Ten years of CAZypedia: a living encyclopedia of carbohydrate-active enzymes

Ten years of CAZypedia: a living encyclopedia of carbohydrate-active enzymes Abstract CAZypedia was initiated in 2007 to create a comprehensive, living encyclopedia of the carbohydrate-active enzymes (CAZymes) and associated carbohydrate-binding modules involved in the synthesis, modification and degradation of complex carbohydrates. CAZypedia is closely connected with the actively curated CAZy database, which provides a sequence-based foundation for the biochemical, mechanistic and structural characterization of these diverse proteins. Now celebrating its 10th anniversary online, CAZypedia is a successful example of dynamic, community-driven and expert-based biocuration. CAZypedia is an open-access resource available at URL http://www.cazypedia.org. biocuration, bioinformatics, carbohydrate-active enzymes, glycoscience, glycobiology Background The Carbohydrate-Active Enzymes (CAZymes) classification groups catalytic and substrate-binding modules of proteins responsible for the assembly and breakdown of complex carbohydrates into sequence-based families. Since the original definition of 35 glycoside hydrolase (GH) families in 1991 (Henrissat 1991), the CAZy database (available at URL http://www.cazy.org/) continues to grow and currently (October 2017) encompasses 105 glycosyltransferase (GT) families, 145 GH families, 27 polysaccharide lyase (PL) families, 16 carbohydrate esterase (CE) families, 13 auxiliary activity (AA) families and 81 carbohydrate-binding module (CBM) families (Levasseur et al. 2013; Lombard et al. 2014). As a result of vigorous biocuration [as defined by Bourne and McEntyre (2006)] and tireless technical development in response to an ever-increasing rate of gene sequencing, the CAZy database has become the de facto framework that unites protein sequence, biochemical and structural data among the tremendous diversity of CAZymes in nature [see (Davies and Sinnott 2008) for an accessible primer and review]. The CAZy database is arranged in a conventional format, with individual family pages consisting of tables of protein names, GenBank and/or UniProt sequence accession codes, EC numbers (when activity has been experimentally defined) and Protein Data Bank accession codes (when a structure has been solved). Each family page contains a compact header that summarizes key information on substrate specificity, catalytic mechanism, three-dimensional protein fold and carbohydrate ligand complexes. Additionally, individual genome pages provide a convenient census of all CAZyme families in individual organisms (Lombard et al. 2014). In keeping with its primary function to list individual family members, family pages in the CAZy database are efficiently minimalistic. CAZypedia arose from the idea that a more detailed and directly accessible summary of the key research on individual CAZy families would be of significant value to glycoscience researchers, particularly highlighting the primacy of key research discoveries in a family, and supporting the activities of all scientists interested in CAZymes. Genesis CAZypedia’s roots can be traced to renowned polysaccharide biochemist Professor Bruce Stone (1928–2008†; Whelan 2009) who proposed the idea of a comprehensive encyclopedia of the CAZymes. Bruce initially raised this idea informally at the 23rd International Carbohydrate Symposium (ICS; Whistler, Canada; July 2006) among a select group of glycoscientists, including Harry Brumer, Anthony Clarke, Gideon Davies, Harry Gilbert, Bernard Henrissat, Antoni Planas, Birte Svensson, David Vocadlo, Spencer Williams, Stephen Withers and others. Bruce’s original vision was to produce a traditional printed book or series, comprising chapters written by specific experts on individual families. It was recognized early on that the sheer number of families at that time (>100 GH families alone), combined with rapid advancements in the field, would make the timely completion of a printed work with lasting value a Sisyphean task. Further ad hoc discussions about the best way to bring Bruce’s vision to fruition continued through subsequent months, culminating at a second, larger group discussion at the seventh Carbohydrate Bioengineering Meeting (CBM7; Braunschweig, Germany; April 2007). Among those in attendance were (again) Bruce Stone, Harry Brumer, Anthony Clarke, Harry Gilbert, Antoni Planas and Birte Svensson, as well as Vincent Bulone, Marco Moracci, Warren Wakarchuk, Tony Warren, Lisa Willis and others. Here, there was general agreement that only an online, internet-based format would have sufficient flexibility and immediacy to match the rapid advances being made in CAZymology. Inspired by the growing impact of Wikipedia as a community-based publishing model of encyclopedic information, the idea to use a wiki (see definition at URL https://en.wikipedia.org/wiki/Wiki) approach to develop an online “Encyclopedia of Carbohydrate-Active Enzymes” was adopted. Hence, CAZypedia was born in May 2007 when Harry Brumer, then of the Kungliga Tekniska Högskolan in Stockholm, established CAZypedia using the MediaWiki software (freely available at URL https://www.mediawiki.org/). Content Content creation for CAZypedia was focussed initially on the GH families, due to a particularly long and rich history of biochemical and structural characterization of these enzymes (Sinnott 1990; Davies and Henrissat 1995). An original set of pages covering families GH1, GH2, GH10 and GH11 by Stephen Withers, together with GH27 and GH36 by Harry Brumer, were produced and refined with editorial input from Bernard Henrissat through the summer of 2007. In this process, a streamlined page format was devised (Figure 1), comprising individual sections on “Substrate specificities”, “Kinetics and mechanism”, “Catalytic residues” and “Three-dimensional structures”, which present a concise summary of common features of each family. A “Family Firsts” section provides a brief, itemized list of references to seminal publications that define the key mechanistic and structural features of the family: the first reaction stereochemistry determination, catalytic residue identification and three-dimensional structure solution. An overarching goal in page design was to provide a rapid entry into the key primary literature on each family (which is not directly available in the CAZy database), through an abbreviated and consistent format. CAZypedia pages may be beneficially embellished with figures, although this is optional. Fig. 1. View largeDownload slide Layout of a typical CAZyme family page in CAZypedia. This figure is available in black and white in print and in colour at Glycobiology online. Fig. 1. View largeDownload slide Layout of a typical CAZyme family page in CAZypedia. This figure is available in black and white in print and in colour at Glycobiology online. As part of an explicit design intent, CAZypedia pages do not necessarily strive to provide comprehensive reviews of all the available literature on individual families, although it should be noted that there is formally no prescribed page length. The reasons for this are largely practical. Initially, pages can be composed rapidly by focussing on the key defining literature. Compilation of a comprehensive corpus of the published work on a family, which is in many cases extensive when all individual biochemical characterization studies are considered, is therefore not required. This focus also helps to future-proof pages in a rapidly evolving field: first achievements will always remain historically significant, regardless of the number of subsequent publications on a family. For the same reason, pages explicitly avoid enumeration of time-sensitive data, such as the number of sequences or structures for individual families, which