Biotechnology for Biofuels | |
Closely related fungi employ diverse enzymatic strategies to degrade plant biomass | |
Isabelle Benoit9  Helena Culleton7  Miaomiao Zhou5  Marcos DiFalco8  Guillermo Aguilar-Osorio1  Evy Battaglia9  Ourdia Bouzid9  Carlo P J M Brouwer5  Hala B O El-Bushari9  Pedro M Coutinho3  Birgit S Gruben9  Kristiina S Hildén4  Jos Houbraken5  Luis Alexis Jiménez Barboza4  Anthony Levasseur6  Eline Majoor5  Miia R Mäkelä4  Hari-Mander Narang5  Blanca Trejo-Aguilar9  Joost van den Brink5  Patricia A vanKuyk5  Ad Wiebenga5  Vincent McKie7  Barry McCleary7  Adrian Tsang8  Bernard Henrissat2  Ronald P de Vries9  | |
[1] Department of Food Science and Biotechnology, Faculty of Chemistry, National University of México, UNAM, Cd. Universitaria, Mexico, C.P. 04510, DF, Mexico | |
[2] Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, Marseille, 13288, France | |
[3] CNRS, UMR7257, Aix-Marseille University, Marseille, 13288, France | |
[4] Division of Microbiology and Biotechnology, Department of Food and Environmental Sciences, Viikki Biocenter 1, University of Helsinki, Helsinki, Finland | |
[5] Fungal Physiology, CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, Utrecht, 3584 CT, The Netherlands | |
[6] INRA, UMR1163 de Biotechnologie des Champignons Filamenteux, ESIL, Marseille, France | |
[7] Megazyme International Ireland, IDA Business Park, Bray, Wicklow, Ireland | |
[8] Centre for Structural and Functional Genomics, Concordia University, 7141 Sherbrooke Street West, Montreal H4B 1R6, QC, Canada | |
[9] Microbiology and Kluyver Centre for Genomics of Industrial Fermentation, Utrecht University, Padualaan 8, Utrecht, 3584 CH, The Netherlands | |
关键词: Plant biomass degradation; Diversity; Saccharification; Biofuel; Polysaccharides; Enzyme production; Aspergillus; | |
Others : 1225780 DOI : 10.1186/s13068-015-0285-0 |
|
received in 2015-04-07, accepted in 2015-07-09, 发布年份 2015 | |
【 摘 要 】
Background
Plant biomass is the major substrate for the production of biofuels and biochemicals, as well as food, textiles and other products. It is also the major carbon source for many fungi and enzymes of these fungi are essential for the depolymerization of plant polysaccharides in industrial processes. This is a highly complex process that involves a large number of extracellular enzymes as well as non-hydrolytic proteins, whose production in fungi is controlled by a set of transcriptional regulators. Aspergillus species form one of the best studied fungal genera in this field, and several species are used for the production of commercial enzyme cocktails.
Results
It is often assumed that related fungi use similar enzymatic approaches to degrade plant polysaccharides. In this study we have compared the genomic content and the enzymes produced by eight Aspergilli for the degradation of plant biomass. All tested Aspergilli have a similar genomic potential to degrade plant biomass, with the exception of A. clavatus that has a strongly reduced pectinolytic ability. Despite this similar genomic potential their approaches to degrade plant biomass differ markedly in the overall activities as well as the specific enzymes they employ. While many of the genes have orthologs in (nearly) all tested species, only very few of the corresponding enzymes are produced by all species during growth on wheat bran or sugar beet pulp. In addition, significant differences were observed between the enzyme sets produced on these feedstocks, largely correlating with their polysaccharide composition.
Conclusions
These data demonstrate that Aspergillus species and possibly also other related fungi employ significantly different approaches to degrade plant biomass. This makes sense from an ecological perspective where mixed populations of fungi together degrade plant biomass. The results of this study indicate that combining the approaches from different species could result in improved enzyme mixtures for industrial applications, in particular saccharification of plant biomass for biofuel production. Such an approach may result in a much better improvement of saccharification efficiency than adding specific enzymes to the mixture of a single fungus, which is currently the most common approach used in biotechnology.
