CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities
Bioresources and Bioprocessing volume 6, Article number: 51 (2019)
Annually, plants convert 100 billion tons of carbon dioxide and water to cellulose through photosynthesis (Field et al. 1998). Plant woody biomass is composed of carbohydrates (65–75%) (majorly separated into cellulose, hemicellulose and pectin), lignin (up to 20–30%), extraneous organic molecules (4–10%) and minerals (Pettersen 1984). Industries and researchers are continuously attempting new methods to explore and exploit plant woody biomass as a source of fermentable sugars (Carroll and Somerville 2009; Glass et al. 2013; Pauly and Keegstra 2008). However, the high recalcitrant nature and intricate networking properties of lignocellulose are major hurdles for industries to efficiently produce biofuels from plant biomass (Bischof et al. 2016; Himmel and Bayer 2009; Kubicek et al. 2009; Peterson and Nevalainen 2012). Previous studies have reported few bacterial strains and several wood-decaying fungi (classified as white rot, brown rot and soft rot fungi) have exhibited extrinsic lignocellulolytic abilities (Bischof et al. 2016; Peterson and Nevalainen 2012). Studies based on microbial degradation and conversion of plant biomass components to cellulosic ethanol and commercially important platform chemicals are rapidly gaining attention around the world (Abraha et al. 2019; Lijó et al. 2019; Lynd et al. 2008; Van Meerbeek et al. 2019; Zhu and Pan 2010). In the last decade several bacterial and fungal strains were identified and characterized around the world specifically to understand their lignocellulose degrading abilities (Bischof et al. 2016). Conventionally, the lignocellulolytic abilities of microorganisms are characterized in laboratories using various biochemical assays and methods. Although, by using the whole genome and transcriptome sequences we can completely understand the genome-wide distribution of CAZymes in a given fungi (Bischof et al. 2016; Lynd et al. 2008; Peterson and Nevalainen 2012; Zhu and Pan 2010).
Fungi secretes a variety of enzymes for the degradation of organic waste present on the earth’s surface thus, fungi play a crucial role in maintaining the nutritional cycles of our ecosystem (Glass et al. 2013). Compared to other microorganisms, filamentous fungi exhibit extrinsic plant biomass degrading abilities and industrially these fungi are highly important, e.g., food, beverage, pharmaceutical industries and also in production of commercially important enzymes (Himmel and Bayer 2009; Kubicek et al. 2009). Trichoderma reesei (Hypocrea jecorina), Aspergillus niger and Neurospora crassa are popular and commonly used industrial fungi for the production of commercial grade cellulases and several other highly catalytic enzymes. Recent fungal genomic studies strongly endorse the plant biomass degrading abilities of ascomycetes and basidiomycetous fungi (de Vries and Visser 2001; Dunlap et al. 2007; Glass et al. 2013). Development of public repositories such as JGI-MycoCosm, 1000 fungal genome project, Hungate genome projects have fueled the genome sequencing projects of several wood-decaying fungi and bacteria (Bischof et al. 2016; Lynd et al. 2008; Peterson and Nevalainen 2012; Zhu and Pan 2010). Understanding the genetic makeup of a microorganism in the first phase can reveal its plant biomass degrading abilities.
State of the art reviews have extensively reported about the plant cell wall-deconstructing enzymes in the past (Bateman and Basham 1976; de Vries and Visser 2001; Doi and Kosugi 2004; Glass et al. 2013; Minic and Jouanin 2006). Zhao et al. (2013) have compared the proteomic annotations of plant cell wall-degrading enzymes of 103 fungi representing different fungal phylum’s (Zhao et al. 2013). This study has reported about the genetic diversity of fungi, and the influence of fungal nutrition and host specificity on genome-wide composition of fungal CAZymes (Zhao et al. 2013). In our previous studies, we have compared the genome-wide distribution of CAZymes (carbohydrate-active enzymes) among the popular white rot, brown rot and soft rot fungi to understand and reveal their lignocellulolytic abilities and later ranked the fungi based on their degrading abilities. Similarly, we have also compared the genome-wide annotations of anaerobic fungi belonging to Neocallimastigomycota division to understand their plant cell wall-degrading and biohydrogen-producing abilities. Studies focused on understanding the plant cell wall-degrading abilities of individual fungal strains were reported in the last decade (Castillo et al. 2017; Geiser et al. 2016; Henske et al. 2017; Hüttner et al. 2017; Looi et al. 2017; Qin et al. 2017; Vidal-Melgosa et al. 2015; Zhang et al. 2016).