can otherwise be gleaned from the continually updated CAZy database (individual CAZypedia and CAZy database pages are cross-linked for this purpose). Thus, CAZypedia pages are designed to be perpetually accurate, regardless of the frequency of future updates from page authors. The appellation “Curator Approved” is given to each newly minted family page once all sections contain a basic coverage of the seminal literature (see also “Technical aspects” section below). From the initial seed of six GH families, CAZypedia has grown to include over 100 individual Curator Approved GH family pages, produced by a similar number of expert contributors from the CAZyme/glycoscience community. Indeed, July 2014 marked a watershed in CAZypedia’s history, with the completion of the GH12 page by Gerlind Sulzenbacher as the 100th Curator Approved GH page. Pages on other groups of CAZymes (i.e., Glycosyltransferases (Coutinho et al. 2003), Polysaccharide Lyases (Lombard et al. 2010) and Auxiliary Activity redox enzymes (Levasseur et al. 2013)) and non-catalytic CBMs (Boraston et al. 2004) continue to be incorporated through growing community engagement. Notable CAZypedia firsts include the completion of the GT42 page by Warren Wakarchuk in April 2010, the PL2 page by Wade Abbott in September 2013, the AA9 lytic polysaccharide mono-oxygenase page by Paul Harris in September 2013, and the CBM32 page by Elizabeth Ficko-Blean and Alisdair Boraston in May 2013. CAZypedia’s History page (available at URL https://www.cazypedia.org/index.php/CAZypedia:History, accessed via the About CAZypedia menu.) serves as a repository for these and future major milestones, while the News page (available at URL https://www.cazypedia.org/index.php/News and via CAZypedia’s Main Page.) covers recent Curator Approved pages and other newsworthy items. In recognition of the complex nature of carbohydrate chemistry and CAZymes, CAZypedia also incorporates a Lexicon that provides a definition of key terms, explanation of specialist nomenclature and tutorial reviews of concepts that are relevant to individual family pages. The Lexicon provides a touchstone for new readers to support their understanding and interpretation of individual families, and is hyperlinked within the text of family pages. The Lexicon and category pages for each major CAZyme class are conveniently accessed under the Content menu, prominently displayed on the left side of all CAZypedia pages (Figure 1). At its 10th anniversary online, CAZypedia currently comprises 106 GH, 10 CBM, 6 PL, 2 AA, 2 GT and 22 Lexicon pages with Curator Approved status. The MediaWiki software upon which CAZypedia relies tracks usage statistics, which are available through the Special Pages menu item. These statistics reveal over 12 million total page views, and over one hundred thousand views for several of the most popular GH and Lexicon pages. More conservative estimates of activity provided by Google Analytics indicate that CAZypedia access has increased to thousands of international users per week since data recording on that utility began in the autumn of 2009 (Figure 2). Regardless of the absolute values, these data highlight the sustained and growing value of CAZypedia to specialists and non-specialists alike. Fig. 2. View largeDownload slide CAZypedia usage statistics from Google Analytics. Access tracking with this service was initiated in August 2009. Sharp dips correspond to December holidays and broad troughs correspond to summer in the northern hemisphere. Fig. 2. View largeDownload slide CAZypedia usage statistics from Google Analytics. Access tracking with this service was initiated in August 2009. Sharp dips correspond to December holidays and broad troughs correspond to summer in the northern hemisphere. Editorial framework During the birth of CAZypedia, there was significant concern about the potential pitfalls of applying directly the Wikipedia model, which allows author anonymity and lacks formal editorial oversight, to the publication of a rigorous scientific encyclopedia. Thus, although CAZypedia adopts many of the general principles and rules of Wikipedia, CAZypedia draws on best-practice authoring and editing principles of peer-reviewed, wiki-based encyclopedia such as Citizendium (available at URL http://en.citizendium.org/) and Scholarpedia (available at URL http://www.scholarpedia.org). CAZypedia strives to be a dynamic, community-based resource, which at the same time balances the need for careful content curation. A full description of CAZypedia’s editorial policies is available on the About page (see URL https://www.cazypedia.org/index.php/CAZypedia:About, accessed via Introduction to CAZypedia under the About CAZypedia menu); however, a few points deserve special comment. The editorial organization of CAZypedia is designed with a minimum of bureaucratic and administrative overhead, because it is entirely volunteer-based and has no direct funding support. CAZypedia generally adopts Wikipedia’s Simplified Ruleset (available at URL http://en.wikipedia.org/wiki/Wikipedia:Simplified_Ruleset), particularly the concepts of using a neutral point-of-view, writing verifiable text, including only peer-reviewed information (no original research), being civil and well-behaved, and not infringing copyright. As a culmination of these principles, CAZypedia reports on—but does not engage in critique of—the published literature, and supports all statements of fact with primary citations. Not least, Wikipedia’s extensive “What Wikipedia is not” page (available at URL http://en.wikipedia.org/wiki/Wikipedia:What_Wikipedia_is_not) can be translated to “What CAZypedia is not” essentially point-by-point. Following the Citizendium model, transparency is achieved through the use of contributors’ real names in CAZypedia. Additionally, individual biographical pages enable readers to evaluate directly each contributor’s expertise in the field. To maintain editorial quality control, every Family and Lexicon page in CAZypedia is overseen by a Responsible Curator, who is primarily responsible for overall content. Responsible Curators are selected by a panel of Senior Curators based on established expertise and a willingness to participate in the active maintenance of specific pages. In turn, Responsible Curators are tasked with recruiting and managing Authors to participate in content creation; Responsible Curators may also contribute directly to composing page content. In the spirit of a community-driven resource, individuals are encouraged to self-nominate to become Responsible Curators or Authors. In general, individuals at any career stage are welcomed to participate as Authors, including keen undergraduates, postgraduate students and post-doctoral scientists. Indeed, the current list of contributors (see below) includes many junior scientists (or scientists who were at least junior at the time of their first contribution). Ultimately, the quality of entries in CAZypedia, like Wikipedia, relies upon the keen eye of readers at-large to identify errors and omissions. All users who spot such oversights are encouraged to contact the Responsible Curator for that page, so that a correction can be made. CAZypedia is an open-access publication, i.e., it is freely available online for anyone to read, study and otherwise use for scholarly pursuits. However, the Authors and Curators of CAZypedia assert their copyright for the sole purpose of preventing outright duplication and uncontrolled modification of the content, which could undermine the expert-based nature of this resource. Although we strongly advocate that readers should cite the primary research literature directly, individual CAZypedia pages may also be cited when practical, analogous to a book chapter or review article. Citation details are provided in the footer and via