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Ten years of CAZypedia : A living encyclopedia of carbohydrate-active enzymes The CAZypedia Consortium Oct 11, 2017

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Ten years of CAZypedia: A living encyclopedia of carbohydrate-active enzymes The CAZypedia Consortium* *A list of contributors at the time of publication is provided in the Acknowledgements.  All past and future CAZypedia Editors and Authors are invited to cite this article in reference to their invaluable contributions to this community resource. 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.  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.  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, B. 1991), the CAZy database1 continues to grow and currently (August 2017) encompasses 104 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, A., Drula, E., et al. 2013, Lombard, V., Ramulu, H.G., et al. 2014).  As a result of vigorous biocuration [as defined by Bourne and McEntyre (Bourne, P.E. and McEntyre, J. 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, G.J. and Sinnott, M.L. 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.                                                            1 Available at URL http://www.cazy.org/  Additionally, individual genome pages provide a convenient census of all CAZyme families in individual organisms (Lombard, V., Ramulu, H.G., 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, W. 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 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 7th 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 wiki2 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.3 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 (Davies, G. and Henrissat, B. 1995, Sinnott, M.L. 1990).  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                                                           2 See definition at URL https://en.wikipedia.org/wiki/Wiki  3 Freely available at URL https://www.mediawiki.org/  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. 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 Glycoside Hydrolase Family 12 page by Gerlind Sulzenbacher as the 100th Curator Approved GH page.  Pages on other groups of CAZymes (i.e., Glycosyltransferases (Coutinho, P.M., Deleury, E., et al. 2003), Polysaccharide Lyases (Lombard, V., Bernard, T., et al. 2010), and Auxiliary Activity redox enzymes (Levasseur, A., Drula, E., et al. 2013)) and non-catalytic Carbohydrate Binding Modules (Boraston, A.B., Bolam, D.N., 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 page4 serves as a repository for these and future major milestones, while the News page5 covers recent Curator Approved pages and other newsworthy items.                                                           4 Available at URL https://www.cazypedia.org/index.php/CAZypedia:History, accessed via the ‘About CAZypedia’ menu. 5 Available at URL https://www.cazypedia.org/index.php/News and via CAZypedia’s Main Page. 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 linked using hyperlinks from 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. 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 Citizendium6 and Scholarpedia7.  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” page8; 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”9, 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” page10 can be translated to “What CAZypedia is not” essentially point-by-point.                                                           6 Available at URL http://en.citizendium.org/  7 Available at URL http://www.scholarpedia.org  8 See URL https://www.cazypedia.org/index.php/CAZypedia:About, accessed via ‘Introduction to CAZypedia’ under the ‘About CAZypedia’ menu 9 Available at URL http://en.wikipedia.org/wiki/Wikipedia:Simplified_Ruleset  10 Available at URL http://en.wikipedia.org/wiki/Wikipedia:What_Wikipedia_is_not  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, post-graduate 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 article; 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, BiblioPlus11 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.12   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.11  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 (Abe, K., Nakajima, M., et al. 2017, Campos, B.M., Liberato, M.V., et al. 2016, Munoz-Munoz, J., Cartmell, A., et al. 2017a, Munoz-Munoz, J., Cartmell, A., et al. 2017b, Ndeh, D., Rogowski, A., et al. 2017, Venditto, I., Luis, A.S., et al. 2016).  Currently, many pages remain to be written and existing pages would benefit from regular updates as new data come to hand, which requires the identification of experts willing to assume the responsibility for page creation and maintenance.                                                            11 Freely available at URL https://www.mediawiki.org/wiki/Extension:BiblioPlus  12 See URL https://www.mediawiki.org/wiki/Extension:Biblio  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/. Acknowledgements 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 extension13.  CAZypedia is the result of many hours of effort by the following group of current contributors:14  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                                                           13 Freely available for download at URL https://www.mediawiki.org/wiki/Extension:BiblioPlus  14 A continually updated list is available at URL http://www.cazypedia.org/index.php/Category:Contributors, accessed via the ‘About CAZypedia’ menu. 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. Journal of Biological Chemistry, 292:7487-7506. 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. Biochemical Journal, 382:769-781. Bourne PE, McEntyre J. 2006. Biocurators: Contributors to the world of science. PLoS Computational Biology, 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. Journal of Biological Chemistry, 291:23734-23743. Coutinho PM, Deleury E, Davies GJ, Henrissat B. 2003. An evolving hierarchical family classification for glycosyltransferases. Journal of Molecular Biology, 328:307-317. Davies G, Henrissat B. 1995. Structures and Mechanisms of Glycosyl Hydrolases. Structure, 3:853-859. Davies GJ, Sinnott ML. 2008. Sorting the Diverse. The Biochemist, 30:26-32. Henrissat B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal, 280:309-316. 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. Biotechnology for Biofuels, 6:14. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 2010. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochemical Journal, 432:437-444. 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. Munoz-Munoz J, Cartmell A, Terrapon N, Basle A, Henrissat B, Gilbert HJ. 2017a. An evolutionarily distinct family of polysaccharide lyases removes rhamnose capping of complex arabinogalactan proteins. The Journal of biological chemistry, 292:13271-13283. Munoz-Munoz J, Cartmell A, Terrapon N, Henrissat B, Gilbert HJ. 2017b. Unusual active site location and catalytic apparatus in a glycoside hydrolase family. Proceedings of the National Academy of Sciences of the United States of America, 114:4936-4941. 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-+. Sinnott ML. 1990. Catalytic mechanisms of enzymatic glycosyl transfer. Chemical Reviews, 90:1171-1202. 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. Proceedings of the National Academy of Sciences of the United States of America, 113:7136-7141. Whelan W. 2009. Obituary: Bruce A. Stone. IUBMB Life, 61:84-84.    Figures  Figure 1. Layout of a typical CAZyme family page in CAZypedia.    Figure 2.  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. 

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