The microbial enzymes involved in plant cell wall-degradation are collectively called carbohydrate-active enzymes (CAZymes). These CAZymes were classified into six major groups as glycoside hydrolases, glycosyl transferases, polysaccharide lyases, carbohydrate esterases, auxiliary activity enzymes and carbohydrate-binding modules (Lombard et al. 2013). CAZy database has played a key role in enhancing present day’s knowledge about carbohydrate-active enzymes and it has influenced various groups around the world to pursue research on CAZymes. The primary understanding of CAZymes’ and their mode of action would significantly benefit the researchers identifying microorganisms with extrinsic plant cell wall-degrading enzymes (King et al. 2011; Kubicek et al. 2009; Zhao et al. 2013). However, the immenseness of the present day’s CAZy database makes it difficult for the researchers to specifically track down CAZymes based on the substrate they degrade. Biological contextualization of the whole genome sequencing studies of microorganisms using annotating databases such as InterPro (Hunter et al. 2008), dbCAN (Yin et al. 2012), CAT (Park et al. 2010) Hotpep (Halima 2019), provides the genome-wide CAZy annotations. However, the CAZyme annotations obtained are listed by their group and family numbers, e.g., GH1. Presently, to find all the enzymes that are classified in the GH1 family one must visit the CAZy web-database → select “Enzyme classes” → select “Glycoside Hydrolases” → select “GH1” and then specifically look for the enzyme of your interest.
In this study, we have reported a basic search page for finding and retrieving the complete list of CAZymes involved in biosynthesis and breakdown of carbohydrates. We have listed all the CAZymes groups and families that are involved in the degradation and conversion of plant cell wall components such as cellulose, hemicellulose, lignin, pectin, starch and inulin. This search page can be used as a primary material for understanding, exploring and designing CAZyme-based experiments. We have also reported a simple and efficient web-database for searching and short-listing the fungi based on CAZyme group or class which are involved in depolymerization of plant cell wall carbohydrates. To the best of our knowledge this study reports the first web-database with search functionalities for identifying a specific fungus based on its CAZyme coding abilities. Understanding the genome-wide distribution of CAZymes in first phase will significantly benefit the fungal laboratory and industrial-based projects.
Materials and methods
Design and construction of S-CAZymes
We have manually retrieved all the carbohydrate-active enzymes from the CAZy database (http://www.cazy.org/) which were originally classified under auxiliary activity, polysaccharide lyases, glucosyl transferases, glycoside hydrolases, carbohydrate esterases and carbohydrate-binding modules enzyme classes, respectively. The S-CAZy website contains three pages:
Plant cell wall-degrading CAZymes (PCW-DE): as our primary research focus was to study about the plant cell wall component degrading CAZymes (such as cellulose, hemicellulose, lignin, pectin, chitin, starch and inulin degrading CAZymes).
Search for CAZymes and CAZy families (S-CAZymes): we have provided a dynamic search functionality to search among all the listed CAZymes (full names) and their corresponding enzyme commission numbers, which enables us to retrieve the list of CAZymes involved in biosynthesis and depolymerization of carbohydrates.
Enzyme activities (E.As) exhibited by carbohydrate-binding modules (CBM): similarly, in E.A-CBM webpage we have provided dynamic functionality to retrieve all the CBMs and their corresponding enzyme activities, E.A-CBM webpage lists the enzyme commission number, enzyme activities exhibited by CBM domains and all the corresponding CBM classes.
We have used HTML (hypertext markup language) version 5 majorly for developing our S-CAZy webpage. The webpage layout was designed and arranged using the bootstrap framework of CSS (cascading style sheets) https://maxcdn.bootstrapcdn.com/bootstrap/3.3.7/css/bootstrap.min.css. The dynamic search functionality for the S-CAZymes and E.A-CBM web pages were developed using the ajax google api https://ajax.googleapis.com/ajax/libs/jquery/3.3.1/jquery.min.js and bootstrap https://maxcdn.bootstrapcdn.com/bootstrap/3.3.7/js/bootstrap.min.js Java scripts, respectively. (http://188.8.131.52/RankEnzymes/SearchCAZymeCAZyClasses).