【 授权许可】
2015 Benoit et al.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150922002539976.pdf | 5268KB | download | |
Fig.4. | 210KB | Image | download |
Fig.3. | 174KB | Image | download |
Fig.2. | 87KB | Image | download |
Fig.1. | 55KB | Image | download |
【 图 表 】
Fig.1.
Fig.2.
Fig.3.
Fig.4.
【 参考文献 】
- [1]de Vries RP, Nayak V, van den Brink J, Vivas Duarte AD, Stalbrand H: Fungal degradation of plant oligo- and polysaccharides. In Carbohydrate modifying biocatalysts. Edited by Grunwald P. Pan Stanford Publishing Pte Ltd., Singapore; 2012:693-759.
- [2]de Vries RP, Visser J: Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microb Mol Biol Rev 2001, 65:497-522.
- [3]Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, Couloux A, et al.: Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 2011, 7:e1002230.
- [4]Battaglia E, Benoit I, van den Brink J, Wiebenga A, Coutinho PM, Henrissat B, et al.: Carbohydrate-active enzymes from the zygomycete fungus Rhizopus oryzae: a highly specialized approach to carbohydrate degradation depicted at genome level. BMC Genom 2011, 12:38. BioMed Central Full Text
- [5]Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, et al.: Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 2011, 29:922-927.
- [6]Coutinho PM, Andersen MR, Kolenova K, vanKuyk PA, Benoit I, Gruben BS, et al.: Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fungal Genet Biol 2009, 46(Suppl 1):S161-S169.
- [7]Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, et al.: The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 2011, 333:762-765.
- [8]Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, et al.: The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 2008, 9:R77. BioMed Central Full Text
- [9]Aro N, Pakula T, Penttila M: Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 2005, 29:719-739.
- [10]Baldrian P, Valaskova V: Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 2008, 32:501-521.
- [11]Kowalczyk JE, Benoit I, de Vries RP: Regulation of plant biomass utilization in Aspergillus. Adv Appl Microbiol 2014, 88:31-56.
- [12]Kubicek CP, Starr TL, Glass NL: Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Ann Rev Phytopathol. 2014, 52:427-451.
- [13]MacDonald J, Suzuki H, Master ER: Expression and regulation of genes encoding lignocellulose-degrading activity in the genus Phanerochaete. Appl Microbiol Biotechnol 2012, 94:339-351.
- [14]Stricker AR, Mach RL, de Graaff LH: Regulation of transcription of cellulases- and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei). Appl Microbiol Biotechnol 2008, 78:211-220.
- [15]Tani S, Kawaguchi T, Kobayashi T: Complex regulation of hydrolytic enzyme genes for cellulosic biomass degradation in filamentous fungi. Appl Microbiol Biotechnol 2014, 98:4829-4837.
- [16]Todd RB, Zhou M, Ohm RA, Leeggangers HA, Visser L, de Vries RP: Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genom 2014, 15:214. BioMed Central Full Text
- [17]Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B: The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014, 42:D490-D495.
- [18]Battaglia E, Visser L, Nijssen A, van Veluw J, Wösten HAB, de Vries RP: Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in the Eurotiales. Stud Mycol 2011, 69:31-38.
- [19]de Vries RP, Visser J, de Graaff LH: CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res Microbiol 1999, 150:281-285.
- [20]Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, et al.: Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 2012, 8:e1002875.
- [21]Hasper AA, Trindade LM, van der Veen D, van Ooyen AJ, de Graaff LH: Functional analysis of the transcriptional activator XlnR from Aspergillus niger. Microbiology 2004, 150:1367-1375.
- [22]Marui J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N: Transcriptional activator, AoXlnR, mediates cellulose-inductive expression of the xylanolytic and cellulolytic genes in Aspergillus oryzae. FEBS Lett 2002, 528:279-282.
- [23]Marui J, Tanaka A, Mimura S, de Graaff LH, Visser J, Kitamoto N, et al.: A transcriptional activator, AoXlnR, controls the expression of genes encoding xylanolytic enzymes in Aspergillus oryzae. Fungal Genet Biol 2002, 35:157-169.
- [24]Noguchi Y, Sano M, Kanamaru K, Ko T, Takeuchi M, Kato M, et al.: Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl Microbiol Biotechnol 2009, 85:141-154.