the Tools menu on each page (Figure 1). Technical aspects Wiki-wiki As introduced above, CAZypedia runs on MediaWiki, the free, open source PHP software originally developed for Wikipedia. This choice was based on the demonstrated robustness and scalability of MediaWiki, as well as the availability of diverse software extensions to add functionality. As Wikipedia is unlikely to disappear anytime soon, so too is MediaWiki’s active community of developers likely to persist well into the future, thereby ensuring continued maintenance of the software running CAZypedia. A full technical and functional description of MediaWiki is beyond the scope of this Letter; interested readers should visit MediaWiki.org for more details. For the content contributor and user, the most important practical aspect of the use of MediaWiki is that CAZypedia is a wiki: edits are displayed instantaneously when saved and do not require approval before appearing online. This enables dynamic development of page content driven by individual Authors. In the initial stages of development, pages are clearly marked as “Under Construction”, with a warning that content is under revision and may be subject to major changes. Once vetted by the Responsible Curator, a page may be upgraded to “Curator Approved” status to indicate that it is factually accurate and essentially complete. However, “completeness” is not absolute: as a wiki, CAZypedia is a living document, so further development of page content is forever possible. Creating content for CAZypedia is relatively intuitive. Once a new Author has been provided with a login, page editing can be conducted within a modern web browser using a simplified markup language. A boilerplate pre-populates the page with the major template features, and Authors can view the code of other pages to get ideas of ways to insert features like hyperlinks, references and figures. A “Getting Started Guide”, along with concise pages that provide help with editing, references and adding images provide guidance to assist the novice. Here, too, the use of MediaWiki as software platform is a considerable benefit, due to vast extant help resources on editing. Finally, assistance is always at hand from CAZypedia Curators, who are able to activity monitor edits via the global “Recent Changes” and individual “History” pages. BiblioPlus MediaWiki functionality can be enhanced through extensions, and CAZypedia utilizes several, including those for user administration, defining page boilerplate content and integrating Google Analytics. Among these, BiblioPlus (freely available at URL https://www.mediawiki.org/wiki/Extension:BiblioPlus) deserves special mention as the MediaWiki extension that drives bibliographic referencing. BiblioPlus is the result of a significant effort by CAZypedia contributor Karen Eddy to correct compatibility issues arising in the original Biblio extension by Martin Jambon and others (see URL https://www.mediawiki.org/wiki/Extension:Biblio). Like its predecessor, BiblioPlus performs automated retrieval and formatting of citations from PubMed and the ISBN databases in MediaWiki pages. Similar to other reference formatting software, BiblioPlus automatically numbers in-text citations and generates a reference section, which is included at the bottom of a page. Notably, the reference section contains hyperlinks to original sources, specifically PubMed or the ISBNdb, HubMed and DOI hyperlinks. BiblioPlus was specifically re-coded to utilize the modern NCBI Entrez Programming Utilities (E-utilities) interface (Anonymous 2010). A full description of features and usage instructions is available on the BiblioPlus Mediawiki extension page (URL https://www.mediawiki.org/wiki/Extension:BiblioPlus). It should be noted that BiblioPlus is freely available and will work together with any modern MediaWiki implementation, so that it may be broadly deployed in any wiki, scientific or otherwise. The next 10 years: CAZypedia needs you! The continued success of CAZypedia will remain entirely dependent on the diligence and commitment of experts and keen junior scientists to voluntarily contribute to the maintenance and growth of this reference work. The job of building CAZypedia is by no means complete, and as a living encyclopedia, it never will be—especially as research continues to reveal new CAZyme families, tertiary structures and mechanistic details (e.g., Campos et al. 2016; Venditto et al. 2016; Abe et al. 2017; Munoz-Munoz, Cartmell, Terrapon, Basle 2017; Munoz-Munoz, Cartmell, Terrapon, Henrissat 2017; Ndeh et al. 2017). Currently, many pages remain to be written and existing pages would benefit from regular updates as new data come to hand, which requires expert volunteers willing to assume the responsibility for page creation and maintenance. Thus, the CAZypedia Consortium openly invites all interested glycoscientists, regardless of career stage (including keen undergraduate and postgraduate students, post-doctoral researchers, industrial scientists and professors) to peruse the “Unassigned Pages” lists for each CAZyme class and see if they might be able to help. The growth of CAZypedia will depend exclusively on the generous and selfless contributions of the existing and new generations of CAZypedians. We invite you to join us! Contact information is available at URL http://www.cazypedia.org/. Acknowledgments We thank Stephen MacDonald and Vince Tingey (Michael Smith Laboratories, University of British Columbia), and Eric Björkvall (School of Biotechnology, Kungliga Tekniska Högskolan), for invaluable IT support. Dr. Karen Eddy (Brumer group, MSL, UBC) is thanked for developing the BiblioPlus extension. CAZypedia is the result of many hours of effort by the following group of current contributors (A continually updated list is available at URL http://www.cazypedia.org/index.php/Category:Contributors, accessed via the “About CAZypedia” menu.): Wade Abbott, Agriculture and Agri-Food Canada, Canada; Orly Alber, Weizmann Institute of Science, Israel; Ed Bayer, Weizmann Institute of Science, Israel; Jean-Guy Berrin, Institut National de la Recherche Agronomique, France; Alisdair Boraston, University of Victoria, Canada; Harry Brumer, University of British Columbia, Canada; Ryszard Brzezinski, Université de Sherbrooke, Canada; Anthony Clarke, University of Guelph, Canada; Beatrice Cobucci-Ponzano, National Research Council of Italy, Italy; Darrell Cockburn, Penn State University, United States of America; Pedro Coutinho, Aix Marseille Université, France; Mirjam Czjzek, Centre National de la Recherche Scientifique, France; Bareket Dassa, Weizmann Institute of Science, Israel; Gideon John Davies, University of York, United Kingdom; Vincent Eijsink, Norwegian University of Life Sciences, Norway; Jens Eklöf, University of British Columbia, Canada; Alfons Felice, Universität für Bodenkultur, Austria; Elizabeth Ficko-Blean, Centre National de la Recherche Scientifique, France; Geoff Fincher, University of Adelaide, Australia; Thierry Fontaine, Institut Pasteur, France; Zui Fujimoto, National Agriculture and Food Research Organisation, Japan; Kiyotaka Fujita, Kagoshima University, Japan; Shinya Fushinobu, University of Tokyo, Japan; Harry Gilbert, Newcastle University, United Kingdom; Tracey Gloster, University of St. Andrews, United Kingdom; Ethan Goddard-Borger, Walter and Eliza Hall Institute of Medical Research, Australia; Ian Greig, Simon Fraser University, Canada; Jan-Hendrik Hehemann, Max Planck Institute for Marine Microbiology, Germany; Glyn Hemsworth, University of Leeds, United Kingdom; Bernard Henrissat, Centre National de la Recherche Scientifique, France; Masafumi Hidaka, University of Tokyo, Japan; Ramon Hurtado-Guerrero, University of Zaragoza, Spain; Kiyohiko Igarashi, University of Tokyo, Japan; Takuya Ishida, University