CBRF web-database design
As of today, the JGI-MycoCosm database resides 1057 fungal genome projects out of which 443 fungal genomes were published, publicly available and 613 fungal genomes are not published. In our present project, we have retrieved genome-wide distribution of CAZy annotations (CAZy groups and classes) of 443 published fungal genomes. Out of these 443 fungal genomes, 56 fungal genomes do not include CAZy annotations as of today. The CBRF web-database was designed with two major functionalities (a) sorting functions: ascending or descending orders and (b) sorting fungi based on CAZymes. The “sorting fungi based on CAZymes” function lists all the CAZy enzyme classes and groups (e.g., AA → AA1), these sorting options can also be selected using the dropdown option (which automatically pops up once user starts typing). Using the existing literature and based on our previous studies we have separated and classified the CAZymes based on the substrate they act such as: (a) cellulose, (b) hemicellulose, (c) lignin, (d) pectin, (e) starch and (f) inulin. We have provided the sorting functions for each of plant cell wall components (i.e., cellulose-C, hemicellulose-H, lignin-L, pectin-P, inulin-In and starch-S, respectively), e.g., the listed fungi are sorted based on their total cellulolytic ability (calculated by adding all the genes encoding for cellulolytic CAZymes). We have also provided a specific “Search-box” function to search for a specific fungus using its scientific name for comparing and analyzing its plant cell wall-degrading abilities.
Results and discussion
Initial understanding about distribution of CAZymes in a selected microorganism’s genome will significantly help in conducting further experiments which benefits several microbe-based industries by developing cost- and time-efficient processes. As mentioned above in data retrieval section CAZy database is widely distributed, each CAZy family further includes several enzymes that are grouped based on their structural features (Busk and Lange 2013; Davies and Henrissat 1995; Henrissat 1991; Henrissat and Bairoch 1993, 1996; Henrissat and Davies 1997). Previous studies have extensively reported that microorganisms with wide variety of CAZymes can exhibit higher plant biomass degrading abilities (Daly et al. 2017; López et al. 2018; Min et al. 2017; Miyauchi et al. 2017; O’Connell et al. 2012) (Fig. 1).
Plant cell wall-degrading CAZymes (PCW-DE)
Using the pre-existing literature and CAZy web-repository, we have tentatively grouped the CAZymes based on the substrate they act upon. The CAZy groups and classes encoding for endoβ-(1→4) glucanases (cellulase), exo β-(1→4) glucanases (cellodextrinases), β-glucosidases, cellulase β-(1→4) cellobiosidase, lytic polysaccharide monoxygenases, cellobiose dehydrogenase, GMC-oxidoreductase and cellulose-binding domains were grouped as cellulose depolymerizing enzymes (Fig. 2). CAZy groups and classes encoding for endo-β-1,4-xylanase, β-glucosidase, β-mannosidase, β-xylosidase, Glucan β-1,3-glucosidase, mannan endo-β-1,4-mannosidase, alpha-l-arabinofuranosidase, xyloglucan-specific endo-β-1,4-glucanase, glucuronoarabinoxylan-specific endo-β-1,4-xylanase, arabinoxylan-specific endo-β-1,4-xylanase, acetyl xylan esterase, LPMO, xylan-binding modules, mannan-binding modules, arabinoxylan-binding modules and xyloglucan-binding modules were listed as hemicellulose-depolymerizing enzymes (Fig. 2).
Similarly, CAZy groups and classes encoding for laccase, p-diphenol oxygen oxidoreductase, ferroxidase, laccase-like multicopper oxidase, lignin peroxidase, manganese peroxidase, versatile peroxidase, peroxidase, aryl-alcohol oxidase, alcohol oxidase, pyranose oxidase, cellobiose dehydrogenase, GMC-oxidoreductases, vanillyl alcohol oxidase, alcohol oxidase, glyoxal oxidase, galactose oxidase, 1,4-benzoquinone reductase, Iron reductase, pyrroloquinoline quinone-dependent oxidoreductase, feruloyl esterase, cinnamoyl esterase, 4-O-methyl-glucuronoyl methylesterase and aryl esterase, carboxyl esterase were listed as lignin depolymerizing enzyme (Fig. 2) (Kameshwar and Qin 2019). The pectin-depolymerizing enzymes contained CAZy groups and classes encoding for polygalacturonase, exo-polygalacturonase, exo-poly-galacturonosidase, rhamnogalacturonase, rhamnogalacturonan α-1,2-galacturonohydrolase, α-l-rhamnosidase, exo-polygalacturonase, rhamnogalacturonan α-l-rhamnohydrolase, α-l-arabinofuranosidase, exo-α-l-1,5-arabinanase, β-galactosidase, pectate lyase, exo-pectate lyase, pectin Lyase, rhamnogalacturonan endolyase, rhamnogalacturonan exolyase, oligogalacturonate lyase, pectin methylesterase, pectin acetylesterase, rhamnogalacturonan acetylesterase, pectin acetylesterase, acetylesterase, pectin binding modules, galactan binding modules, l-rhamnose binding modules, arabinogalactan binding modules, respectively (Fig. 2). Finally, the CAZy groups and classes encoding for α-amylases, LPMO, α-glucosidase, starch phosphorylase, starch binding modules and endo-inulinase, exo-inulinase, inulin lyase and inulin binding module were listed for the starch and inulin depolymerizing enzymes, respectively (Fig. 2) (Kameshwar and Qin 2019).
