Bernard Henrissat

Ghent University, Gand, Flanders, Belgium

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Publications (460)2937.64 Total impact

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    ABSTRACT: As the volume of data relating to proteins increases, researchers rely more and more on the analysis of published data, thus increasing the importance of good access to these data that vary from the supplemental material of individual papers, all the way to major reference databases with professional staff and long-term funding. Specialist protein resources fill an important middle ground, providing interactive web interfaces to their databases for a focused topic or family of proteins, using specialised approaches that are not feasible in the major reference databases. Many are labours of love, run by a single lab with little or no dedicated funding and there are many challenges to building and maintaining them. This perspective arose from a meeting of several specialist protein resources and major reference databases held at the Wellcome Trust Genome Campus (Cambridge, UK) on the 11th and 12th of August 2014. During this meeting some common key challenges involved in creating and maintaining such resources were discussed, along with various approaches to address them. In laying out these challenges, we aim to inform users about how these issues impact our resources and illustrate ways in which our working together could enhance their accuracy, currency, and overall value. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    Proteins Structure Function and Bioinformatics 03/2015; 83(6). DOI:10.1002/prot.24803 · 2.63 Impact Factor
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    ABSTRACT: A new chitinase-like agglutinin, RobpsCRA, related to family GH18 chitinases, has previously been identified in black locust (Robinia pseudoacacia) bark. The crystal structure of RobpsCRA at 1.85 Å resolution reveals unusual molecular determinants responsible for the lack of its ancestral chitinase activity. Unlike other chitinase-like proteins, which lack chitinase catalytic residues, RobpsCRA has conserved its catalytic machinery. However, concerted rearrangements of loop regions coupled to non-conservative substitutions of aromatic residues central to the chitin-binding groove explain the lack of hydrolytic activity against chitin and the switch towards recognition of high-mannose type N-glycans. Identification of close homologs in flowering plants with conservation of sequence motifs associated to the structural adaptations seen in RobpsCRA defines an emerging class of agglutinins, as emphasized by a phylogenetic analysis, that are likely to share a similar carbohydrate binding specificity for high-mannose type N-glycans. This study illustrates the recent evolution and molecular adaptation of a versatile TIM-barrel scaffold within the ancestral GH18 family. Copyright © 2015 Elsevier Inc. All rights reserved.
    Journal of Structural Biology 02/2015; 190(2). DOI:10.1016/j.jsb.2015.01.013 · 3.23 Impact Factor
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    ABSTRACT: To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall–degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7–38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a ‘symbiosis toolkit’, with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.
    Nature Genetics 02/2015; 47(4). DOI:10.1038/ng.3223 · 29.35 Impact Factor
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    ABSTRACT: Lytic polysaccharide monooxygenases (LPMOs) are recently discovered enzymes that oxidatively deconstruct polysaccharides. LPMOs are fundamental in the effective utilization of these substrates by bacteria and fungi; moreover, the enzymes have significant industrial importance. We report here the activity, spectroscopy and three-dimensional structure of a starch-active LPMO, a representative of the new CAZy AA13 family. We demonstrate that these enzymes generate aldonic acid-terminated malto-oligosaccharides from retrograded starch and boost significantly the conversion of this recalcitrant substrate to maltose by β-amylase. The detailed structure of the enzyme’s active site yields insights into the mechanism of action of this important class of enzymes.