of Tokyo, Japan; Stefan Janecek, Slovak Academy of Sciences, Slovakia; Seino Jongkees, University of Tokyo, Japan; Nathalie Juge, Quadram Institute, United Kingdom; Satoshi Kaneko, University of the Ryukyus, Japan; Takane Katayama, Ishikawa Prefectural University, Japan; Motomitsu Kitaoka, National Agriculture and Food Research Organisation, Japan; Naotake Konno, Utsunomiya University, Japan; Daniel Kracher, Universität für Bodenkultur, Austria; Anna Kulminskaya, Petersburg Nuclear Physics Institute, Russia; Alicia Lammerts van Bueren, University of Groningen, Netherlands; Sine Larsen, University of Copenhagen, Denmark; Junho Lee, University of British Columbia, Canada; Markus Linder, Aalto University, Finland; Leila LoLeggio, University of Copenhagen, Denmark; Roland Ludwig, Universität für Bodenkultur, Austria; Ana Luis, Universtiy of Lisbon, Portugal; Mirko Maksimainen, University of Oulu, Finland; Brian Mark, University of Manitoba, Canada; Richard McLean, University of Lethbridge, Canada; Gurvan Michel, Centre National de la Recherche Scientifique, France; Cedric Montanier, Institut National de la Recherche Agronomique, France; Marco Moracci, National Research Council of Italy, Italy; Haruhide Mori, Hokkaido University, Japan; Hiroyuki Nakai, Niigata University, Japan; Wim Nerinckx, Ghent University, Belgium; Takayuki Ohnuma, Kinki University, Japan; Richard Pickersgill, Queen Mary University of London, United Kingdom; Kathleen Piens, Sveriges Lantbruksuniversitet, Sweden; Tirso Pons, National Centre for Biotechnology, Spain; Etienne Rebuffet, Centre National de la Recherche Scientifique, France; Peter Reilly, Iowa State University, United States of America; Magali Remaud-Simeon, Institut National des Sciences Appliquées, France; Brian Rempel, University of British Columbia, Canada; Kyle Robinson, University of British Columbia, Canada; David Rose, University of Waterloo, Canada; Juha Rouvinen, University of Eastern Finland, Finland; Wataru Saburi, Hokkaido University, Japan; Yuichi Sakamoto, Iwate Biotechnology Research Center, Japan; Mats Sandgren, Sveriges Lantbruksuniversitet, Sweden; Fathima Shaikh, University of British Columbia, Canada; Yuval Shoham, Technion, Israel; Franz St. John, United States Department of Agriculture, United States of America; Jerry Stahlberg, Sveriges Lantbruksuniversitet, Sweden; Michael Suits, Wilfrid Laurier University, Canada; Gerlind Sulzenbacher, Centre National de la Recherche Scientifique, France; Tomomi Sumida, RIKEN, Japan; Ryuichiro Suzuki, Akita Prefectural University, Japan; Birte Svensson, Danmarks Tekniske Universitet, Denmark; Toki Taira, University of the Ryukyus, Japan; Ed Taylor, University of Lincoln, United Kingdom; Takashi Tonozuka, Tokyo University of Agriculture and Technology, Japan; Breeanna Urbanowicz, University of Georgia, United States of America; Gustav Vaaje-Kolstad, Norwegian University of Life Sciences, Norway; Wim Van den Ende, Katholieke Universiteit Leuven, Belgium; Annabelle Varrot, Centre National de la Recherche Scientifique, France; Maxime Versluys, Katholieke Universiteit Leuven, Belgium; Florence Vincent, Centre National de la Recherche Scientifique, France; David Vocadlo, Simon Fraser University, Canada; Warren Wakarchuk, Ryerson University, Canada; Tom Wennekes, Universiteit Utrecht, Netherlands; Rohan Williams, University of Melbourne, Australia; Spencer Williams, University of Melbourne, Australia; David Wilson†, Cornell University, United States of America; Stephen Withers, University of British Columbia, Canada; Katsuro Yaoi, National Institute of Advanced Industrial Science and Technology, Japan; Vivian Yip, University of British Columbia, Canada; Ran Zhang, University of British Columbia, Canada. This Letter was composed by H. Brumer (brumer@msl.ubc.ca) and S.J. Williams (sjwill@unimelb.edu.au), with input from B. Svensson, B. Henrissat, G.J. Davies, H.J. Gilbert, A.J. Clarke, W.W. Wakarchuk, D.W. Abbott, D.J. Vocadlo, E. Ficko-Blean, A.B. Boraston, A. Planas, and S. Fushinobu. Page charges for this article were supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to H. Brumer. References Abe K, Nakajima M, Yamashita T, Matsunaga H, Kamisuki S, Nihira T, Takahashi Y, Sugimoto N, Miyanaga A, Nakai H et al.  . 2017. Biochemical and structural analyses of a bacterial endo-beta-1,2-glucanase reveal a new glycoside hydrolase family. J Biol Chem . 292: 7487– 7506. Google Scholar CrossRef Search ADS PubMed  Anonymous. 2010. Entrez Programming Utilities Help National Center for Biotechnology Information:Bethesda, MD, USA. Available from: https://www.ncbi.nlm.nih.gov/books/NBK25501/. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 2004. Carbohydrate-binding modules: Fine-tuning polysaccharide recognition. Biochem J . 382: 769– 781. Google Scholar CrossRef Search ADS PubMed  Bourne PE, McEntyre J. 2006. Biocurators: Contributors to the world of science. PLoS Comput Biol . 2: 1185– 1185. Campos BM, Liberato MV, Alvarez TM, Zanphorlin LM, Ematsu GC, Barud H, Polikarpov I, Ruller R, Gilbert HJ, Zeri ACD et al.  . 2016. A novel carbohydrate-binding module from sugar cane soil metagenome featuring unique structural and carbohydrate affinity properties. J Biol Chem . 291: 23734– 23743. Google Scholar CrossRef Search ADS PubMed  Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J Mol Biol . 328: 307– 317. Google Scholar CrossRef Search ADS PubMed  Davies G, Henrissat B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure . 3: 853– 859. Google Scholar CrossRef Search ADS PubMed  Davies GJ, Sinnott ML. 2008. Sorting the diverse. Biochemist . 30: 26– 32. Henrissat B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J . 280: 309– 316. Google Scholar CrossRef Search ADS PubMed  Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. 2013. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels . 6: 14. Google Scholar CrossRef Search ADS PubMed  Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 2010. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J . 432: 437– 444. Google Scholar CrossRef Search ADS PubMed  Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res . 42: D490– D495. Google Scholar CrossRef Search ADS PubMed  Munoz-Munoz J, Cartmell A, Terrapon N, Basle A, Henrissat B, Gilbert HJ. 2017. An evolutionarily distinct family of polysaccharide lyases removes rhamnose capping of complex arabinogalactan proteins. J Biol Chem . 292: 13271– 13283. Google Scholar CrossRef Search ADS PubMed  Munoz-Munoz J, Cartmell A, Terrapon N, Henrissat B, Gilbert HJ. 2017. Unusual active site location and catalytic apparatus in a glycoside hydrolase family. Proc Natl Acad Sci U S A . 114: 4936– 4941. Google Scholar CrossRef Search ADS PubMed  Ndeh D, Rogowski A, Cartmell A, Luis AS, Basle A, Gray J, Venditto I, Briggs J, Zhang XY, Labourel A et al.  . 2017. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature . 544: 65– 70. Google Scholar CrossRef Search ADS PubMed  Sinnott ML. 1990. Catalytic mechanisms of enzymatic glycosyl transfer. Chem Rev . 90: 1171– 1202. Google Scholar CrossRef Search ADS   Venditto I, Luis AS, Rydahl M, Schuckel J, Fernandes VO, Vidal-Melgosa S, Bule P, Goyal A, Pires VMR, Dourado CG et al.  . 2016. Complexity of the Ruminococcus flavefaciens cellulosome reflects an expansion in glycan recognition. Proc Natl Acad Sci U S A . 113: 7136– 7141. Google Scholar CrossRef Search ADS PubMed  Whelan W. 2009. Obituary: Bruce A. Stone. IUBMB Life . 61: 84– 84. Google Scholar CrossRef Search ADS   Author notes Dedication: CAZypedia is dedicated to Emeritus Professor Bruce Stone (1928–2008†), whose enthusiasm to create a comprehensive encyclopedia of carbohydrate-active enzymes was essential to the genesis of this resource. © The Author 2017. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Glycobiology Oxford University Press