Search-CAZymes (S-CAZy) and E.A-CBM webpages
The webpage: S-CAZy and enzymatic activities exhibited by CBM domains contain an efficient search option for finding a specific CAZyme from the complete CAZy classification. For instance, searching the S-CAZy webpage with the term “endo-beta-1,4-glucanase” would result in GH families GH5, GH7 and GH48, respectively. The S-CAZy webpage can also be used to find all the CAZymes involved in biosynthesis and breakdown of a specific substrate. For instance, the searching the S-CAZy webpage with first three letters of the term “manno”, “arabino” or “fructo” will result in all the CAZymes involved with biosynthesis or degradation of mannans, arabinans and fructosans (inulin), respectively. During its evolution glycoside hydrolases have separated into catalytic domain and non-catalytic carbohydrate-binding modules (CBM) which bind to the solid polysaccharides (Boraston et al. 2004). Previously, these polysaccharide recognizing polypeptides were named as cellulose-binding modules (CBM) or binding domains (CBD), however, due to their binding ability to a variety of polysaccharides, they were renamed as carbohydrate-binding modules (Boraston 1999). As of today, CAZy database hosts 83 CBM families, out of which cellulose-binding modules are distributed in 25 CBM families. CBMs can be majorly classified into three types: A-type (CBMs bind to surfaces of crystalline polysaccharides, e.g., cellulose, chitin), B-type (CBMs bind to internal longer sugar chains with more than four monosaccharide units) and C-type (CBMs bind to the ends of shorter sugar chains with not more than 3 monosaccharide units) (Armenta et al. 2017; Boraston et al. 2004; Gilbert et al. 2013). The “Enzymatic activities exhibited by CBM domains” webpage can be used for finding the carbohydrate-binding modules associated with a specific enzyme module. For e.g., searching E.A-CBM webpage with “cellulase” or with its E.C. number-184.108.40.206 will list all the CBM families associated with the cellulase enzymes, respectively. However, this page does not list the enzymatic activities corresponding to enzyme commission numbers “1.-.-.-.”, “2.4.1.-”, “2.4.2.-”, “3.1.1.-”, “3.2.1.-” and “4.2.2.-” as they do not correspond to a specific enzyme type.
Genome-wide proteomic studies of bacteria and fungi using microarray and RNA-sequencing results in huge data containing gene expression profiles which are either up or down regulated at cellular level. The RNA sequencing of various basidiomycetous fungi especially Phanerochaete chrysosporium, Postia placenta and several bacterial species have been already reported in the literature. The CAZy database (dbCAN) is widely used for annotating the newly sequenced genomes however, these genome-wide annotations are represented by their respective CAZy group and class number, e.g., GH1, GH2, GH45, etc. These CAZy group and class number does not reveal any additional information about the CAZyme or its function. At the same time, it is tedious to individually retrieve all the CAZymes based on the substrate they degrade from the CAZy database in a single step. The S-CAZy website can be used as a primer for specifically retrieving (a) all the plant cell wall-degrading CAZymes based on substrates; (b) classification (CAZy group and class) of a specific CAZyme in the CAZy database and (c) the basic information of the CAZymes of interest (Additional file 1) [Note: S-CAZymes webpage is just a simple search page to support and simplify the search process of CAZymes. However, for further information about carbohydrate-active enzymes (CAZymes) please visit: http://www.cazy.org/CAZy database].
Putative plant cell wall-degrading abilities
Recent genomic and proteomic studies of various plant cell wall-degrading fungi were centrally focused on lignocellulolytic CAZymes their occurrence and expression (Castillo et al. 2017; Geiser et al. 2016; Vidal-Melgosa et al. 2015; Zhang et al. 2016; Zhao et al. 2013). Knowing about the lignocellulolytic abilities of a microorganism prior to its experimentation will significantly benefit both the laboratory and industrial-based projects. Thus, in CBRF web database we have specifically added the simple functionalities for sorting fungi based on its plant cell wall-degrading abilities. We have retrieved the tentative CAZy groups and classes involved in cellulose, hemicellulose, lignin, pectin, starch and inulin depolymerization from the PCW-DE webpage of S-CAZymes. Using this information, we have tentatively developed a function for calculating all the genes encoding for CAZy groups and classes involved in degradation of plant cell wall components among all the 443 annotated fungal genomes. CBRF web-database displays all the fungi based on the selected sorting order. Using the CBRF web-database one can easily identify a specific fungus exhibiting extrinsic plant biomass degrading abilities (cellulose, hemicellulose, pectin, lignin, starch and inulin degrading CAZymes) by using the above-mentioned sorting functionality (Fig. 2).
