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Enzymatic degradation of xyloglucans by Aspergillus species: a comparative view of this genus

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Abstract

Aspergillus species are closely associated with humanity through fermentation, infectious disease, and mycotoxin contamination of food. Members of this genus produce various enzymes to degrade plant polysaccharides, including starch, cellulose, xylan, and xyloglucan. This review focus on the machinery of the xyloglucan degradation using glycoside hydrolases, such as xyloglucanases, isoprimeverose-producing oligoxyloglucan hydrolases, and α-xylosidases, in Aspergillus species. Some xyloglucan degradation-related glycoside hydrolases are well conserved in this genus; however, other enzymes are not. Cooperative actions of these glycoside hydrolases are crucial for xyloglucan degradation in Aspergillus species.

Key points

•Xyloglucan degradation-related enzymes of Aspergillus species are reviewed.

•Each Aspergillus species possesses a different set of glycoside hydrolases.

•The machinery of xyloglucan degradation of A. oryzae is overviewed.

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References

  • Abe K, Gomi K (2008) Food products fermented by Aspergillus oryzae. In: Goldman GH, Osmani SA (eds) The Aspergilli: genomics, medical aspects, biotechnology, and research methods. CRC Press, Boca Raton, pp 429–439

    Google Scholar 

  • Agger JW, Isaksen T, Várnai A, Vidal-Melgosa S, Willats WG, Ludwig R, Horn SJ, Eijsink VG, Westereng B (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A 111:6287–6292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amaike S, Keller NP (2011) Aspergillus flavus. Annu Rev Phytopathol 49:107–133

    Article  CAS  PubMed  Google Scholar 

  • Arnal G, Stogios PJ, Asohan J, Attia MA, Skarina T, Viborg AH, Henrissat B, Savchenko A, Brumer H (2019) Substrate specificity, regiospecificity, and processivity in glycoside hydrolase family 74. J Biol Chem 294:13233–13247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnal G, Stogios PJ, Asohan J, Skarina T, Savchenko A, Brumer H (2018) Structural enzymology reveals the molecular basis of substrate regiospecificity and processivity of an exemplar bacterial glycoside hydrolase family 74 endo-xyloglucanase. Biochem J 475:3963–3978

    Article  CAS  PubMed  Google Scholar 

  • Aspeborg H, Coutinho PM, Wang Y, Brumer H III, Henrissat B (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attia MA, Brumer H (2016) Recent structural insights into the enzymology of the ubiquitous plant cell wall glycan xyloglucan. Curr Opin Struct Biol 40:43–53

    Article  CAS  PubMed  Google Scholar 

  • Augur C, Yu L, Sasaki K, Ogawa T, Sinay P, Darvill AL, Albersheim P (1992) Further studies of the ability of xyloglucan oligosaccharides to inhibit auxin-stimulated growth. Plant Physiol 99:180–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauer S, Vasu P, Mort AJ, Somerville CR (2005) Cloning, expression, and characterization of an oligoxyloglucan reducing end-specific xyloglucanobiohydrolase from Aspergillus nidulans. Carbohydr Res 340:2590–2597

    Article  CAS  PubMed  Google Scholar 

  • Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR (2006) Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci U S A 103:11417–11422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behera BC (2020) Citric acid from Aspergillus niger: a comprehensive overview. Crit Rev Microbiol 46:727–749

    Article  CAS  PubMed  Google Scholar 

  • Bennati-Granier C, Garajova S, Champion C, Grisel S, Haon M, Zhou S, Fanuel M, Ropartz D, Rogniaux H, Gimbert I, Record E, Berrin JG (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8:90

    Article  PubMed  PubMed Central  Google Scholar 

  • Benoit I, Culleton H, Zhou M, DiFalco M, Aguilar-Osorio G, Battaglia E, Bouzid O, Brouwer CPJM, El-Bushari HBO, Coutinho PM, Gruben BS, Hildén KS, Houbraken J, Barboza LAJ, Levasseur A, Majoor E, Mäkelä MR, Narang H-M, Trejo-Aguilar B, Brink J, Kuyk PA, Ad W, McKie V, McCleary B, Tsang A, Henrissat B, Vries RP (2015) Closely related fungi employ diverse enzymatic strategies to degrade plant biomass. Biotechnol Biofuels 8:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernardi AV, de Gouvêa PF, Gerolamo LE, Yonamine DK, de Lourdes de Lima BL, Uyemura SA, Dinamarco TM (2018) Functional characterization of GH7 endo-1,4-β-glucanase from Aspergillus fumigatus and its potential industrial application. Protein Expr Purif 150:1–11

