Chitinases CtcB and CfcI modify the cell wall in sporulating aerial mycelium of Aspergillus niger

Microbiology (United Kingdom)

Volumn 159, Issue PART 9, 2013, Pages 1853-1867

  van Munster, Jolanda M ^a,e   Nitsche, Benjamin M ^b,f   Krijgsheld, Pauline ^c   van Wijk, Alle ^d   Dijkhuizen, Lubbert ^a   Wösten, Han A ^c   Ram, Arthur F ^b   van der Maarel, Marc J E C ^a,d  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; CHITINASE; OLIGOSACCHARIDE; TRANSCRIPTOME;

ARTICLE; ASPERGILLUS NIGER; CARBOHYDRATE ANALYSIS; CELL ADHESION; CONIDIUM; FUNGAL CELL WALL; FUNGUS GROWTH; FUNGUS HYPHAE; GERMINATION; GROWTH RATE; MYCELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; SPOROGENESIS;

EID: 84883317856     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.067967-0     Document Type: Article

References (81)

1. Adams, T. H., Wieser, J. K. & Yu, J. H. (1998). Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62, 35-54.
2. Aguilar-Osorio, G., Vankuyk, P. A., Seiboth, B., Blom, D., Solomon, P. S., Vinck, A., Kindt, F., Wösten, H. A. & de Vries, R. P. (2010). Spatial and developmental differentiation of mannitol dehydrogenase and mannitol-1-phosphate dehydrogenase in Aspergillus niger. Eukaryot Cell 9, 1398-1402.
3. Alcazar-Fuoli, L., Clavaud, C., Lamarre, C., Aimanianda, V., Seidl-Seiboth, V., Mellado, E. & Latgé, J. P. (2011). Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol 48, 418-429.
4. Alic, M. & Bennett, J. W. & Lasure, L. L. (1991). More Gene Manipulations in Fungi. San Diego, CA: Academic Press.
5. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
6. Arentshorst, M., Ram, A. F. & Meyer, V. (2012). Using nonhomologous end-joining-deficient strains for functional gene analyses in filamentous fungi. Methods Mol Biol 835, 133-150.
7. Arnaud, M. B., Chibucos, M. C., Costanzo, M. C., Crabtree, J., Inglis, D. O., Lotia, A., Orvis, J., Shah, P., Skrzypek, M. S. & other authors (2010). The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 38 (Database issue), D420-D427.
8. Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K. H. & other authors (2011). NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 39 (Database issue), D1005-D1010.
9. Bauer, S., Vasu, P., Persson, S., Mort, A. J. & Somerville, C. R. (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.
10. Bleichrodt, R., Vinck, A., Krijgsheld, P., van Leeuwen, M. R., Dijksterhuis, J. & Wösten, H. A. B. (2013). Cytosolic streaming in vegetative mycelium and aerial structures of Aspergillus niger. Stud Mycol 74, 31-46.
11. Bolwerk, A., Lagopodi, A. L., Lugtenberg, B. J. & Bloemberg, G. V. (2005). Visualization of interactions between a pathogenic and a beneficial Fusarium strain during biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 18, 710-721.
12. Bos, C. J., Debets, A. J., Swart, K., Huybers, A., Kobus, G. & Slakhorst, S. M. (1988). Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger. Curr Genet 14, 437-443.
13. Braaksma, M., Martens-Uzunova, E. S., Punt, P. J. & Schaap, P. J. (2010). An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC Genomics 11, 584.
14. Cabib, E. (2009). Two novel techniques for determination of polysaccharide cross-links show that Crh1p and Crh2p attach chitin to both b(1-6)-and b(1-3)glucan in the Saccharomyces cerevisiae cell wall. Eukaryot Cell 8, 1626-1636.
15. Cabib, E., Farkas, V., Kosík, O., Blanco, N., Arroyo, J. & McPhie, P. (2008). Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro. J Biol Chem 283, 29859-29872.
16. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V. & Henrissat, B. (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37 (Database issue), D233-D238.
17. de Groot, P. W., Hellingwerf, K. J. & Klis, F. M. (2003). Genome-wide identification of fungal GPI proteins. Yeast 20, 781-796.
18. Delmas, S., Pullan, S. T., Gaddipati, S., Kokolski, M., Malla, S., Blythe, M. J., Ibbett, R., Campbell, M., Liddell, S. & other authors (2012). Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8, e1002875.
19. Eisenhaber, B., Schneider, G., Wildpaner, M. & Eisenhaber, F. (2004). A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol 337, 243-253.