Ten years of CAZypedia: a living encyclopedia of carbohydrate-active enzymes

Loading next page...
 
/lp/ou_press/ten-years-of-cazypedia-a-living-encyclopedia-of-carbohydrate-active-knSyzEnGzy
Publisher
Oxford University Press
Copyright
© The Author 2017. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
0959-6658
eISSN
1460-2423
D.O.I.
10.1093/glycob/cwx089
Publisher site
See Article on Publisher Site

Abstract

Abstract CAZypedia was initiated in 2007 to create a comprehensive, living encyclopedia of the carbohydrate-active enzymes (CAZymes) and associated carbohydrate-binding modules involved in the synthesis, modification and degradation of complex carbohydrates. CAZypedia is closely connected with the actively curated CAZy database, which provides a sequence-based foundation for the biochemical, mechanistic and structural characterization of these diverse proteins. Now celebrating its 10th anniversary online, CAZypedia is a successful example of dynamic, community-driven and expert-based biocuration. CAZypedia is an open-access resource available at URL http://www.cazypedia.org. biocuration, bioinformatics, carbohydrate-active enzymes, glycoscience, glycobiology Background The Carbohydrate-Active Enzymes (CAZymes) classification groups catalytic and substrate-binding modules of proteins responsible for the assembly and breakdown of complex carbohydrates into sequence-based families. Since the original definition of 35 glycoside hydrolase (GH) families in 1991 (Henrissat 1991), the CAZy database (available at URL http://www.cazy.org/) continues to grow and currently (October 2017) encompasses 105 glycosyltransferase (GT) families, 145 GH families, 27 polysaccharide lyase (PL) families, 16 carbohydrate esterase (CE) families, 13 auxiliary activity (AA) families and 81 carbohydrate-binding module (CBM) families (Levasseur et al. 2013; Lombard et al. 2014). As a result of vigorous biocuration [as defined by Bourne and McEntyre (2006)] and tireless technical development in response to an ever-increasing rate of gene sequencing, the CAZy database has become the de facto framework that unites protein sequence, biochemical and structural data among the tremendous diversity of CAZymes in nature [see (Davies and Sinnott 2008) for an accessible primer and review]. The CAZy database is arranged in a conventional format, with individual family pages consisting of tables of protein names, GenBank and/or UniProt sequence accession codes, EC numbers (when activity has been experimentally defined) and Protein Data Bank accession codes (when a structure has been solved). Each family page contains a compact header that summarizes key information on substrate specificity, catalytic mechanism, three-dimensional protein fold and carbohydrate ligand complexes. Additionally, individual genome pages provide a convenient census of all CAZyme families in individual organisms (Lombard et al. 2014). In keeping with its primary function to list individual family members, family pages in the CAZy database are efficiently minimalistic. CAZypedia arose from the idea that a more detailed and directly accessible summary of the key research on individual CAZy families would be of significant value to glycoscience researchers, particularly highlighting the primacy of key research discoveries in a family, and supporting the activities of all scientists interested in CAZymes. Genesis CAZypedia’s roots can be traced to renowned polysaccharide biochemist Professor Bruce Stone (1928–2008†; Whelan 2009) who proposed the idea of a comprehensive encyclopedia of the CAZymes. Bruce initially raised this idea informally at the 23rd International Carbohydrate Symposium (ICS; Whistler, Canada; July 2006) among a select group of glycoscientists, including Harry Brumer, Anthony Clarke, Gideon Davies, Harry Gilbert, Bernard Henrissat, Antoni Planas, Birte Svensson, David Vocadlo, Spencer Williams, Stephen Withers and others. Bruce’s original vision was to produce a traditional printed book or series, comprising chapters written by specific experts on individual families. It was recognized early on that the sheer number of families at that time (>100 GH families alone), combined with rapid advancements in the field, would make the timely completion of a printed work with lasting value a Sisyphean task. Further ad hoc discussions about the best way to bring Bruce’s vision to fruition continued through subsequent months, culminating at a second, larger group discussion at the seventh Carbohydrate Bioengineering Meeting (CBM7; Braunschweig, Germany; April 2007). Among those in attendance were (again) Bruce Stone, Harry Brumer, Anthony Clarke, Harry Gilbert, Antoni Planas and Birte Svensson, as well as Vincent Bulone, Marco Moracci, Warren Wakarchuk, Tony Warren, Lisa Willis and others. Here, there was general agreement that only an online, internet-based format would have sufficient flexibility and immediacy to match the rapid advances being made in CAZymology. Inspired by the growing impact of Wikipedia as a community-based publishing model of encyclopedic information, the idea to use a wiki (see definition at URL https://en.wikipedia.org/wiki/Wiki) approach to develop an online “Encyclopedia of Carbohydrate-Active Enzymes” was adopted. Hence, CAZypedia was born in May 2007 when Harry Brumer, then of the Kungliga Tekniska Högskolan in Stockholm, established CAZypedia using the MediaWiki software (freely available at URL https://www.mediawiki.org/). Content Content creation for CAZypedia was focussed initially on the GH families, due to a particularly long and rich history of biochemical and structural characterization of these enzymes (Sinnott 1990; Davies and Henrissat 1995). An original set of pages covering families GH1, GH2, GH10 and GH11 by Stephen Withers, together with GH27 and GH36 by Harry Brumer, were produced and refined with editorial input from Bernard Henrissat through the summer of 2007. In this process, a streamlined page format was devised (Figure 1), comprising individual sections on “Substrate specificities”, “Kinetics and mechanism”, “Catalytic residues” and “Three-dimensional structures”, which present a concise summary of common features of each family. A “Family Firsts” section provides a brief, itemized list of references to seminal publications that define the key mechanistic and structural features of the family: the first reaction stereochemistry determination, catalytic residue identification and three-dimensional structure solution. An overarching goal in page design was to provide a rapid entry into the key primary literature on each family (which is not directly available in the CAZy database), through an abbreviated and consistent format. CAZypedia pages may be beneficially embellished with figures, although this is optional. Fig. 1. View largeDownload slide Layout of a typical CAZyme family page in CAZypedia. This figure is available in black and white in print and in colour at Glycobiology online. Fig. 1. View largeDownload slide Layout of a typical CAZyme family page in CAZypedia. This figure is available in black and white in print and in colour at Glycobiology online. As part of an explicit design intent, CAZypedia pages do not necessarily strive to provide comprehensive reviews of all the available literature on individual families, although it should be noted that there is formally no prescribed page length. The reasons for this are largely practical. Initially, pages can be composed rapidly by focussing on the key defining literature. Compilation of a comprehensive corpus of the published work on a family, which is in many cases extensive when all individual biochemical characterization studies are considered, is therefore not required. This focus also helps to future-proof pages in a rapidly evolving field: first achievements will always remain historically significant, regardless of the number of subsequent publications on a family. For the same reason, pages explicitly avoid enumeration of time-sensitive data, such as the number of sequences or structures for individual families, which can otherwise be gleaned from the continually updated CAZy database (individual CAZypedia and