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Sunkara S, Bhatnagar-Panwar M, Waliyar F, Sharma KK (2015) Biotechnological advances for combating Aspergillus flavus and aflatoxin contamination in crops. Plant Sci 234:119–132

    Article  CAS  PubMed  Google Scholar 

  • Brandl J, Andersen MR (2017) Aspergilli: models for systems biology in filamentous fungi. Curr Opin Syst Biol 6:67–73

    Article  Google Scholar 

  • Buckeridge MS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol 154:1017–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlsen M, Nielsen J (2001) Influence of carbon source on α-amylase production by Aspergillus oryzae. Appl Microbiol Biotechnol 57:346–349

    Article  CAS  PubMed  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structure models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Chaillou S, Lokman BC, Leer RJ, Posthuma C, Postma PW, Pouwels PH (1998) Cloning, sequence analysis, and characterization of the genes involved in isoprimeverose metabolism in Lactobacillus pentosus. J Bacteriol 180:2312–2320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Culleton H, McKie V, de Vries RP (2013) Physiological and molecular aspects of degradation of plant polysaccharides by fungi: what have we learned from Aspergillus? Biotechnol J 8:884–894

    Article  CAS  PubMed  Google Scholar 

  • Damásio AR, Ribeiro LF, Ribeiro LF, Furtado GP, Segato F, Almeida FB, Crivellari AC, Backeridge MS, Souza TA, Murakami MT, Ward RJ, Prade RA, Polizeli ML (2012) Functional characterization and oligomerization of a recombinant xyloglucan-specific endo-β-1,4-glucanase (GH12) from Aspergillus niveus. Biochim Biophys Acta 1824:461–467

    Article  PubMed  Google Scholar 

  • Damasio AR, Rubio MV, Gonçalves TA, Persinoti GF, Segato F, Prade RA, Contesini FJ, de Souza AP, Buckeridge MS, Squina FM (2017) Xyloglucan breakdown by endo-xyloglucanase family 74 from Aspergillus fumigatus. Appl Microbiol Biotechnol 101:2893–2903

    Article  CAS  PubMed  Google Scholar 

  • Dragosits M, Pflügl S, Kurz S, Razzazi-Fazeli E, Wilson IB, Rendic D (2014) Recombinant Aspergillus β-galactosidases as a robust glycomic and biotechnological tool. Appl Microbiol Biotechnol 98:3553–3567

    Article  CAS  PubMed  Google Scholar 

  • Frisvad JC, Larsen TO (2015) Chemodiversity in the genus Aspergillus. Appl Microbiol Biotechnol 99:7859–7877

    Article  CAS  PubMed  Google Scholar 

  • Fry SC (1992) Xyloglucan: a metabolically dynamic polysaccharide. Trends Glycosci Glycotechnol 4:279–289

    Article  CAS  Google Scholar 

  • Fry SC, York WS, Albersheim P, Darvill A, Hayashi T, Joseleau J-P, Kato Y, Lorences EP, Maclachlan GA, McNeil M, Mort AJ, Grant Reid JS, Seitz HU, Selvendran RR, Voragen AGJ, White AR (1993) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89:1–3

    Article  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Baştürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115

    Article  CAS  PubMed  Google Scholar 

  • Gloster TM, Ibatullin FM, Macauley K, Eklöf JM, Roberts S, Turkenburg JP, Bjørnvad ME, Jørgensen PL, Danielsen S, Johansen KS, Borchert TV, Wilson KS, Brumer H, Davies GJ (2007) Characterization and three-dimensional structures of two distinct bacterial xyloglucanases from families GH5 and GH12. J Biol Chem 282:19177–19189

    Article  CAS  PubMed  Google Scholar 

  • Gomi K (2019) Regulatory mechanisms for amylolytic gene expression in the koji mold Aspergillus oryzae. Biosci Biotechnol Biochem 83:1385–1401

    Article  CAS  PubMed  Google Scholar 

  • Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I, Shabalov I (2014) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42:D699–D704