20. Erdei, E., Pusztahelyi, T., Miskei, M., Barna, T. & Pócsi, I. (2008). Characterization and heterologous expression of an age-dependent fungal/bacterial type chitinase of Aspergillus nidulans. Acta Microbiol Immunol Hung 55, 351-361.
21. Etxebeste, O., Garzia, A., Espeso, E. A. & Ugalde, U. (2010). Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol 18, 569-576.
22. Foreman, P. K., Brown, D., Dankmeyer, L., Dean, R., Diener, S., Dunn-Coleman, N. S., Goedegebuur, F., Houfek, T. D., England, G. J. & other authors (2003). Transcriptional regulation of biomassdegrading enzymes in the filamentous fungus Trichoderma reesei. J Biol Chem 278, 31988-31997.
23. François, J. M. (2007). A simple method for quantitative determination of polysaccharides in fungal cell walls. Nat Protoc 1, 2995-3000.
24. Fujiwara, M., Ichinomiya, M., Motoyama, T., Horiuchi, H., Ohta, A. & Takagi, M. (2000). Evidence that the Aspergillus nidulans class I and class II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J Biochem 127, 359-366.
25. Gastebois, A., Clavaud, C., Aimanianda, V. & Latgé, J. P. (2009). Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol 4, 583-595.
26. Gastebois, A., Fontaine, T., Latgé, J. P. & Mouyna, I. (2010a). b(1-3) Glucanosyltransferase Gel4p is essential for Aspergillus fumigatus. Eukaryot Cell 9, 1294-1298.
27. Gastebois, A., Mouyna, I., Simenel, C., Clavaud, C., Coddeville, B., Delepierre, M., Latgé, J. P. & Fontaine, T. (2010b). Characterization of a new b(1-3)-glucan branching activity of Aspergillus fumigatus. J Biol Chem 285, 2386-2396.
28. Hamaguchi, T., Ito, T., Inoue, Y., Limpaseni, T., Pongsawasdi, P. & Ito, K. (2010). Purification, characterization and molecular cloning of a novel endo-b-N-acetylglucosaminidase from the basidiomycete, Flammulina velutipes. Glycobiology 20, 420-432.
29. Hartl, L., Gastebois, A., Aimanianda, V. & Latgé, J. P. (2011). Characterization of the GPI-anchored endo β-1,3-glucanase Eng2 of Aspergillus fumigatus. Fungal Genet Biol 48, 185-191.
30. Ishida, T., Fushinobu, S., Kawai, R., Kitaoka, M., Igarashi, K. & Samejima, M. (2009). Crystal structure of glycoside hydrolase family 55 β-1,3-glucanase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 284, 10100-10109.
31. Itoh, T., Ochiai, A., Mikami, B., Hashimoto, W. & Murata, K. (2006). A novel glycoside hydrolase family 105: the structure of family 105 unsaturated rhamnogalacturonyl hydrolase complexed with a disaccharide in comparison with family 88 enzyme complexed with the disaccharide. J Mol Biol 360, 573-585.
32. Jäger, G., Girfoglio, M., Dollo, F., Rinaldi, R., Bongard, H., Commandeur, U., Fischer, R., Spiess, A. C. & Büchs, J. (2011). How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 4, 33.
33. Jaques, A. K., Fukamizo, T., Hall, D., Barton, R. C., Escott, G. M., Parkinson, T., Hitchcock, C. A. & Adams, D. J. (2003). Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology 149, 2931-2939.
34. Jørgensen, T. R., Nitsche, B. M., Lamers, G. E., Arentshorst, M., van den Hondel, C. A. & Ram, A. F. (2010). Transcriptomic insights into the physiology of Aspergillus niger approaching a specific growth rate of zero. Appl Environ Microbiol 76, 5344-5355.
35. Jørgensen, T. R., Park, J., Arentshorst, M., van Welzen, A. M., Lamers, G., Vankuyk, P. A., Damveld, R. A., van den Hondel, C. A., Nielsen, K. F. & other authors (2011). Themolecular and genetic basis of conidial pigmentation in Aspergillus niger. Fungal Genet Biol 48, 544-553.
36. Karlsson, M. & Stenlid, J. (2008). Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinform Online 4, 47-60.
37. Kitagaki, H., Wu, H., Shimoi, H. & Ito, K. (2002). Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae. Mol Microbiol 46, 1011-1022.
38. Krijgsheld, P., Bleichrodt, R., van Veluw, G. J., Wang, F., Müller, W. H., Dijksterhuis, J. & Wösten, H. A. (2013). Development in Aspergillus. Stud Mycol 74, 1-29.
39. Kuranda, M. J. & Robbins, P. W. (1991). Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266, 19758-19767.
40. Latgé, J. P., Mouyna, I., Tekaia, F., Beauvais, A., Debeaupuis, J. P. & Nierman, W. (2005). Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Med Mycol 43 (Suppl 1), 15-22.