CAZy database pages are cross-linked for this purpose). Thus, CAZypedia pages are designed to be perpetually accurate, regardless of the frequency of future updates from page authors. The appellation “Curator Approved” is given to each newly minted family page once all sections contain a basic coverage of the seminal literature (see also “Technical aspects” section below). From the initial seed of six GH families, CAZypedia has grown to include over 100 individual Curator Approved GH family pages, produced by a similar number of expert contributors from the CAZyme/glycoscience community. Indeed, July 2014 marked a watershed in CAZypedia’s history, with the completion of the GH12 page by Gerlind Sulzenbacher as the 100th Curator Approved GH page. Pages on other groups of CAZymes (i.e., Glycosyltransferases (Coutinho et al. 2003), Polysaccharide Lyases (Lombard et al. 2010) and Auxiliary Activity redox enzymes (Levasseur et al. 2013)) and non-catalytic CBMs (Boraston et al. 2004) continue to be incorporated through growing community engagement. Notable CAZypedia firsts include the completion of the GT42 page by Warren Wakarchuk in April 2010, the PL2 page by Wade Abbott in September 2013, the AA9 lytic polysaccharide mono-oxygenase page by Paul Harris in September 2013, and the CBM32 page by Elizabeth Ficko-Blean and Alisdair Boraston in May 2013. CAZypedia’s History page (available at URL https://www.cazypedia.org/index.php/CAZypedia:History, accessed via the About CAZypedia menu.) serves as a repository for these and future major milestones, while the News page (available at URL https://www.cazypedia.org/index.php/News and via CAZypedia’s Main Page.) covers recent Curator Approved pages and other newsworthy items. In recognition of the complex nature of carbohydrate chemistry and CAZymes, CAZypedia also incorporates a Lexicon that provides a definition of key terms, explanation of specialist nomenclature and tutorial reviews of concepts that are relevant to individual family pages. The Lexicon provides a touchstone for new readers to support their understanding and interpretation of individual families, and is hyperlinked within the text of family pages. The Lexicon and category pages for each major CAZyme class are conveniently accessed under the Content menu, prominently displayed on the left side of all CAZypedia pages (Figure 1). At its 10th anniversary online, CAZypedia currently comprises 106 GH, 10 CBM, 6 PL, 2 AA, 2 GT and 22 Lexicon pages with Curator Approved status. The MediaWiki software upon which CAZypedia relies tracks usage statistics, which are available through the Special Pages menu item. These statistics reveal over 12 million total page views, and over one hundred thousand views for several of the most popular GH and Lexicon pages. More conservative estimates of activity provided by Google Analytics indicate that CAZypedia access has increased to thousands of international users per week since data recording on that utility began in the autumn of 2009 (Figure 2). Regardless of the absolute values, these data highlight the sustained and growing value of CAZypedia to specialists and non-specialists alike. Fig. 2. View largeDownload slide CAZypedia usage statistics from Google Analytics. Access tracking with this service was initiated in August 2009. Sharp dips correspond to December holidays and broad troughs correspond to summer in the northern hemisphere. Fig. 2. View largeDownload slide CAZypedia usage statistics from Google Analytics. Access tracking with this service was initiated in August 2009. Sharp dips correspond to December holidays and broad troughs correspond to summer in the northern hemisphere. Editorial framework During the birth of CAZypedia, there was significant concern about the potential pitfalls of applying directly the Wikipedia model, which allows author anonymity and lacks formal editorial oversight, to the publication of a rigorous scientific encyclopedia. Thus, although CAZypedia adopts many of the general principles and rules of Wikipedia, CAZypedia draws on best-practice authoring and editing principles of peer-reviewed, wiki-based encyclopedia such as Citizendium (available at URL http://en.citizendium.org/) and Scholarpedia (available at URL http://www.scholarpedia.org). CAZypedia strives to be a dynamic, community-based resource, which at the same time balances the need for careful content curation. A full description of CAZypedia’s editorial policies is available on the About page (see URL https://www.cazypedia.org/index.php/CAZypedia:About, accessed via Introduction to CAZypedia under the About CAZypedia menu); however, a few points deserve special comment. The editorial organization of CAZypedia is designed with a minimum of bureaucratic and administrative overhead, because it is entirely volunteer-based and has no direct funding support. CAZypedia generally adopts Wikipedia’s Simplified Ruleset (available at URL http://en.wikipedia.org/wiki/Wikipedia:Simplified_Ruleset), particularly the concepts of using a neutral point-of-view, writing verifiable text, including only peer-reviewed information (no original research), being civil and well-behaved, and not infringing copyright. As a culmination of these principles, CAZypedia reports on—but does not engage in critique of—the published literature, and supports all statements of fact with primary citations. Not least, Wikipedia’s extensive “What Wikipedia is not” page (available at URL http://en.wikipedia.org/wiki/Wikipedia:What_Wikipedia_is_not) can be translated to “What CAZypedia is not” essentially point-by-point. Following the Citizendium model, transparency is achieved through the use of contributors’ real names in CAZypedia. Additionally, individual biographical pages enable readers to evaluate directly each contributor’s expertise in the field. To maintain editorial quality control, every Family and Lexicon page in CAZypedia is overseen by a Responsible Curator, who is primarily responsible for overall content. Responsible Curators are selected by a panel of Senior Curators based on established expertise and a willingness to participate in the active maintenance of specific pages. In turn, Responsible Curators are tasked with recruiting and managing Authors to participate in content creation; Responsible Curators may also contribute directly to composing page content. In the spirit of a community-driven resource, individuals are encouraged to self-nominate to become Responsible Curators or Authors. In general, individuals at any career stage are welcomed to participate as Authors, including keen undergraduates, postgraduate students and post-doctoral scientists. Indeed, the current list of contributors (see below) includes many junior scientists (or scientists who were at least junior at the time of their first contribution). Ultimately, the quality of entries in CAZypedia, like Wikipedia, relies upon the keen eye of readers at-large to identify errors and omissions. All users who spot such oversights are encouraged to contact the Responsible Curator for that page, so that a correction can be made. CAZypedia is an open-access publication, i.e., it is freely available online for anyone to read, study and otherwise use for scholarly pursuits. However, the Authors and Curators of CAZypedia assert their copyright for the sole purpose of preventing outright duplication and uncontrolled modification of the content, which could undermine the expert-based nature of this resource. Although we strongly advocate that readers should cite the primary research literature directly, individual CAZypedia pages may also be cited when practical, analogous to a book chapter or review article. Citation details are provided in the footer and via the Tools menu on each page (Figure 1). Technical aspects Wiki-wiki As introduced above, CAZypedia runs on MediaWiki, the free, open source PHP software originally developed for Wikipedia. This choice was based on the demonstrated robustness and scalability of MediaWiki, as well as the availability of diverse software extensions to add functionality. As Wikipedia is unlikely to disappear anytime soon, so too is MediaWiki’s active community of developers