    Article  CAS  PubMed  Google Scholar 

  • Grishutin SG, Gusakov AV, Markov AV, Ustinov BB, Semenova MV, Sinitsyn AP (2004) Specific xyloglucanases as a new class of polysaccharide-degrading enzymes. Biochim Biophys Acta 1674:268–281

    Article  CAS  PubMed  Google Scholar 

  • Hamamoto T, Foong F, Shoseyov O, Doi RH (1992) Analysis of functional domains of endoglucanases from Clostridium cellulovorans by gene cloning, nucleotide sequencing and chimeric protein construction. Mol Gen Genet 231:472–479

    Article  CAS  PubMed  Google Scholar 

  • Hasper AA, Dekkers E, van Mil M, van de Vondervoort PJ, de Graaff LH (2002) EglC, a new endoglucanase from Aspergillus niger with major activity towards xyloglucan. Appl Environ Microbiol 68:1556–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Y, Wang B, Chen W, Cox RJ, He J, Chen F (2018) Recent advances in reconstructing microbial secondary metabolites biosynthesis in Aspergillus spp. Biotechnol Adv 36:739–783

    Article  CAS  PubMed  Google Scholar 

  • Hemsworth GR, Thompson AJ, Stepper J, Sobala ŁF, Coyle T, Larsbrink J, Spadiut O, Goddard-Borger ED, Stubbs KA, Brumer H, Davies GJ (2016) Structural dissection of a complex Bacteroides ovatus gene locus conferring xyloglucan metabolism in the human gut. Open Biol 6:160142

    Article  PubMed  PubMed Central  Google Scholar 

  • Henrissat B, Claeyssens M, Tomme P, Lemesle L, Mornon JP (1989) Cellulase families revealed by hydrophobic cluster analysis. Gene 81:83–95

    Article  CAS  PubMed  Google Scholar 

  • Hong SB, Lee M, Kim DH, Varga J, Frisvad JC, Perrone G, Gomi K, Yamada O, Machida M, Houbraken J, Samson RA (2013) Aspergillus luchuensis, an industrially important black Aspergillus in East Asia. PLoS One 8:e63769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichishima E (2016) Development of enzyme technology for Aspergillus oryzae, A. sojae, and A. luchuensis, the national microorganisms of Japan. Biosci Biotechnol Biochem 80:1681–1692

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Sasaki T, Kitamoto K, Kumagai C, Takahashi K, Gomi K, Tamura G (2002) Cloning, nucleotide sequencing, and expression of the β-galactosidase-encoding gene (lacA) from Aspergillus oryzae. J Gen Appl Microbiol 48:135–142

    Article  CAS  PubMed  Google Scholar 

  • Jagadeeswaran G, Gainey L, Prade R, Mort AJ (2016) A family of AA9 lytic polysaccharide monooxygenases in Aspergillus nidulans is differentially regulated by multiple substrates and at least one is active on cellulose and xyloglucan. Appl Microbiol Biotechnol 100:4535–4547

    Article  CAS  PubMed  Google Scholar 

  • Karaffa L, Kubicek CP (2019) Citric acid and itaconic acid accumulation: variations of the same story? Appl Microbiol Biotechnol 103:2889–2902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karkehabadi S, Helmich KE, Kaper T, Hansson H, Mikkelsen NE, Gudmundsson M, Piens K, Fujdala M, Banerjee G, Scott-Craig JS, Walton JD, Phillips GN Jr, Sandgren M (2014) Biochemical characterization and crystal structures of a fungal family 3 β-glucosidase, Cel3A from Hypocrea jecorina. J Biol Chem 289:31624–31637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato Y, Matsushita J, Kubodera T, Matsuda K (1985) A novel enzyme producing isoprimeverose from oligoxyloglucans of Aspergillus oryzae. J Biochem 97:801–810

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita K, Nakamura H (2004) eF-site and PDBjViewer: database and viewer for protein functional sites. Bioinformatics 20:1329–1330

    Article  CAS  PubMed  Google Scholar 

  • Kojima K, Várnai A, Ishida T, Sunagawa N, Petrovic DM, Igarashi K, Jellison J, Goodell B, Alfredsen G, Westereng B, Eijsink VG, Yoshida M (2016) A lytic polysaccharide monooxygenase with broad xyloglucan specificity from the brown-rot fungus Gloeophyllum trabeum and its action on cellulose-xyloglucan complexes. Appl Environ Microbiol 82:6557–6572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kooiman P (1957) Amyloids of seed plants. Nature 179:107–109