    Nature Communications 01/2015; 6. DOI:10.1038/ncomms6961 · 11.47 Impact Factor
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    ABSTRACT: Clonostachys rosea is a mycoparasitic fungus that can control several important plant diseases. Here we report on the genome sequencing of C. rosea and a comparative genome analysis, in order to resolve the phylogenetic placement of C. rosea and to study the evolution of mycoparasitism as a fungal lifestyle. The genome of C. rosea is estimated to 58.3 Mbp, and contains 14268 predicted genes. A phylogenomic analysis shows that C. rosea clusters as sister taxon to plant pathogenic Fusarium species, with mycoparasitic/saprotrophic Trichoderma species in an ancestral position. A comparative analysis of gene family evolution reveals several distinct differences between the included mycoparasites. C. rosea contains significantly more ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome P450 monooxygenases, pectin lyases, glucose-methanol-choline oxidoreductases and lytic polysaccharide monooxygenases compared with other fungi in the Hypocreales. Interestingly, the increase of ABC transporter gene number in C. rosea is associated with phylogenetic subgroups B (multidrug resistance proteins) and G (pleiotropic drug resistance transporters), while an increase in subgroup C (multidrug resistance-associated proteins) is evident in T. virens. In contrast with mycoparasitic Trichoderma species, C. rosea contains very few chitinases. Expression of six group B and group G ABC transporter genes were induced in C. rosea during exposure to the Fusarium mycotoxin zearalenone, the fungicide Boscalid or metabolites from the biocontrol bacterium Pseudomonas chlororaphis. The data suggests that tolerance towards secondary metabolites is a prominent feature in the biology of C. rosea. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 01/2015; 7(2). DOI:10.1093/gbe/evu292 · 4.23 Impact Factor
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    ABSTRACT: The ascomycete fungus Ophiostoma novo-ulmi is responsible for the pandemic of Dutch Elm Disease that has been ravaging Europe and North America for 50 years. We proceeded to annotate the genome of the O. novo-ulmi strain H327 that was sequenced in 2012. The 31.784 Mb nuclear genome (50.1% GC) is organized into 8 chromosomes containing a total of 8,640 protein-coding genes that we validated with RNA-seq analysis. Approximately 53% of these genes have their closest match to Grosmannia clavigera kw1407, followed by 36% in other close Sordariomycetes, 5% in other Pezizomycotina and surprisingly few (5%) orphans. A relatively small portion (~3.4%) of the genome is occupied by repeat sequences, however the mechanism of repeat-induced point mutation appears active in this genome. Approximately 76% of the proteins could be assigned functions using Gene Ontology analysis; we identified 311 carbohydrate-active enzymes, 48 cytochrome P450s, and 1731 proteins potentially involved in pathogen-host interaction, along with 7 clusters of fungal secondary metabolites. Complementary mating-locus sequencing, mating tests, and culturing in the presence of elm terpenes were conducted. Our analysis identified a specific genetic arsenal impacting the sexual and vegetative growth, phytopathogenicity, and signaling/plant-defense-degradation relationship between O. novo-ulmi and its elm host and insect vectors. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Genome Biology and Evolution 12/2014; 7(2). DOI:10.1093/gbe/evu281 · 4.23 Impact Factor
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    Moran Kopel · William Helbert · Bernard Henrissat · Tirza Doniger · Ehud Banin ·
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    ABSTRACT: We present the draft genome sequence of Pseudoalteromonas sp. strain PLSV, isolated from the feces of an Aplysia sea slug. The addition of the PLSV genome to the existing genomes of three other ulvan-degrading bacterial species will enhance our understanding of ulvan utilization. Copyright © 2014 Kopel et al.
    Genome Announcements 12/2014; 2(6). DOI:10.1128/genomeA.01257-14
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    ABSTRACT: Collectively classified as white-rot fungi, certain basidiomycetes efficiently degrade the major structural polymers of wood cell walls. A small subset of these Agaricomycetes, exemplified by Phlebiopsis gigantea, is capable of colonizing freshly exposed conifer sapwood despite its high content of extractives, which retards the establishment of other fungal species. The mechanism(s) by which P. gigantea tolerates and metabolizes resinous compounds have not been explored. Here, we report the annotated P. gigantea genome and compare profiles of its transcriptome and secretome when cultured on fresh-cut versus solvent-extracted loblolly pine wood. The P. gigantea genome contains a conventional repertoire of hydrolase genes involved in cellulose/hemicellulose degradation, whose patterns of expression were relatively unperturbed by the absence of extractives. The expression of genes typically ascribed to lignin degradation was also largely unaffected. In contrast, genes likely involved in the transformation and detoxification of wood extractives were highly induced in its presence. Their products included an ABC transporter, lipases, cytochrome P450s, glutathione S-transferase and aldehyde dehydrogenase. Other regulated genes of unknown function and several constitutively expressed genes are also likely involved in P. gigantea's extractives metabolism. These results contribute to our fundamental understanding of pioneer colonization of conifer wood and provide insight into the diverse chemistries employed by fungi in carbon cycling processes.