likely to persist well into the future, thereby ensuring continued maintenance of the software running CAZypedia. A full technical and functional description of MediaWiki is beyond the scope of this Letter; interested readers should visit MediaWiki.org for more details. For the content contributor and user, the most important practical aspect of the use of MediaWiki is that CAZypedia is a wiki: edits are displayed instantaneously when saved and do not require approval before appearing online. This enables dynamic development of page content driven by individual Authors. In the initial stages of development, pages are clearly marked as “Under Construction”, with a warning that content is under revision and may be subject to major changes. Once vetted by the Responsible Curator, a page may be upgraded to “Curator Approved” status to indicate that it is factually accurate and essentially complete. However, “completeness” is not absolute: as a wiki, CAZypedia is a living document, so further development of page content is forever possible. Creating content for CAZypedia is relatively intuitive. Once a new Author has been provided with a login, page editing can be conducted within a modern web browser using a simplified markup language. A boilerplate pre-populates the page with the major template features, and Authors can view the code of other pages to get ideas of ways to insert features like hyperlinks, references and figures. A “Getting Started Guide”, along with concise pages that provide help with editing, references and adding images provide guidance to assist the novice. Here, too, the use of MediaWiki as software platform is a considerable benefit, due to vast extant help resources on editing. Finally, assistance is always at hand from CAZypedia Curators, who are able to activity monitor edits via the global “Recent Changes” and individual “History” pages. BiblioPlus MediaWiki functionality can be enhanced through extensions, and CAZypedia utilizes several, including those for user administration, defining page boilerplate content and integrating Google Analytics. Among these, BiblioPlus (freely available at URL https://www.mediawiki.org/wiki/Extension:BiblioPlus) deserves special mention as the MediaWiki extension that drives bibliographic referencing. BiblioPlus is the result of a significant effort by CAZypedia contributor Karen Eddy to correct compatibility issues arising in the original Biblio extension by Martin Jambon and others (see URL https://www.mediawiki.org/wiki/Extension:Biblio). Like its predecessor, BiblioPlus performs automated retrieval and formatting of citations from PubMed and the ISBN databases in MediaWiki pages. Similar to other reference formatting software, BiblioPlus automatically numbers in-text citations and generates a reference section, which is included at the bottom of a page. Notably, the reference section contains hyperlinks to original sources, specifically PubMed or the ISBNdb, HubMed and DOI hyperlinks. BiblioPlus was specifically re-coded to utilize the modern NCBI Entrez Programming Utilities (E-utilities) interface (Anonymous 2010). A full description of features and usage instructions is available on the BiblioPlus Mediawiki extension page (URL https://www.mediawiki.org/wiki/Extension:BiblioPlus). It should be noted that BiblioPlus is freely available and will work together with any modern MediaWiki implementation, so that it may be broadly deployed in any wiki, scientific or otherwise. The next 10 years: CAZypedia needs you! The continued success of CAZypedia will remain entirely dependent on the diligence and commitment of experts and keen junior scientists to voluntarily contribute to the maintenance and growth of this reference work. The job of building CAZypedia is by no means complete, and as a living encyclopedia, it never will be—especially as research continues to reveal new CAZyme families, tertiary structures and mechanistic details (e.g., Campos et al. 2016; Venditto et al. 2016; Abe et al. 2017; Munoz-Munoz, Cartmell, Terrapon, Basle 2017; Munoz-Munoz, Cartmell, Terrapon, Henrissat 2017; Ndeh et al. 2017). Currently, many pages remain to be written and existing pages would benefit from regular updates as new data come to hand, which requires expert volunteers willing to assume the responsibility for page creation and maintenance. Thus, the CAZypedia Consortium openly invites all interested glycoscientists, regardless of career stage (including keen undergraduate and postgraduate students, post-doctoral researchers, industrial scientists and professors) to peruse the “Unassigned Pages” lists for each CAZyme class and see if they might be able to help. The growth of CAZypedia will depend exclusively on the generous and selfless contributions of the existing and new generations of CAZypedians. We invite you to join us! Contact information is available at URL http://www.cazypedia.org/. Acknowledgments We thank Stephen MacDonald and Vince Tingey (Michael Smith Laboratories, University of British Columbia), and Eric Björkvall (School of Biotechnology, Kungliga Tekniska Högskolan), for invaluable IT support. Dr. Karen Eddy (Brumer group, MSL, UBC) is thanked for developing the BiblioPlus extension. CAZypedia is the result of many hours of effort by the following group of current contributors (A continually updated list is available at URL http://www.cazypedia.org/index.php/Category:Contributors, accessed via the “About CAZypedia” menu.): Wade Abbott, Agriculture and Agri-Food Canada, Canada; Orly Alber, Weizmann Institute of Science, Israel; Ed Bayer, Weizmann Institute of Science, Israel; Jean-Guy Berrin, Institut National de la Recherche Agronomique, France; Alisdair Boraston, University of Victoria, Canada; Harry Brumer, University of British Columbia, Canada; Ryszard Brzezinski, Université de Sherbrooke, Canada; Anthony Clarke, University of Guelph, Canada; Beatrice Cobucci-Ponzano, National Research Council of Italy, Italy; Darrell Cockburn, Penn State University, United States of America; Pedro Coutinho, Aix Marseille Université, France; Mirjam Czjzek, Centre National de la Recherche Scientifique, France; Bareket Dassa, Weizmann Institute of Science, Israel; Gideon John Davies, University of York, United Kingdom; Vincent Eijsink, Norwegian University of Life Sciences, Norway; Jens Eklöf, University of British Columbia, Canada; Alfons Felice, Universität für Bodenkultur, Austria; Elizabeth Ficko-Blean, Centre National de la Recherche Scientifique, France; Geoff Fincher, University of Adelaide, Australia; Thierry Fontaine, Institut Pasteur, France; Zui Fujimoto, National Agriculture and Food Research Organisation, Japan; Kiyotaka Fujita, Kagoshima University, Japan; Shinya Fushinobu, University of Tokyo, Japan; Harry Gilbert, Newcastle University, United Kingdom; Tracey Gloster, University of St. Andrews, United Kingdom; Ethan Goddard-Borger, Walter and Eliza Hall Institute of Medical Research, Australia; Ian Greig, Simon Fraser University, Canada; Jan-Hendrik Hehemann, Max Planck Institute for Marine Microbiology, Germany; Glyn Hemsworth, University of Leeds, United Kingdom; Bernard Henrissat, Centre National de la Recherche Scientifique, France; Masafumi Hidaka, University of Tokyo, Japan; Ramon Hurtado-Guerrero, University of Zaragoza, Spain; Kiyohiko Igarashi, University of Tokyo, Japan; Takuya Ishida, University of Tokyo, Japan; Stefan Janecek, Slovak Academy of Sciences, Slovakia; Seino Jongkees, University of Tokyo, Japan; Nathalie Juge, Quadram Institute, United Kingdom; Satoshi Kaneko, University of the Ryukyus, Japan; Takane Katayama, Ishikawa Prefectural University, Japan; Motomitsu Kitaoka, National Agriculture and Food Research Organisation, Japan; Naotake Konno, Utsunomiya University, Japan; Daniel Kracher, Universität für Bodenkultur, Austria; Anna Kulminskaya, Petersburg Nuclear Physics Institute, Russia; Alicia Lammerts van Bueren, University of Groningen, Netherlands; Sine Larsen, University of Copenhagen, Denmark; Junho Lee, University of British Columbia, Canada; Markus Linder, Aalto University, Finland; Leila LoLeggio, University of Copenhagen, Denmark; Roland Ludwig, Universität für