41. Lee, J. I., Choi, J. H., Park, B. C., Park, Y. H., Lee, M. Y., Park, H. M. & Maeng, P. J. (2004). Differential expression of the chitin synthase genes of Aspergillus nidulans, chsA, chsB, and chsC, in response to developmental status and environmental factors. Fungal Genet Biol 41, 635-646.
42. Levin, A. M., de Vries, R. P., Conesa, A., de Bekker, C., Talon, M., Menke, H. H., van Peij, N. N. M. E. & Wösten, H. A. B. (2007). Spatial differentiation in the vegetative mycelium of Aspergillus niger. Eukaryot Cell 6, 2311-2322.
43. Maddi, A., Fu, C. & Free, S. J. (2012). The Neurospora crassa dfg5 and dcw1 genes encode α-1,6-mannanases that function in the incorporation of glycoproteins into the cell wall. PLoS ONE 7, e38872.
44. Martens-Uzunova, E. S. & Schaap, P. J. (2009). Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet Biol 46 (Suppl 1), S170-S179.
45. Maubon, D., Park, S., Tanguy, M., Huerre, M., Schmitt, C., Prévost, M. C., Perlin, D. S., Latgé, J. P. & Beauvais, A. (2006). AGS3, an a(1-3) glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genet Biol 43, 366-375.
46. Meyer, V., Ram, A. F. & Punt, P. J. (2010). Genetics, genetic manipulation and approaches to strain improvement of filamentous fungi. In Manual of Industrial Microbiology and Biotechnology, 3rd edn, pp. 318-329. Edited by R. H. Baltz, A. L. Demain & J. E. Davies. New York: Wiley.
47. Meyer, V., Wanka, F., van Gent, J., Arentshorst, M., van den Hondel, C. A. & Ram, A. F. (2011). Fungal gene expression on demand: an inducible, tunable, and metabolism-independent expression system for Aspergillus niger. Appl Environ Microbiol 77, 2975-2983.
48. Mouyna, I., Hartland, R. P., Fontaine, T., Diaquin, M., Simenel, C., Delepierre, M., Henrissat, B. & Latgé, J. P. (1998). A 1,3-betaglucanosyltransferase isolated from the cell wall of Aspergillus fumigatus is a homologue of the yeast Bgl2p. Microbiology 144, 3171-3180.
49. Mouyna, I., Fontaine, T., Vai, M., Monod, M., Fonzi, W. A., Diaquin, M., Popolo, L., Hartland, R. P. & Latgé, J. P. (2000). Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275, 14882-14889.
50. Mouyna, I., Morelle, W., Vai, M., Monod, M., Léchenne, B., Fontaine, T., Beauvais, A., Sarfati, J., Prévost, M. C. & other authors (2005). Deletion of GEL2 encoding for a b(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol Microbiol 56, 1675-1688.
51. Nitsche, B. M., Jørgensen, T. R., Akeroyd, M., Meyer, V. & Ram, A. F. (2012). The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13, 380.
52. Oda, K., Kasahara, S., Yamagata, Y., Abe, K. & Nakajima, T. (2002). Cloning and expression of the exo-b-D-1,3-glucanase gene (exgS) from Aspergillus saitoi. Biosci Biotechnol Biochem 66, 1587-1590.
53. Pel, H. J., de Winde, J. H., Archer, D. B., Dyer, P. S., Hofmann, G., Schaap, P. J., Turner, G., de Vries, R. P., Albang, R. & other authors (2007). Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25, 221-231.
54. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H. & van den Hondel, C. A. (1987). Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56, 117-124.
55. Pusztahelyi, T., Molnár, Z., Emri, T., Klement, E., Miskei, M., Kerékgyárto, J., Balla, J. & Pócsi, I. (2006). Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans. Folia Microbiol (Praha) 51, 547-554.
56. Ragni, E., Coluccio, A., Rolli, E., Rodriguez-Peña, J. M., Colasante, G., Arroyo, J., Neiman, A. M. & Popolo, L. (2007a). GAS2 and GAS4, a pair of developmentally regulated genes required for spore wall assembly in Saccharomyces cerevisiae. Eukaryot Cell 6, 302-316.
57. Ragni, E., Fontaine, T., Gissi, C., Latgè, J. P. & Popolo, L. (2007b). The Gas family of proteins of Saccharomyces cerevisiae: characterization and evolutionary analysis. Yeast 24, 297-308.
58. Ram, A. F. & Klis, F. M. (2006). Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1, 2253-2256.
59. Riou, C., Salmon, J. M., Vallier, M. J., Günata, Z. & Barre, P. (1998). Purification, characterization, and substrate specificity of a novel highly glucose-tolerant beta-glucosidase from Aspergillus oryzae. Appl Environ Microbiol 64, 3607-3614.
60. Sambrook, J., Frisch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
