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Comparative Genomics of the White-Rot Fungi, Phanerochaete Carnosa and P

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Comparative Genomics of the White-Rot Fungi, Phanerochaete Carnosa and P Suzuki et al. BMC Genomics 2012, 13:444 http://www.biomedcentral.com/1471-2164/13/444 RESEARCH ARTICLE Open Access Comparative genomics of the white-rot fungi, Phanerochaete carnosa and P. chrysosporium,to elucidate the genetic basis of the distinct wood types they colonize Hitoshi Suzuki1, Jacqueline MacDonald1, Khajamohiddin Syed2, Asaf Salamov3, Chiaki Hori5, Andrea Aerts3, Bernard Henrissat4, Ad Wiebenga8, Patricia A vanKuyk8, Kerrie Barry3, Erika Lindquist3, Kurt LaButti3, Alla Lapidus3, Susan Lucas3, Pedro Coutinho4, Yunchen Gong7, Masahiro Samejima5, Radhakrishnan Mahadevan1, Mamdouh Abou-Zaid6, Ronald P de Vries8, Kiyohiko Igarashi5, Jagjit S Yadav2, Igor V Grigoriev3 and Emma R Master1* Abstract Background: Softwood is the predominant form of land plant biomass in the Northern hemisphere, and is among the most recalcitrant biomass resources to bioprocess technologies. The white rot fungus, Phanerochaete carnosa, has been isolated almost exclusively from softwoods, while most other known white-rot species, including Phanerochaete chrysosporium, were mainly isolated from hardwoods. Accordingly, it is anticipated that P. carnosa encodes a distinct set of enzymes and proteins that promote softwood decomposition. To elucidate the genetic basis of softwood bioconversion by a white-rot fungus, the present study reports the P. carnosa genome sequence and its comparative analysis with the previously reported P. chrysosporium genome. Results: P. carnosa encodes a complete set of lignocellulose-active enzymes. Comparative genomic analysis revealed that P. carnosa is enriched with genes encoding manganese peroxidase, and that the most divergent glycoside hydrolase families were predicted to encode hemicellulases and glycoprotein degrading enzymes. Most remarkably, P. carnosa possesses one of the largest P450 contingents (266 P450s) among the sequenced and annotated wood-rotting basidiomycetes, nearly double that of P. chrysosporium. Along with metabolic pathway modeling, comparative growth studies on model compounds and chemical analyses of decomposed wood components showed greater tolerance of P. carnosa to various substrates including coniferous heartwood. Conclusions: The P. carnosa genome is enriched with genes that encode P450 monooxygenases that can participate in extractives degradation, and manganese peroxidases involved in lignin degradation. The significant expansion of P450s in P. carnosa, along with differences in carbohydrate- and lignin-degrading enzymes, could be correlated to the utilization of heartwood and sapwood preparations from both coniferous and hardwood species. Keywords: Phanerochaete carnosa, Comparative genomics, Phanerochaete chrysosporium, Softwood degradation * Correspondence: [email protected] 1Department of Chemical Engineering & Applied Chemistry, University of Toronto, 200 College Street, Toronto, ON M5S 3E5, Canada Full list of author information is available at the end of the article © 2012 Suzuki et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Suzuki et al. BMC Genomics 2012, 13:444 Page 2 of 17 http://www.biomedcentral.com/1471-2164/13/444 Background analysis of closely related lignocellulose-degrading fungi The lignocellulose fraction of plant cell walls is the most having different substrate preferences. For instance, abundant renewable carbon source on earth, and is a key genomic comparison of P. chrysosporium and the resource for substituting petroleum in the production of softwood-degrading, model brown-rot fungus, Postia energy, chemicals and materials. Among the various types placenta, revealed that brown-rot is characterized by the of lignocellulosic biomasses, softwood is the predominant contraction of multiple gene families, including cellobio- form of land plant biomass in the Northern hemisphere hydrolases and cellulose-binding domains [12]. Moreover, [1]. Softwood (coniferous) and hardwood (deciduous) fiber comparative analysis of Aspergillus genomes identified cor- mainly differ in the structure and composition of hemicel- relations between genome content, plant polysaccharide lulose and lignin components. For instance, glucuronoxy- degradation, and respective biotope [13]. Given the appar- lan comprises approximately 20–30% of the secondary cell ent differences in substrate preference of P. carnosa and wall polysaccharides in hardwood, while galactoglucoman- P. chrysosporium, and their phylogenetic similarity based nan is the main hemicellulose in secondary cell walls of on internal transcribed spacer (ITS) region sequences [14], softwood. Moreover, softwoods contain mainly guaiacyl it is anticipated that comparative analysis of P. carnosa and lignin, whereas hardwoods contain varying ratios of syrin- P. chrysosporium genomes could reveal enzymes and meta- gyl and guaiacyl lignins [2]. The recalcitrance of softwood bolic pathways that are key to efficient biotransformation of lignocellulose to bioprocess technologies has been attribu- recalcitrant softwood feedstocks. Accordingly, the present ted to its higher lignin content, smaller pore size, and studyreportsthefirstanalysisoftheP. carnosa draft gen- fewer hemicellulose-derived acetyl groups in comparison ome, and compares P. carnosa and P. chrysosporium with hardwood [3]. in terms of genome composition and organization, as Although relatively few organisms are known to effect- well as growth on model and woody substrates. These ively utilize all components of lignocellulose, white-rot analyses revealed significant expansion of P450 genes basidiomycetes transform cellulose, hemicellulose and in P. carnosa compared to P. chrysosporium, and high- lignin, and so are regarded as essential contributors to lighted several differences in carbohydrate active enzymes global carbon cycling [4]. While most known white-rot and lignin-degrading enzymes, which may facilitate soft- species, including the model fungus Phanerochaete chry- wood utilization by P. carnosa. sosporium [5,6], have been mainly isolated from hard- woods, the white-rot basidiomycete, Phanerochaete Results and discussion carnosa, has been isolated almost exclusively from soft- Assembly and overview of the P. carnosa genome woods, including Abies balsamea (balsam fir), Abies con- The net length of the P. carnosa genome sequence was color (white fir), and Pinus ponderosa (ponderosa pine) 46.3 Mb, and while distributed over 1137 scaffolds, the [7]. Previous studies have revealed differences in gene six largest scaffolds contained half of the total sequence expression between P. carnosa and P. chrysosporium, and 57% of the 13,937 predicted genes (Additional file 1: suggesting that P. carnosa may possess an enzyme com- Table S1, Table S2, Table S3). A summary of functional plement that is efficient for softwood bioconversion. For annotations by several classifications is shown in example, proteomic characterization of P. carnosa secre- Additional file 1: Table S4. Of these genes, those pre- tomes showed that P. carnosa produces a glycoside dicted to encode P450 monooxygenases, MFS transpor- hydrolase (GH) family 2 mannanase, a multicopper oxi- ters, and signaling proteins (e.g. WD40 and protein dase, and glycopeptides that likely participate in carbo- kinases), comprised the largest families based on PFAM hydrate and lignin degradation [8], which were not domains of translated sequences, and were expanded previously identified in proteomic analysis of P. chrysos- relative to other Basidiomycetes (Additional file 1: Table porium [6,9]. More recent transcriptomic analyses evalu- S5). Notably, the P. carnosa genome has 503 tandem ated gene expression in P. carnosa grown on various gene duplication regions containing a total of 1660 softwood species (white spruce, lodgepole pine, and bal- genes, significantly higher numbers than the P. chrysos- sam fir), as well as a hardwood (sugar maple). Notably, porium genome, which contains 305 duplication regions transcripts predicted to encode lignin-degrading activ- with 865 genes. Indeed, most of the top 50 PFAM ities (particularly manganese peroxidases) were more domains are expanded in P. carnosa relative to P. chry- abundant than those predicted to encode carbohydrate- sosporium (Additional file 1: Table S5) and these are active enzymes [10], which is in contrast to earlier stud- largely responsible for the differences in gene count and ies of P. chrysosporium grown on wood that revealed genome size between the two organisms. comparatively high levels of transcripts encoding A synteny display based on orthologous proteins in carbohydrate-active enzymes [11]. P. carnosa and P. chrysosporium revealed significant Key requirements for the biotransformation of particular rearrangement in the evolutionary history of these biomass resources could be elucidated through comparative two Phanerochaete genomes (Figure 1). Most of the Suzuki et al. BMC Genomics 2012, 13:444 Page 3 of 17 http://www.biomedcentral.com/1471-2164/13/444 Figure 1 Syntenic regions of the 10 largest scaffolds of P. carnosa with scaffolds of P. chrysosporium. Scaffolds are shown as vertical bars, sequence starting from bottom to top, where the length of scaffolds is proportional to sequence length (largest: scaffold_1; smallest: scaffolds 9 and 10). Colors on the scaffolds refer to positions of genes
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