    Article  Google Scholar 

  • Larsbrink J, Izumi A, Ibatullin FM, Nakhai A, Gilbert HJ, Davies GJ, Brumer H (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31 α-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem J 436:567–580

    Article  CAS  PubMed  Google Scholar 

  • Larsbrink J, Rogers TE, Hemsworth GR, McKee LS, Tauzin AS, Spadiut O, Klinter S, Pudlo NA, Urs K, Koropatkin NM, Creagh AL, Haynes CA, Kelly AG, Cederholm SN, Davies GJ, Martens EC, Brumer H (2014a) A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroides. Nature 506:498–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsbrink J, Thompson AJ, Lundqvist M, Gardner JG, Davies GJ, Brumer H (2014b) A complex gene locus enables xyloglucan utilization in the model saprophyte Cellvibrio japonicus. Mol Microbiol 94:418–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latgé JP, Chamilos G (2019) Aspergillus fumigatus and aspergillosis in 2019. Clin Microbiol Rev 33:e00140–e00118

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Q, Ray CS, Callow NV, Loman AA, Islam SMM, Ju LK (2020) Aspergillus niger production of pectinase and α-galactosidase for enzymatic soy processing. Enzym Microb Technol 134:109476

    Article  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  CAS  PubMed  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

    Article  PubMed  Google Scholar 

  • Machida M, Yamada O, Gomi K (2008) Genomics of Aspergillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res 15:173–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda H, Sakai D, Kobayashi T, Morita H, Okamoto A, Takeuchi M, Kusumoto K, Amano H, Ishida H, Yamagata Y (2016) Three extracellular dipeptidyl peptidases found in Aspergillus oryzae show varying substrate specificities. Appl Microbiol Biotechnol 100:4947–4958

    Article  CAS  PubMed  Google Scholar 

  • Marui J, Tanaka A, Mimura S, de Graaff LH, Visser J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N (2002) A transcriptional activator, AoXlnR, controls the expression of genes encoding xylanolytic enzymes in Aspergillus oryzae. Fungal Genet Biol 35:157–169

    Article  CAS  PubMed  Google Scholar 

  • Master ER, Zheng Y, Storms R, Tsang A, Powlowski J (2008) A xyloglucan-specific family 12 glycosyl hydrolase from Aspergillus niger: recombinant expression, purification and characterization. Biochem J 411:161–170

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Kameyama A, Yaoi K (2018) A novel isoprimeverose-producing enzyme from Phaeoacremonium minimum is active with low concentrations of xyloglucan oligosaccharides. FEBS Open Bio 9:92–100

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsuzawa T, Kameyama A, Yaoi K (2020a) Identification and characterization of α-xylosidase involved in xyloglucan degradation in Aspergillus oryzae. Appl Microbiol Biotechnol 104:201–210

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Kameyama A, Nakamichi Y, Yaoi K (2020b) Identification and characterization of two xyloglucan-specific endo-1,4-glucanases in Aspergillus oryzae. Appl Microbiol Biotechnol 104:8761–8773

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Kimura N, Suenaga H, Yaoi K (2016a) Screening, identification, and characterization of α-xylosidase from a soil metagenome. J Biosci Bioeng 122:393–399

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Mitsuishi Y, Kameyama A, Yaoi K (2016b) Identification of the gene encoding isoprimeverose-producing oligoxyloglucan hydrolase in Aspergillus oryzae. J Biol Chem 291:5080–5087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuzawa T, Saito Y, Yaoi K (2014) Key amino acid residues for the endo-processive activity of GH74 xyloglucanase. FEBS Lett 588:1731–1738

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Watanabe M, Kameda T, Kameyama A, Yaoi K (2019a) Cooperation between β-galactosidase and an isoprimeverose-producing oligoxyloglucan hydrolase is key for xyloglucan degradation in Aspergillus oryzae. FEBS J 286:3182–3193

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Watanabe M, Nakamichi Y, Fujimoto Z, Yaoi K (2019b) Crystal structure and substrate recognition mechanism of Aspergillus oryzae isoprimeverose-producing enzyme. J Struct Biol 205:84–90