- [25]Noguchi Y, Tanaka H, Kanamaru K, Kato M, Kobayashi T: Xylose triggers reversible phosphorylation of XlnR, the fungal transcriptional activator of xylanolytic and cellulolytic genes in Aspergillus oryzae. Biosci Biotechnol Biochem 2011, 75:953-959.
- [26]Tamayo EN, Villanueva A, Hasper AA, de Graaff LH, Ramon D, Orejas M: CreA mediates repression of the regulatory gene xlnR which controls the production of xylanolytic enzymes in Aspergillus nidulans. Fungal Genet Biol 2008, 45:984-993.
- [27]van Peij N, Gielkens MMC, de Vries RP, Visser J, de Graaff LH: The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 1998, 64:3615-3619.
- [28]van Peij NN, Visser J, de Graaff LH: Isolation and analysis of xlnR, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 1998, 27:131-142.
- [29]Bakri Y, Masson M, Thonart P: Isolation and identification of two new fungal strains for xylanase production. Appl Biochem Biotechnol 2010, 162:1626-1634.
- [30]de Souza CG, Girardo NS, Costa MA, Peralta RM: Influence of growth conditions on the production of xylanolytic enzymes by Aspergillus flavus. J Basic Microbiol 1999, 39:155-160.
- [31]Elshafei AM, Hassan MM, Haroun BM, Abdel-Fatah OM, Atta HM, Othman AM: Purification and properties of an endoglucanase of Aspergillus terreus DSM 826. J Basic Microbiol 2009, 49:426-432.
- [32]Gawande PV, Kamat MY: Production of Aspergillus xylanase by lignocellulosic waste fermentation and its application. J Appl Microbiol 1999, 87:511-519.
- [33]Mellon JE, Cotty PJ, Callicott KA, Abbas H: Identification of a major xylanase from Aspergillus flavus as a 14-kD protein. Mycopathologia 2011, 172:299-305.
- [34]Peixoto-Nogueira Sde C, Michelin M, Betini JH, Jorge JA, Terenzi HF, Polizeli Mde L: Production of xylanase by Aspergilli using alternative carbon sources: application of the crude extract on cellulose pulp biobleaching. J Ind Microbiol Biotechnol 2009, 36:149-155.
- [35]Tani S, Kanamasa S, Sumitani J-I, Arai M, Kawaguchi T (2012) XlnR-independent signaling pathway regulates both cellulase and xylanase genes in response to cellobiose in Aspergillus aculeatus. Curr Genet 58:93–104
- [36]Klaubauf S, Narang HM, Post H, Zhou M, Brunner K, Mach-Aigner AR, et al.: Similar is not the same: Differences in the function of the (hemi-)cellulolytic regulator XlnR (Xlr1/Xyr1) in filamentous fungi. Fungal Genet Biol 2014, 72:73-81.
- [37]Kunitake E, Tani S, Sumitani J, Kawaguchi T: A novel transcriptional regulator, ClbR, controls the cellobiose- and cellulose-responsive induction of cellulase and xylanase genes regulated by two distinct signaling pathways in Aspergillus aculeatus. Appl Microbiol Biotechnol 2013, 97:2017-2028.
- [38]de Vries RP, Jansen J, Aguilar G, Parenicová L, Benen JAE, Joosten V, et al.: Expression profiling of pectinolytic genes from Aspergillus niger. FEBS Lett 2002, 530:41-47.
- [39]Gruben BS, Zhou M, Wiebenga A, Ballering J, Overkamp KM, Punt PJ, et al.: Aspergillus niger RhaR, a regulator involved in L-rhamnose release and catabolism. Appl Microbiol Biotechnol 2014, 98:5531-5540.
- [40]Martens-Uzunova ES, Schaap PJ: Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet Biol 2009, 46(Suppl 1):S170-S179.
- [41]Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, et al.: Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 2007, 25:221-231.
- [42]Murphy C, Powlowski J, Wu M, Butler G, Tsang A: Curation of characterized glycoside hydrolases of fungal origin. Database J Biol Databases Curation 2011, 2011:bar020.