    PLoS Genetics 12/2014; 10(12). DOI:10.1371/journal.pgen.1004759 · 7.53 Impact Factor
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    ABSTRACT: Bacteria play many important roles in animal digestive systems, including the provision of enzymes critical to digestion. Typically, complex communities of bacteria reside in the gut lumen in direct contact with the ingested materials they help to digest. Here, we demonstrate a previously undescribed digestive strategy in the wood-eating marine bivalve Bankia setacea, wherein digestive bacteria are housed in a location remote from the gut. These bivalves, commonly known as shipworms, lack a resident microbiota in the gut compartment where wood is digested but harbor endosymbiotic bacteria within specialized cells in their gills. We show that this comparatively simple bacterial community produces wood-degrading enzymes that are selectively translocated from gill to gut. These enzymes, which include just a small subset of the predicted wood-degrading enzymes encoded in the endosymbiont genomes, accumulate in the gut to the near exclusion of other endosymbiont-made proteins. This strategy of remote enzyme production provides the shipworm with a mechanism to capture liberated sugars from wood without competition from an endogenous gut microbiota. Because only those proteins required for wood digestion are translocated to the gut, this newly described system reveals which of many possible enzymes and enzyme combinations are minimally required for wood degradation. Thus, although it has historically had negative impacts on human welfare, the shipworm digestive process now has the potential to have a positive impact on industries that convert wood and other plant biomass to renewable fuels, fine chemicals, food, feeds, textiles, and paper products.
    Proceedings of the National Academy of Sciences 11/2014; 111(47). DOI:10.1073/pnas.1413110111 · 9.67 Impact Factor
  • Henk Brouwer · Pedro M. Coutinho · Bernard Henrissat · Ronald P. de Vries ·
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    ABSTRACT: Carbohydrate-Active enZymes (CAZymes) form particularly interesting targets to study in plant pathogens. Despite the fact that many CAZymes are pathogenicity factors, oomycete CAZymes have received significantly less attention than effectors in the literature. Here we present an analysis of the CAZymes present in the Phytophthora infestans, Ph. ramorum, Ph. sojae and Pythium ultimum genomes compared to growth of these species on a range of different carbon sources. Growth on these carbon sources indicates that the size of enzyme families involved in degradation of cell-wall related substrates like cellulose, xylan and pectin is not always a good predictor of growth on these substrates. While a capacity to degrade xylan and cellulose exists the products are not fully saccharified and used as a carbon source. The Phytophthora genomes encode larger CAZyme sets when compared to Py. ultimum, and encode putative cutinases, GH12 xyloglucanases and GH10 xylanases that are missing in the Py. ultimum genome. Phytophthora spp. also encode a larger number of enzyme families and genes involved in pectin degradation. No loss or gain of complete enzyme families was found between the Phytophthora genomes, but there are some marked differences in the size of some enzyme families.