    Article  CAS  PubMed  Google Scholar 

  • Matsuzawa T, Yaoi K (2016) GH74 xyloglucanases: structures and modes of activity. Trends Glycosci Glycotechnol 28:E63–E70

    Article  Google Scholar 

  • Max B, Salgado JM, Rodríguez N, Cortés S, Converti A, Domínguez JM (2010) Biotechnological production of citric acid. Braz J Microbiol 41:862–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDougall GJ, Fry SC (1989) Structure-activity relationship for xyloglucan oligosaccharides with antiauxin activity. Plant Physiol 89:883–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGregor N, Morar M, Fenger TH, Stogios P, Lenfant N, Yin V, Xu X, Evdokimova E, Cui H, Henrissat B, Savchenko A, Brumer H (2016) Structure-function analysis of a mixed-linkage β-glucanase/xyloglucanase from the key ruminal Bacteroidetes Prevotella bryantii B14. J Biol Chem 291:1175–1197

    Article  CAS  PubMed  Google Scholar 

  • Moracci M, Cobucci Ponzano B, Trincone A, Fusco S, De Rose M, van Der Oost J, Sensen CW, Charlebois RL, Rossi M (2000) Identification and molecular characterization of the first α-xylosidase from an archaeon. J Biol Chem 275:22082–22089

    Article  CAS  PubMed  Google Scholar 

  • Nakazawa H, Okada K, Kobayashi R, Kubota T, Onodera T, Ochiai N, Omata N, Ogasawara W, Okada H, Morikawa Y (2008) Characterization of the catalytic domains of Trichoderma reesei endoglucanase I, II, and III, expressed in Escherichia coli. Appl Microbiol Biotechnol 81:681–689

    Article  CAS  PubMed  Google Scholar 

  • Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, García JL, García MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, Gwilliam R, Haas B, Haas H, Harris D, Horiuchi H, Huang J, Humphray S, Jiménez J, Keller N, Khouri H, Kitamoto K, Kobayashi T, Konzack S, Kulkarni R, Kumagai T, Lafon A, Latgé JP, Li W, Lord A, Lu C, Majoros WH, May GS, Miller BL, Mohamoud Y, Molina M, Monod M, Mouyna I, Mulligan S, Murphy L, O'Neil S, Paulsen I, Peñalva MA, Pertea M, Price C, Pritchard BL, Quail MA, Rabbinowitsch E, Rawlins N, Rajandream MA, Reichard U, Renauld H, Robson GD, Rodriguez de Córdoba S, Rodríguez-Peña JM, Ronning CM, Rutter S, Salzberg SL, Sanchez M, Sánchez-Ferrero JC, Saunders D, Seeger K, Squares R, Squares S, Takeuchi M, Tekaia F, Turner G, Vazquez de Aldana CR, Weidman J, White O, Woodward J, Yu JH, Fraser C, Galagan JE, Asai K, Machida M, Hall N, Barrell B, Denning DW (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156

    Article  CAS  PubMed  Google Scholar 

  • Nierman WC, Yu J, Fedorova-Abrams ND, Losada L, Cleveland TE, Bhatnagar D, Bennett JW, Dean R, Payne GA (2015) Genome sequence of Aspergillus flavus NRRL 3357, a strain that causes aflatoxin contamination of food and feed. Genome Announc 3:e00168–e00115

    Article  PubMed  PubMed Central  Google Scholar 

  • Noguchi Y, Sano M, Kanamaru K, Ko T, Takeuchi M, Kato M, Kobayashi T (2009) Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl Microbiol Biotechnol 85:141–154

    Article  CAS  PubMed  Google Scholar 

  • Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194

    Article  CAS  PubMed  Google Scholar 

  • Paulussen C, Hallsworth JE, Álvarez-Pérez S, Nierman WC, Hamill PG, Blain D, Rediers H, Lievens B (2017) Ecology of aspergillosis: insights into the pathogenic potency of Aspergillus fumigatus and some other Aspergillus species. Microb Biotechnol 10:296–322

    Article  PubMed  Google Scholar 

  • Pauly M, Andersen LN, Kauppinen S, Kofod LV, York WS, Albersheim P, Darvill A (1999) A xyloglucan-specific endo-β-1,4-glucanase from Aspergillus aculeatus: expression cloning in yeast, purification and characterization of the recombinant enzyme. Glycobiology 9:93–100

