reveals unique metabolic roles in biomass saccharification

Nelson

Attia

Rogowski

et al. 2017

Environmental Microbiology

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“…In light of the widespread distribution of MLG and XyG across the plant kingdom, there is a clear and pressing need to achieve a comprehensive understanding of the enzymology of the biosynthesis and biodegradation of these key matrix glycans (Fincher, 2009;Burton et al, 2010;Attia and Brumer, 2016;Pauly and Keegstra, 2016). Endogenous endohydrolysis of MLG, the key initial step in glucose mobilization, was previously thought to be catalyzed exclusively by plant Glycoside Hydrolase Family 17 (GH17) members (Fincher, 2009).…”

Section: Plant Eg16 Members Represent a Unique Class Of Bifunctional mentioning

confidence: 99%

Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases

et al. 2017

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SUMMARY The xyloglucan endo-transglycosylase/hydrolase (XTH) gene family encodes enzymes of central importance to plant cell wall remodelling. The evolutionary history of plant XTH gene products is incompletely understood vis-à-vis the larger body of bacterial endo-glycanases in Glycoside Hydrolase Family 16 (GH16). To provide molecular insight into this issue, high-resolution X-ray crystal structures and detailed enzyme kinetics of an extant transitional plant endo-glucanase (EG) were determined. Functionally intermediate between plant XTH gene products and bacterial licheninases of GH16, Vitis vinifera EG16 (VvEG16) effectively catalyzes the hydrolysis of the backbones of two dominant plant cell wall matrix glycans, xyloglucan (XyG) and β(1,3)/β(1,4)-mixed-linkage glucan (MLG). Crystallographic complexes with extended oligosaccharide substrates reveal the structural basis for the accommodation of both unbranched, mixed-linked (MLG) and highly decorated, linear (XyG) polysaccharide chains in a broad, extended active-site cleft. Structural comparison with representative bacterial licheninases, a xyloglucan endo-tranglycosylase (XET), and a xyloglucan endo-hydrolase (XEH) outline the functional ramifications of key sequence deletions and insertions across the phylogenetic landscape of GH16. Although the biological role(s) of EG16 orthologs remains to be fully resolved, the present biochemical and tertiary structural characterization provides key insight into plant cell wall enzyme evolution, which will continue to inform genomic analyses and functional studies across species.

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“…The importance of fungal and bacteria α-L-fucosidases in plant polysaccharide degradation, namely, on xyloglucan has been reported previously [10,12]. A secreted α-L-fucosidase belonging to the GH29 family from the plant pathogenic fungus Fusarium graminearum was shown to be active in releasing fucose from a xyloglucan fragment [13].…”

Section: Introductionmentioning

confidence: 88%

“…α-L-fucosidases were also searched in B. xylophilus transcriptome BioProject PRJNA192936 [15] and genome Bioproject PRJEA64437 [2] to look for the characteristic InterPro domain IPR000933 of GH29 [16]. This domain was also searched in other plantparasitic nematodes genomes available from WormBase Parasite [17]: Globodera rostochiensis PRJEB13504-Ro1; G. pallida PRJEB123; Meloidogyne arenaria PRJEB8714; M. floridensis PRJEB6016; M. The importance of fungal and bacteria α-l-fucosidases in plant polysaccharide degradation, namely, on xyloglucan has been reported previously [10,12]. A secreted α-l-fucosidase belonging to the GH29 family from the plant pathogenic fungus Fusarium graminearum was shown to be active in releasing fucose from a xyloglucan fragment [13].…”

Section: In Silico Identification Of Fucosidase Sequencesmentioning

confidence: 99%

α-l-Fucosidases from Bursaphelenchus xylophilus Secretome—Molecular Characterization and Their Possible Role in Breaking Down Plant Cell Walls

Cardoso

Fonseca

Abrantes

2020

Forests

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The pinewood nematode (PWN) Bursaphelenchus xylophilus, the causal agent of the pine wilt disease (PWD), enters above-ground parts of the tree, migrates through the resin canals and feeds on plant cells causing extensive damage. In order to penetrate the cell wall and establish a parasitic relationship with host trees, the PWN needs to secretea mixture of active cell wall degrading enzymes. In maritime pine, Pinus pinaster, which is high susceptible to PWN, xyloglucan is the major hemicellulosic polysaccharide in primary cells. The xyloglucan backbone is susceptible to hydrolysis by numerous endoglucanases, some of them specific to xyloglucan. However, to completely degrade xyloglucan, all substitutions on the glucan backbones must be released, and l-fucose residues in xyloglucan branches are released by α-l-fucosidases. In the present study, the molecular characterization of two α-l-fucosidases found in PWN secretome was performed. Moreover, a novel α-l-fucosidase was identified and its cDNA and gene sequence were determined. The three-dimensional structures of these α-l-fucosidases were predicted and the transcript levels were analyzed, thus providing new insights into fundamental PWN biology and the possible role of these proteins as cell wall degrading enzymes.

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Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan

Cited by 35 publications

References 59 publications

Comprehensive functional characterization of the glycoside hydrolase family 3 enzymes from Cellvibrio japonicus reveals unique metabolic roles in biomass saccharification

Comprehensive functional characterization of the glycoside hydrolase family 3 enzymes from Cellvibrio japonicus reveals unique metabolic roles in biomass saccharification

Crystallographic insight into the evolutionary origins of xyloglucan endotransglycosylases and endohydrolases

α-l-Fucosidases from Bursaphelenchus xylophilus Secretome—Molecular Characterization and Their Possible Role in Breaking Down Plant Cell Walls

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