    Fungal Genetics and Biology 11/2014; 72. DOI:10.1016/j.fgb.2014.08.011 · 2.59 Impact Factor
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    ABSTRACT: The fungal genus Sporothrix includes at least four human pathogenic species. One of these species, S. brasiliensis, is the causal agent of a major ongoing zoonotic outbreak of sporotrichosis in Brazil. Elsewhere, sapronoses are caused by S. schenckii and S. globosa. The major aims on this comparative genomic study are: 1) to explore the presence of virulence factors in S. schenckii and S. brasiliensis; 2) to compare S. brasiliensis, which is cat-transmitted and infects both humans and cats with S. schenckii, mainly a human pathogen; 3) to compare these two species to other human pathogens (Onygenales) with similar thermo-dimorphic behavior and to other plant-associated Sordariomycetes. The genomes of S. schenckii and S. brasiliensis were pyrosequenced to 17x and 20x coverage comprising a total of 32.3 Mb and 33.2 Mb, respectively. Pair-wise genome alignments revealed that the two species are highly syntenic showing 97.5% average sequence identity. Phylogenomic analysis reveals that both species diverged about 3.8-4.9 MYA suggesting a recent event of speciation. Transposable elements comprise respectively 0.34% and 0.62% of the S. schenckii and S. brasiliensis genomes and expansions of Gypsy-like elements was observed reflecting the accumulation of repetitive elements in the S. brasiliensis genome. Mitochondrial genomic comparisons showed the presence of group-I intron encoding homing endonucleases (HE’s) exclusively in S. brasiliensis. Analysis of protein family expansions and contractions in the Sporothrix lineage revealed expansion of LysM domain-containing proteins, small GTPases, PKS type1 and leucin-rich proteins. In contrast, a lack of polysaccharide lyase genes that are associated with decay of plants was observed when compared to other Sordariomycetes and dimorphic fungal pathogens, suggesting evolutionary adaptations from a plant pathogenic or saprobic to an animal pathogenic life style. Comparative genomic data suggest a unique ecological shift in the Sporothrix lineage from plant-association to mammalian parasitism, which contributes to the understanding of how environmental interactions may shape fungal virulence. . Moreover, the striking differences found in comparison with other dimorphic fungi revealed that dimorphism in these close relatives of plant-associated Sordariomycetes is a case of convergent evolution, stressing the importance of this morphogenetic change in fungal pathogenesis.
    BMC Genomics 10/2014; 15:943. DOI:10.1186/1471-2164-15-943 · 3.99 Impact Factor
  • Nicolas Terrapon · Vincent Lombard · Harry J Gilbert · Bernard Henrissat ·
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    ABSTRACT: Motivation: A bacterial polysaccharide utilization locus (PUL) is a set of physically linked genes that orchestrate the breakdown of a specific glycan. PULs are prevalent in the Bacteroidetes phylum and are key to the digestion of complex carbohydrates, notably by the human gut microbiota. A given Bacteroidetes genome can encode dozens of different PULs whose boundaries and precise gene content are difficult to predict. Results: Here, we present a fully automated approach for PUL prediction using genomic context and domain annotation alone. By combining the detection of a pair of marker genes with operon prediction using intergenic distances, and queries to the carbohydrate-active enzymes database (, our predictor achieved above 86% accuracy in two Bacteroides species with extensive experimental PUL characterization. Availability and implementation: PUL predictions in 67 Bacteroidetes genomes from the human gut microbiota and two additional species, from the canine oral sphere and from the environment, are presented in our database accessible at
    Bioinformatics 10/2014; 31(5). DOI:10.1093/bioinformatics/btu716 · 4.98 Impact Factor
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    ABSTRACT: Crucial virulence determinants of disease causing Neisseria meningitidis species are their extracellular polysaccharide capsules. In the serogroups W and Y, these are heteropolymers of the repeating units (→6)-α-d-Gal-(1→4)-α-Neu5Ac-(2→)n in NmW and (→6)-α-d-Glc-(1→4)-α-Neu5Ac-(2→)n in NmY. The capsule polymerases, SiaDW and SiaDY, which synthesize these highly unusual polymers, are composed of two predicted GT-B fold domains separated by a large stretch of amino acids (aa 399–762). We recently showed that residues critical to the hexosyl- and sialyltransferase activity are found in the predicted N-terminal (aa 1–398) and C-terminal (aa 763–1037) GT-B fold domains, respectively. Here we use a mutational approach and synthetic fluorescent substrates to define the boundaries of the hexosyl- and sialyltransferase domains. Our results reveal that the active sialyltransferase domain extends well beyond the predicted C-terminal GT-B domain and defines a new glycosyltransferase family, GT97, in CAZy (Carbohydrate-Active enZYmes Database).