- [43]Battaglia E, Hansen SF, Leendertse A, Madrid S, Mulder H, Nikolaev I, et al.: Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger. Appl Microbiol Biotechnol 2011, 91:387-397.
- [44]Makita T, Katsuyama Y, Tani S, Suzuki H, Kato N, Todd RB, et al.: Inducer-dependent nuclear localization of a Zn(II)(2)Cys(6) transcriptional activator, AmyR, in Aspergillus nidulans. Biosci Biotechnol Biochem 2009, 73:391-399.
- [45]Murakoshi Y, Makita T, Kato M, Kobayashi T: Comparison and characterization of alpha-amylase inducers in Aspergillus nidulans based on nuclear localization of AmyR. Appl Microbiol Biotechnol 2012, 94:1629-1635.
- [46]Suzuki K, Tanaka M, Konno Y, Ichikawa T, Ichinose S, Hasegawa-Shiro S, et al.: Distinct mechanism of activation of two transcription factors, AmyR and MalR, involved in amylolytic enzyme production in Aspergillus oryzae. Appl Microbiol Biotechnol 2015, 99:1805-1815.
- [47]Vankuyk PA, Benen JA, Wosten HA, Visser J, de Vries RP: A broader role for AmyR in Aspergillus niger: regulation of the utilisation of D-glucose or D-galactose containing oligo- and polysaccharides. Appl Microbiol Biotechnol 2012, 93:285-293.
- [48]Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V: Induction and transcriptional regulation of laccases in fungi. Curr Genomics 2011, 12:104-112.
- [49]Levasseur A, Saloheimo M, Navarro D, Andberg M, Pontarotti P, Kruus K, et al.: Exploring laccase-like multicopper oxidase genes from the ascomycete Trichoderma reesei: a functional, phylogenetic and evolutionary study. BMC Biochem 2010, 11:32. BioMed Central Full Text
- [50]Tsai HF, Wheeler MH, Chang YC, Kwon-Chung KJ: A developmentally regulated gene cluster involved in conidial pigment biosynthesis in Aspergillus fumigatus. J Bacteriol 1999, 181:6469-6477.
- [51]Couturier M, Haon M, Coutinho PM, Henrissat B, Lesage-Meessen L, Berrin JG: Podospora anserina hemicellulases potentiate the Trichoderma reesei secretome for saccharification of lignocellulosic biomass. Appl Environ Microbiol 2010, 77:237-246.
- [52]de Vries RP, Burgers K, van de Vondervoort PJI, Frisvad JC, Samson RA, Visser J: A new black Aspergillus species, A. vadensis, is a promising host for homologous and heterologous protein production. Appl Environ Microbiol. 2004, 70:3954-3959.
- [53]Kuhnel S, Schols HA, Gruppen H: Aiming for the complete utilization of sugar-beet pulp: examination of the effects of mild acid and hydrothermal pretreatment followed by enzymatic digestion. Biotechnol Biofuels 2011, 4:14. BioMed Central Full Text
- [54]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al.: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
- [55]Eddy SR: Profile hidden Markov models. Bioinformatics 1998, 14:755-763.
- [56]Li L, Stoeckert CJ Jr, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189.
- [57]Boekhorst J, Snel B: Identification of homologs in insignificant blast hits by exploiting extrinsic gene properties. BMC Bioinform 2007, 8:356. BioMed Central Full Text
- [58]Crabtree J, Angiuoli SV, Wortman JR, White OR: Sybil: methods and software for multiple genome comparison and visualization. Methods Mol Biol 2007, 408:93-108.
- [59]Katoh K, Kuma K-I, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33:511-518.
- [60]Ozturkoglu Budak S, Zhou M, Brouwer C, Wiebenga A, Benoit I, Di Falco M, et al.: A genomic survey of proteases in Aspergilli. BMC Genomics 2014, 15:523. BioMed Central Full Text
- [61]Team RDC: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna; 2009.
- [62]Letunic I, Bork P: Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23:127-128.
- [63]Letunic I, Bork P: Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 2011, 39:W475-W478.
- [64]Sturn A, Quackenbush J, Trajanoski Z: Genesis: cluster analysis of microarray data. Bioinformatics 2002, 18:207-208.
- [65]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
- [66]Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 2008, 57:758-771.