    Article  CAS  PubMed  Google Scholar 

  • Pauly M, Keegstra K (2016) Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol 67:235–259

    Article  CAS  PubMed  Google Scholar 

  • Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d'Enfert C, Geysens S, Goosen C, Groot GS, de Groot PW, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JP, van den Hondel CA, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel MJ, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NN, Ram AF, Rinas U, Roubos JA, Sagt CM, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJ, Wedler H, Wösten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221–231

    Article  PubMed  Google Scholar 

  • Peña-Montes C, González A, Castro-Ochoa D, Farrés A (2008) Purification and biochemical characterization of a broad substrate specificity thermostable alkaline protease from Aspergillus nidulans. Appl Microbiol Biotechnol 78:603–612

    Article  PubMed  Google Scholar 

  • Powlowski J, Mahajan S, Schapira M, Master ER (2009) Substrate recognition and hydrolysis by a fungal xyloglucan-specific family 12 hydrolase. Carbohydr Res 344:1175–1179

    Article  CAS  PubMed  Google Scholar 

  • Rico-Díaz A, Ramírez-Escudero M, Vizoso-Vázquez Á, Cerdán ME, Becerra M, Sanz-Aparicio J (2017) Structural features of Aspergillus niger β-galactosidase define its activity against glycoside linkages. FEBS J 284:1815–1829

    Article  PubMed  Google Scholar 

  • Samarntarn W, Cheevadhanarak S, Tanticharoen M (1999) Production of alkaline protease by a genetically engineered Aspergillus oryzae U1521. J Gen Appl Microbiol 45:99–103

    Article  CAS  PubMed  Google Scholar 

  • Savitha J, Bhargavi SD, Praveen VK (2016) Complete genome sequence of soil fungus Aspergillus terreus (KM017963), a potent lovastatin producer. Genome Announc 4:e00491–e00416

    Article  PubMed  PubMed Central  Google Scholar 

  • Scott-Craig JS, Borrusch MS, Banerjee G, Harvey CM, Walton JD (2011) Biochemical and molecular characterization of secreted α-xylosidase from Aspergillus niger. J Biol Chem 286:42848–42854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segato F, Damásio AR, de Lucas RC, Squina FM, Prade RA (2014) Genomics review of holocellulose deconstruction by aspergilli. Microbiol Mol Biol Rev 78:588–613

  • Tada S, Iimura Y, Gomi K, Takahashi K, Hara S, Yoshizawa K (1989) Cloning and nucleotide sequence of the genomic Taka-amylase A gene of Aspergillus oryzae. Agric Biol Chem 53:593–599

    CAS  Google Scholar 

  • Tuomivaara ST, Yaoi K, O’Neill MA, York WS (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature. Carbohydr Res 402:56–66

    Article  CAS  PubMed  Google Scholar 

  • Vadlapudi V, Borah N, Yellusani KR, Gade S, Reddy P, Rajamanikyam M, Vempati LNS, Gubbala SP, Chopra P, Upadhyayula SM, Amanchy R (2017) Aspergillus secondary metabolite database, a resource to understand the Secondary metabolome of Aspergillus genus. Sci Rep 7:7325

    Article  PubMed  PubMed Central  Google Scholar 

  • Vitcosque GL, Ribeiro LF, de Lucas RC, da Silva TM, Ribeiro LF, de Lima Damasio AR, Farinas CS, Gonçalves AZ, Segato F, Buckeridge MS, Jorge JA, Polizeli ML (2016) The functional properties of a xyloglucanase (GH12) of Aspergillus terreus expressed in Aspergillus nidulans may increase performance of biomass degradation. Appl Microbiol Biotechnol 100:9133–9144

    Article  CAS  PubMed  Google Scholar 

  • Wu M, McNulty NP, Rodionov DA, Khoroshkin MS, Griffin NW, Cheng J, Latreille P, Kerstetter RA, Terrapon N, Henrissat B, Osterman AL, Gordon J (2015) Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350:aac5992