    Journal of Biological Chemistry 10/2014; 289(49). DOI:10.1074/jbc.M114.597773 · 4.57 Impact Factor
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    ABSTRACT: Background Enzymatic breakdown of lignocellulosic biomass is a known bottleneck for the production of high-value molecules and biofuels from renewable sources. Filamentous fungi are the predominant natural source of enzymes acting on lignocellulose. We describe the extraordinary cellulose-deconstructing capacity of the basidiomycete Laetisaria arvalis, a soil-inhabiting fungus. Results The L. arvalis strain displayed the capacity to grow on wheat straw as the sole carbon source and to fully digest cellulose filter paper. The cellulolytic activity exhibited in the secretomes of L. arvalis was up to 7.5 times higher than that of a reference Trichoderma reesei industrial strain, resulting in a significant improvement of the glucose release from steam-exploded wheat straw. Global transcriptome and secretome analyses revealed that L. arvalis produces a unique repertoire of carbohydrate-active enzymes in the fungal taxa, including a complete set of enzymes acting on cellulose. Temporal analyses of secretomes indicated that the unusual degradation efficiency of L. arvalis relies on its early response to the carbon source, and on the finely tuned sequential secretion of several lytic polysaccharide monooxygenases and hydrolytic enzymes targeting cellulose. Conclusions The present study illustrates the adaptation of a litter-rot fungus to the rapid breakdown of recalcitrant plant biomass. The cellulolytic capabilities of this basidiomycete fungus result from the rapid, selective and successive secretion of oxidative and hydrolytic enzymes. These enzymes expressed at critical times during biomass degradation may inspire the design of improved enzyme cocktails for the conversion of plant cell wall resources into fermentable sugars. Electronic supplementary material The online version of this article (doi:10.1186/s13068-014-0143-5) contains supplementary material, which is available to authorized users.
    Biotechnology for Biofuels 10/2014; 7(1):143. DOI:10.1186/s13068-014-0143-5 · 6.04 Impact Factor
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    ABSTRACT: To study how microbes establish themselves in a mammalian gut environment, we colonized germ-free mice with microbial communities from human, zebrafish, and termite guts, human skin and tongue, soil, and estuarine microbial mats. Bacteria from these foreign environments colonized and persisted in the mouse gut; their capacity to metabolize dietary and host carbohydrates and bile acids correlated with colonization success. Cohousing mice harboring these xenomicrobiota or a mouse cecal microbiota, along with germ-free "bystanders," revealed the success of particular bacterial taxa in invading guts with established communities and empty gut habitats. Unanticipated patterns of ecological succession were observed; for example, a soil-derived bacterium dominated even in the presence of bacteria from other gut communities (zebrafish and termite), and human-derived bacteria colonized germ-free bystander mice before mouse-derived organisms. This approach can be generalized to address a variety of mechanistic questions about succession, including succession in the context of microbiota-directed therapeutics.