Bodenkultur, Austria; Ana Luis, Universtiy of Lisbon, Portugal; Mirko Maksimainen, University of Oulu, Finland; Brian Mark, University of Manitoba, Canada; Richard McLean, University of Lethbridge, Canada; Gurvan Michel, Centre National de la Recherche Scientifique, France; Cedric Montanier, Institut National de la Recherche Agronomique, France; Marco Moracci, National Research Council of Italy, Italy; Haruhide Mori, Hokkaido University, Japan; Hiroyuki Nakai, Niigata University, Japan; Wim Nerinckx, Ghent University, Belgium; Takayuki Ohnuma, Kinki University, Japan; Richard Pickersgill, Queen Mary University of London, United Kingdom; Kathleen Piens, Sveriges Lantbruksuniversitet, Sweden; Tirso Pons, National Centre for Biotechnology, Spain; Etienne Rebuffet, Centre National de la Recherche Scientifique, France; Peter Reilly, Iowa State University, United States of America; Magali Remaud-Simeon, Institut National des Sciences Appliquées, France; Brian Rempel, University of British Columbia, Canada; Kyle Robinson, University of British Columbia, Canada; David Rose, University of Waterloo, Canada; Juha Rouvinen, University of Eastern Finland, Finland; Wataru Saburi, Hokkaido University, Japan; Yuichi Sakamoto, Iwate Biotechnology Research Center, Japan; Mats Sandgren, Sveriges Lantbruksuniversitet, Sweden; Fathima Shaikh, University of British Columbia, Canada; Yuval Shoham, Technion, Israel; Franz St. John, United States Department of Agriculture, United States of America; Jerry Stahlberg, Sveriges Lantbruksuniversitet, Sweden; Michael Suits, Wilfrid Laurier University, Canada; Gerlind Sulzenbacher, Centre National de la Recherche Scientifique, France; Tomomi Sumida, RIKEN, Japan; Ryuichiro Suzuki, Akita Prefectural University, Japan; Birte Svensson, Danmarks Tekniske Universitet, Denmark; Toki Taira, University of the Ryukyus, Japan; Ed Taylor, University of Lincoln, United Kingdom; Takashi Tonozuka, Tokyo University of Agriculture and Technology, Japan; Breeanna Urbanowicz, University of Georgia, United States of America; Gustav Vaaje-Kolstad, Norwegian University of Life Sciences, Norway; Wim Van den Ende, Katholieke Universiteit Leuven, Belgium; Annabelle Varrot, Centre National de la Recherche Scientifique, France; Maxime Versluys, Katholieke Universiteit Leuven, Belgium; Florence Vincent, Centre National de la Recherche Scientifique, France; David Vocadlo, Simon Fraser University, Canada; Warren Wakarchuk, Ryerson University, Canada; Tom Wennekes, Universiteit Utrecht, Netherlands; Rohan Williams, University of Melbourne, Australia; Spencer Williams, University of Melbourne, Australia; David Wilson†, Cornell University, United States of America; Stephen Withers, University of British Columbia, Canada; Katsuro Yaoi, National Institute of Advanced Industrial Science and Technology, Japan; Vivian Yip, University of British Columbia, Canada; Ran Zhang, University of British Columbia, Canada. This Letter was composed by H. Brumer (brumer@msl.ubc.ca) and S.J. Williams (sjwill@unimelb.edu.au), with input from B. Svensson, B. Henrissat, G.J. Davies, H.J. Gilbert, A.J. Clarke, W.W. Wakarchuk, D.W. Abbott, D.J. Vocadlo, E. Ficko-Blean, A.B. Boraston, A. Planas, and S. Fushinobu. Page charges for this article were supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to H. Brumer. References Abe K, Nakajima M, Yamashita T, Matsunaga H, Kamisuki S, Nihira T, Takahashi Y, Sugimoto N, Miyanaga A, Nakai H et al.  . 2017. Biochemical and structural analyses of a bacterial endo-beta-1,2-glucanase reveal a new glycoside hydrolase family. J Biol Chem . 292: 7487– 7506. Google Scholar CrossRef Search ADS PubMed  Anonymous. 2010. Entrez Programming Utilities Help National Center for Biotechnology Information:Bethesda, MD, USA. Available from: https://www.ncbi.nlm.nih.gov/books/NBK25501/. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 2004. Carbohydrate-binding modules: Fine-tuning polysaccharide recognition. Biochem J . 382: 769– 781. Google Scholar CrossRef Search ADS PubMed  Bourne PE, McEntyre J. 2006. Biocurators: Contributors to the world of science. PLoS Comput Biol . 2: 1185– 1185. Campos BM, Liberato MV, Alvarez TM, Zanphorlin LM, Ematsu GC, Barud H, Polikarpov I, Ruller R, Gilbert HJ, Zeri ACD et al.  . 2016. A novel carbohydrate-binding module from sugar cane soil metagenome featuring unique structural and carbohydrate affinity properties. J Biol Chem . 291: 23734– 23743. Google Scholar CrossRef Search ADS PubMed  Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. J Mol Biol . 328: 307– 317. Google Scholar CrossRef Search ADS PubMed  Davies G, Henrissat B. 1995. Structures and mechanisms of glycosyl hydrolases. Structure . 3: 853– 859. Google Scholar CrossRef Search ADS PubMed  Davies GJ, Sinnott ML. 2008. Sorting the diverse. Biochemist . 30: 26– 32. Henrissat B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J . 280: 309– 316. Google Scholar CrossRef Search ADS PubMed  Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. 2013. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels . 6: 14. Google Scholar CrossRef Search ADS PubMed  Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 2010. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J . 432: 437– 444. Google Scholar CrossRef Search ADS PubMed  Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res . 42: D490– D495. Google Scholar CrossRef Search ADS PubMed  Munoz-Munoz J, Cartmell A, Terrapon N, Basle A, Henrissat B, Gilbert HJ. 2017. An evolutionarily distinct family of polysaccharide lyases removes rhamnose capping of complex arabinogalactan proteins. J Biol Chem . 292: 13271– 13283. Google Scholar CrossRef Search ADS PubMed  Munoz-Munoz J, Cartmell A, Terrapon N, Henrissat B, Gilbert HJ. 2017. Unusual active site location and catalytic apparatus in a glycoside hydrolase family. Proc Natl Acad Sci U S A . 114: 4936– 4941. Google Scholar CrossRef Search ADS PubMed  Ndeh D, Rogowski A, Cartmell A, Luis AS, Basle A, Gray J, Venditto I, Briggs J, Zhang XY, Labourel A et al.  . 2017. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature . 544: 65– 70. Google Scholar CrossRef Search ADS PubMed  Sinnott ML. 1990. Catalytic mechanisms of enzymatic glycosyl transfer. Chem Rev . 90: 1171– 1202. Google Scholar CrossRef Search ADS   Venditto I, Luis AS, Rydahl M, Schuckel J, Fernandes VO, Vidal-Melgosa S, Bule P, Goyal A, Pires VMR, Dourado CG et al.  . 2016. Complexity of the Ruminococcus flavefaciens cellulosome reflects an expansion in glycan recognition. Proc Natl Acad Sci U S A . 113: 7136– 7141. Google Scholar CrossRef Search ADS PubMed  Whelan W. 2009. Obituary: Bruce A. Stone. IUBMB Life . 61: 84– 84. Google Scholar CrossRef Search ADS   Author notes Dedication: CAZypedia is dedicated to Emeritus Professor Bruce Stone (1928–2008†), whose enthusiasm to create a comprehensive encyclopedia of carbohydrate-active enzymes was essential to the genesis of this resource. © The Author 2017. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

Journal

GlycobiologyOxford University Press

Published: Jan 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 12 million articles from more than
10,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Unlimited reading

Read as many articles as you need. Full articles with original layout, charts and figures. Read online, from anywhere.

Stay up to date

Keep up with your field with Personalized Recommendations and Follow Journals to get automatic updates.

Organize your research

It’s easy to organize your research with our built-in tools.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

Monthly Plan

  • Read unlimited articles
  • Personalized recommendations
  • No expiration
  • Print 20 pages per month
  • 20% off on PDF purchases
  • Organize your research
  • Get updates on your journals and topic searches

$49/month

Start Free Trial

14-day Free Trial

Best Deal — 39% off

Annual Plan

  • All the features of the Professional Plan, but for 39% off!
  • Billed annually
  • No expiration
  • For the normal price of 10 articles elsewhere, you get one full year of unlimited access to articles.

$588

$360/year

billed annually
Start Free Trial

14-day Free Trial