61. Stals, I., Samyn, B., Sergeant, K., White, T., Hoorelbeke, K., Coorevits, A., Devreese, B., Claeyssens, M. & Piens, K. (2010). Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina. FEMS Microbiol Lett 303, 9-17.
62. Stals, I., Karkehabadi, S., Kim, S., Ward, M., Van Landschoot, A., Devreese, B. & Sandgren, M. (2012). High resolution crystal structure of the endo-N-acetyl-b-D-glucosaminidase responsible for the deglycosylation of Hypocrea jecorina cellulases. PLoS ONE 7, e40854.
63. Stolz, J. & Munro, S. (2002). The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis. J Biol Chem 277, 44801-44808.
64. Tamano, K., Satoh, Y., Ishii, T., Terabayashi, Y., Ohtaki, S., Sano, M., Takahashi, T., Koyama, Y., Mizutani, O. & other authors (2007). The β-1,3-exoglucanase gene exgA (exg1) of Aspergillus oryzae is required to catabolize extracellular glucan, and is induced in growth on a solid surface. Biosci Biotechnol Biochem 71, 926-934.
65. Tjoelker, L. W., Gosting, L., Frey, S., Hunter, C. L., Trong, H. L., Steiner, B., Brammer, H. & Gray, P. W. (2000). Structural and functional definition of the human chitinase chitin-binding domain. J Biol Chem 275, 514-520.
66. Tusher, V. G., Tibshirani, R. & Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98, 5116-5121.
67. Ujita, M., Sakai, K., Hamazaki, K., Yoneda, M., Isomura, S. & Hara, A. (2003). Carbohydrate binding specificity of the recombinant chitinbinding domain of human macrophage chitinase. Biosci Biotechnol Biochem 67, 2402-2407.
68. Vaaje-Kolstad, G., Horn, S. J., van Aalten, D. M., Synstad, B. & Eijsink, V. G. (2005). The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280, 28492-28497.
69. Vaaje-Kolstad, G., Westereng, B., Horn, S. J., Liu, Z., Zhai, H., Sørlie, M. & Eijsink, V. G. (2010). An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330, 219-222.
70. van den Burg, H. A., Harrison, S. J., Joosten, M. H., Vervoort, J. & de Wit, P. J. (2006). Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19, 1420-1430.
71. van der Kaaij, R. M., Yuan, X. L., Franken, A., Ram, A. F., Punt, P. J., van der Maarel, M. J. & Dijkhuizen, L. (2007). Two novel, putatively cell wall-associated and glycosylphosphatidylinositol-anchored aglucanotransferase enzymes of Aspergillus niger. Eukaryot Cell 6, 1178-1188.
72. van Esse, H. P., Bolton, M. D., Stergiopoulos, I., de Wit, P. J. & Thomma, B. P. (2007). The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20, 1092-1101.
73. van Gorcom, R. F. & van den Hondel, C. A. (1988). Expression analysis vectors for Aspergillus niger. Nucleic Acids Res 16, 9052.
74. van Hartingsveldt, W., Mattern, I. E., van Zeijl, C. M. J., Pouwels, P. H. & van den Hondel, C. A. M. J. J. (1987). Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol Gen Genet 206, 71-75.
75. van Leeuwen, M. R., Krijgsheld, P., Bleichrodt, R., Menke, H., Stam, H., Stark, J., Wösten, H. A. & Dijksterhuis, J. (2013). Germination of conidia of Aspergillus niger is accompanied by major changes in RNA profiles. Stud Mycol 74, 59-70.
76. van Munster, J. M., van der Kaaij, R. M., Dijkhuizen, L. & van der Maarel, M. J. E. C. (2012). Biochemical characterization of Aspergillus niger CfcI, a glycoside hydrolase family 18 chitinase that releases monomers during substrate hydrolysis. Microbiology 158, 2168-2179.
77. Vinck, A., de Bekker, C., Ossin, A., Ohm, R. A., de Vries, R. P. & Wösten, H. A. B. (2011). Heterogenic expression of genes encoding secreted proteins at the periphery of Aspergillus niger colonies. Environ Microbiol 13, 216-225.
78. Wei, H., Scherer, M., Singh, A., Liese, R. & Fischer, R. (2001). Aspergillus nidulans α-1,3 glucanase (mutanase), mutA, is expressed during sexual development and mobilizes mutan. Fungal Genet Biol 34, 217-227.
79. Yamazaki, H., Yamazaki, D., Takaya, N., Takagi, M., Ohta, A. & Horiuchi, H. (2007). A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans. Curr Genet 51, 89-98.
80. Yamazaki, H., Tanaka, A., Kaneko, J., Ohta, A. & Horiuchi, H. (2008). Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet Biol 45, 963-972.
81. Yuan, X. L., van der Kaaij, R. M., van den Hondel, C. A., Punt, P. J., van der Maarel, M. J., Dijkhuizen, L. & Ram, A. F. (2008). Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics 279, 545-561