    Cell 10/2014; DOI:10.1016/j.cell.2014.09.008 · 32.24 Impact Factor
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    ABSTRACT: Glycosylation of proteins and lipids involves over 200 known glycosyltransferases (GTs), and deleterious defects in many of the genes encoding these enzymes cause disorders collectively classified as congenital disorders of glycosylation (CDGs). Most known CDGs are caused by defects in glycogenes that affect glycosylation globally. Many GTs are members of homologous isoenzyme families and deficiencies in individual isoenzymes may not affect glycosylation globally. In line with this, there appears to be an underrepresentation of disease-causing glycogenes among these larger isoenzyme homologous families. However, genome-wide association studies have identified such isoenzyme genes as candidates for different diseases, but validation is not straightforward without biomarkers. Large-scale whole-exome sequencing (WES) provides access to mutations in, for example, GT genes in populations, which can be used to predict and/or analyze functional deleterious mutations. Here, we constructed a draft of a functional mutational map of glycogenes, GlyMAP, from WES of a rather homogenous population of 2000 Danes. We cataloged all missense mutations and used prediction algorithms, manual inspection and in case of carbohydrate-active enzymes family GT27 experimental analysis of mutations to map deleterious mutations. GlyMAP ( provides a first global view of the genetic stability of the glycogenome and should serve as a tool for discovery of novel CDGs. © 2014 The Author 2014. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected] /* */
    Glycobiology 09/2014; 25(2). DOI:10.1093/glycob/cwu104 · 3.15 Impact Factor
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    Moran Kopel · William Helbert · Bernard Henrissat · Tirza Doniger · Ehud Banin ·
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    ABSTRACT: Here, we report the draft genome sequence of two ulvan-degrading Alteromonas spp. isolated from the feces of the sea slug, Aplysia. These sequenced genomes display a unique ulvan degradation machinery compared with ulvanolytic enzymes previously identified in Nonlabens ulvanivorans.
    Genome Announcements 09/2014; 2(5). DOI:10.1128/genomeA.01081-14
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    ABSTRACT: Ectomycorrhizal fungi, living in soil forests, are required microorganisms to sustain tree growth and productivity. The establishment of mutualistic interaction with roots to form ectomycorrhiza (ECM) is not well known at the molecular level. In particular, how fungal and plant cell walls are rearranged to establish a fully functional ectomycorrhiza is poorly understood. Nevertheless, it is likely that Carbohydrate Active enZymes (CAZyme) produced by the fungus participate in this process. Genome-wide transcriptome profiling during ECM development was used to examine how the CAZome of Laccaria bicolor is regulated during symbiosis establishment. CAZymes active on fungal cell wall were upregulated during ECM development in particular after 4weeks of contact when the hyphae are surrounding the root cells and start to colonize the apoplast. We demonstrated that one expansin-like protein, whose expression is specific to symbiotic tissues, localizes within fungal cell wall. Whereas L. bicolor genome contained a constricted repertoire of CAZymes active on cellulose and hemicellulose, these CAZymes were expressed during the first steps of root cells colonization. L. bicolor retained the ability to use homogalacturonan, a pectin-derived substrate, as carbon source. CAZymes likely involved in pectin hydrolysis were mainly expressed at the stage of a fully mature ECM. All together, our data suggest an active remodelling of fungal cell wall with a possible involvement of expansin during ECM development. By contrast, a soft remodelling of the plant cell wall likely occurs through the loosening of the cellulose microfibrils by AA9 or GH12 CAZymes and middle lamella smooth remodelling through pectin (homogalacturonan) hydrolysis likely by GH28, GH12 CAZymes.
    Fungal Genetics and Biology 08/2014; 72. DOI:10.1016/j.fgb.2014.08.007 · 2.59 Impact Factor
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    ABSTRACT: Clostridium termitidis strain CT1112 is an anaerobic, gram positive, mesophilic, cellulolytic bacillus isolated from the gut of the wood-feeding termite, Nasutitermes lujae. It produces biofuels such as hydrogen and ethanol from cellulose, cellobiose, xylan, xylose, glucose, and other sugars, and therefore could be used for biofuel production from biomass through consolidated bioprocessing. The first step in the production of biofuel from biomass by microorganisms is the hydrolysis of complex carbohydrates present in biomass. This is achieved through the presence of a repertoire of secreted or complexed carbohydrate active enzymes (CAZymes), sometimes organized in an extracellular organelle called cellulosome. To assess the ability and understand the mechanism of polysaccharide hydrolysis in C. termitidis, the recently sequenced strain CT1112 of C. termitidis was analyzed for both CAZymes and cellulosomal components, and compared to other cellulolytic bacteria. A total of 355 CAZyme sequences were identified in C. termitidis, significantly higher than other Clostridial species. Of these, high numbers of glycoside hydrolases (199) and carbohydrate binding modules (95) were identified. The presence of a variety of CAZymes involved with polysaccharide utilization/degradation ability suggests hydrolysis potential for a wide range of polysaccharides. In addition, dockerin-bearing enzymes, cohesion domains and a cellulosomal gene cluster were identified, indicating the presence of potential cellulosome assembly.