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamada O, Machida M, Hosoyama A, Goto M, Takahashi T, Futagami T, Yamagata Y, Takeuchi M, Kobayashi T, Koike H, Abe K, Asai K, Arita M, Fujita N, Fukuda K, Higa K, Horikawa H, Ishikawa T, Jinno K, Kato Y, Kirimura K, Mizutani O, Nakasone K, Sano M, Shiraishi Y, Tsukahara M, Gomi K (2016) Genome sequence of Aspergillus luchuensis NBRC4314. DNA Res 23:507–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaoi K, Mitsuishi Y (2002) Purification, characterization, cloning, and expression of a novel xyloglucan-specific glycosidase, oligoxyloglucan reducing end-specific cellobiohydrolase. J Biol Chem 277:48276–48281

    Article  CAS  PubMed  Google Scholar 

  • Yaoi K, Mitsuishi Y (2004) Purification, characterization, cDNA cloning, and expression of a xyloglucan endoglucanase from Geotrichum sp. M128. FEBS Lett 560:45–50

    Article  CAS  PubMed  Google Scholar 

  • Yaoi K, Nakai T, Kameda Y, Hiyoshi A, Mitsuishi Y (2005) Cloning and characterization of two xyloglucanases from Paenibacillus sp. strain KM21. Appl Environ Microbiol 71:7670–7678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaoi K, Hiyoshi A, Mitsuishi Y (2007a) Screening, purification and characterization of a prokaryotic isoprimeverose-producing oligoxyloglucan hydrolase from Oerskovia sp. Y1. J Appl Glycosci 54:91–94

    Article  CAS  Google Scholar 

  • Yaoi K, Kondo H, Noro N, Suzuki M, Tsuda S, Mitsuishi Y (2004) Tandem repeat of a seven-bladed β-propeller domain in oligoxyloglucan reducing-end-specific cellobiohydrolase. Structure 12:1209–1217

    Article  CAS  PubMed  Google Scholar 

  • Yaoi K, Kondo H, Hiyoshi A, Noro N, Sugimoto H, Tsuda S, Mitsuishi Y, Miyazaki K (2007b) The structural basis for the exo-mode of action in GH74 oligoxyloglucan reducing end-specific cellobiohydrolase. J Mol Biol 370:53–62

    Article  CAS  PubMed  Google Scholar 

  • Yaoi K, Miyazaki K (2012) Cloning and expression of isoprimeverose-producing oligoxyloglucan hydrolase from actinomycetes species, Oerskovia sp. Y1. (2012). J Appl Glycosci 59:83–88

    Article  CAS  Google Scholar 

  • York WS, Oates JE, van Halbeek H, Darvill AG, Albersheim P, Tiller PR, Dell A (1988) Location of the O-acetyl substituents on a nonasaccharide repeating unit of sycamore extracellular xyloglucan. Carbohydr Res 173:113–132

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa K, Yamamoto K, Okada S (1994) Classification of some α-glucosidases and α-xylosidases on the basis of substrate specificity. Biosci Biotechnol Biochem 58:1392–1398

    Article  CAS  PubMed  Google Scholar 

  • Zabotina OA (2012) Xyloglucan and its biosynthesis. Front Plant Sci 3:134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Wang X, Chen Y, Wagner E, Cosgrove DJ (2018) Xyloglucan in the primary cell wall: assessment by FESEM, selective enzyme digestions and nanogold affinity tags. Plant J 93:211–226

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was supported by the Japan Society for the Promotion of Science KAKENHI (Grant-in-Aid for Scientific Research B, Grant No. 18H02132).

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Authors and Affiliations

  1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki, 305-8566, Japan

    Tomohiko Matsuzawa & Katsuro Yaoi

  2. Department of Bioindustrial Informatics and Genomics, Graduate School of Agricultural Science, Tohoku University, 468-1 Aoba, Aramaki, Aoba-ku, Sendai, 980-8572, Japan

    Akira Watanabe, Takahiro Shintani & Katsuya Gomi

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  1. Tomohiko Matsuzawa
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  2. Akira Watanabe
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  3. Takahiro Shintani
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TM conceived the manuscript topics and designed the structure of this review. TM, AW, TS, and KG wrote the manuscript. KY helped in manuscript editing. All authors read and approved the manuscript.

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Correspondence to Tomohiko Matsuzawa.

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Matsuzawa, T., Watanabe, A., Shintani, T. et al. Enzymatic degradation of xyloglucans by Aspergillus species: a comparative view of this genus. Appl Microbiol Biotechnol 105, 2701–2711 (2021). https://doi.org/10.1007/s00253-021-11236-8

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