CBRF framework, design and layout
As of today, approximately 11,264 studies include the term “plant cell wall degradation” in PubMed database, respectively. Out of which, 244 studies were related to plant cell wall-degrading microorganisms, 268 studies were based on CAZymes, 2985 studies related to plant cell wall degradation by fungi and 15 studies were based on plant cell wall-degrading fungal CAZymes, respectively (Fig. 3a). The JGI-MycoCosm, public repository presently hosts 1087-fungal genomes out of which 443-fungal genomes are published and 644-fungal genomes are sequenced but not published as of today (Fig. 3b) (Grigoriev et al. 2011, 2013). Based on their classification these 443 publicly available fungal genomes can be separated into 134 Basidiomycota, 264 Ascomycota, 7 Glomeromycota, 2 Mortierellomycotina, 12 Mucoromycotina, 2 Entomophthoromycotina, 6 Kickxellomycotina, 1 Blastocladiomycota, 3 Chytridiomycota, 5 Neocallimastigomycota, 8 Microsporidia and 1 Cryptomycota (Fig. 3b). However, out of these 443 fungal genomes, 386 genomes possess CAZy annotations and 57 genomes do not possess CAZy annotations as of today (Fig. 3b). The CBRF web-database was developed in the eclipse IDE photon platform using the Spring data JPA, Apache POI and Maven frameworks. The CBRF web database can be specifically used for sorting and searching fungi either by using a specific CAZy group or class or by using a specific plant biomass degrading ability, e.g., cellulose, hemicellulose, pectin, lignin, starch and inulin degrading abilities (Fig. 3a). Thus, obtained list can be easily downloaded in either of the file formats excel (.xls or .csv), PDF and user can also print or copy the results from the CBRF web-database. The CBRF web-database displays additional necessary information including genome code, complete scientific name, cellulose (C), hemicellulose (H), lignin (Li), pectin (Pe), starch (St), inulin (In), search CAZy term (e.g., AA), assembly length (A. Len), gene, total enzymes (#Enz) and published (Pub), respectively (Figs. 4a, b, 5).
The CBRF web-database was developed to identify and compare a specific fungus based on its plant cell wall-degrading abilities. The searching, and sorting functions of CBRF web-database enables users to find fungi both locally and dynamically among the 443 published fungal genomes. We intend to update the CBRF web-database regularly with the release of new published fungal genome sequences in the JGI-MycoCosm database. We have also developed a simple search page for understanding and finding a specific CAZyme and its classification among different CAZy groups and families. The S-CAZymes search page can also be used for finding all the enzymes involved in the biosynthesis and breakdown of a carbohydrate substrate. We also have reported about all the CAZy groups and families which are tentatively involved in synthesis and breakdown of the plant cell wall components. S-CAZymes search page can be used as a primer or preliminary material for understanding the CAZymes distribution and CAZymes required for the degradation and biosynthesis of plant cell wall polysaccharides. Our future works include updating CBRF web-database with the recently published open access fungal genomes by retrieving their genome-wide CAZy annotations. Similarly, we also intend to update the S-CAZymes webpage based on the carbohydrate-active enzymes classification updates of CAZy website.
Availability of data and materials
The data used and described in this paper can be freely accessed by using the CBRF web site at http://220.127.116.11/RankEnzymes/about through the latest versions of Google Chrome, Mozilla Firefox, Microsoft Internet Explorer and Apple Safari. The CBRF source code developed can be provided upon request.
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We sincerely thank Hari Krishna Manupadi, Sai Sudha Anupindi for their valuable suggestions.
This work was supported by Natural Sciences and Engineering Research Council of Canada Funding (RGPIN-2017-05366) to Wensheng Qin and Mitacs Globalink Research Scholarship award to Ayyappa Kumar Sista Kameshwar.
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Kameshwar, A.K.S., Ramos, L.P. & Qin, W. CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities. Bioresour. Bioprocess. 6, 51 (2019). https://doi.org/10.1186/s40643-019-0286-0