    PLoS ONE 08/2014; 9(8):e104260. DOI:10.1371/journal.pone.0104260 · 3.23 Impact Factor

Publication Stats

38k Citations
2,937.64 Total Impact Points


  • 2015
    • Ghent University
      Gand, Flanders, Belgium
  • 2014-2015
    • King Abdulaziz University
      • • Department of Biological Science
      • • Faculty of Sciences
      Djidda, Makkah, Saudi Arabia
    • Universidade Católica de Brasília
      • Pós-Graduação em Ciências Genômicas e Biotecnologia
      Brasília, Federal, Brazil
  • 2002-2015
    • Aix-Marseille Université
      • Unité de Recherche d'Architecture et Fonction des Macromolécules Biologiques (UMR 7257 AFMB)
      Marsiglia, Provence-Alpes-Côte d'Azur, France
    • CUNY Graduate Center
      New York, New York, United States
    • European Synchrotron Radiation Facility
      Grenoble, Rhône-Alpes, France
  • 1998-2014
    • Architecture et Fonction des Macromolécules Biologiques
      Marsiglia, Provence-Alpes-Côte d'Azur, France
  • 1989-2014
    • French National Centre for Scientific Research
      • • Laboratoire Information Génomique et Structurale (IGS)
      • • Laboratoire de Architecture et Fonction des Macromolécules Biologiques
      • • Centre de Recherches sur les Macromolécules Végétales
      Lutetia Parisorum, Île-de-France, France
  • 2013
    • Cornell University
      • Department of Plant Pathology and Plant-Microbe Biology
      Итак, New York, United States
  • 1988-2012
    • French National Institute for Agricultural Research
      Lutetia Parisorum, Île-de-France, France
  • 2010
    • The University of Tennessee Medical Center at Knoxville
      Knoxville, Tennessee, United States
  • 2008
    • Howard University
      • Department of Biology
      Washington, West Virginia, United States
  • 2007
    • Lawrence Livermore National Laboratory
      Livermore, California, United States
    • Washington University in St. Louis
      San Luis, Missouri, United States
  • 2004
    • Kyoto University
      • Department of Pathology and Tumor Biology
      Kyoto, Kyoto-fu, Japan
  • 2001
    • Cea Leti
      Grenoble, Rhône-Alpes, France
    • Virginia Polytechnic Institute and State University
      Blacksburg, Virginia, United States
  • 1997-2001
    • The University of York
      • • York Structural Biology Laboratory
      • • Department of Chemistry
      York, England, United Kingdom
  • 1995-1997
    • University Joseph Fourier - Grenoble 1
      • Centre de Recherche sur les MAcromolécules Végétales
      Grenoble, Rhône-Alpes, France
  • 1996
    • Max-Delbrück-Centrum für Molekulare Medizin
      Berlín, Berlin, Germany
  • 1994
    • Niigata University
      • Faculty of Agriculture
      Niahi-niigata, Niigata, Japan
  • 1993
    • Technical University of Denmark
      København, Capital Region, Denmark
  • 1991
    • University of British Columbia - Vancouver
      • Department of Microbiology and Immunology
      Vancouver, British Columbia, Canada
  • 1990
    • John Innes Centre
      • The Sainsbury Laboratory
      Norwich, England, United Kingdom
  • 1987
    • Institute of Food Research
      Norwich, England, United Kingdom
  • 1985
    • University of Grenoble
      Grenoble, Rhône-Alpes, France