Extra-and intracellular lactose catabolism in Penicillium chrysogenum: Phylogenetic and expression analysis of the putative permease and hydrolase genes

Journal of Antibiotics

Volumn 67, Issue 7, 2014, Pages 489-497

  Jónás, Ágota ^a   Fekete, Erzsébet ^a   Flipphi, Michel ^a,b   Sándor, Erzsébet ^c   Jäger, Szilvia ^a   Molnár, Ákos P ^a   Szentirmai, Attila ^a   Karaffa, Levente ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b CNRS   (France)

^c UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

beta galactosidase; D galactose; L arabinose; lactose; Penicillium chrysogenum; permease

Indexed keywords

ARABINOSE; ASPERGILLUS NIDULANS; BETA-GALACTOSIDASE; FUNGAL PROTEINS; HYDROLASES; LACTOSE; MEMBRANE TRANSPORT PROTEINS; METABOLISM; PENICILLINS; PENICILLIUM CHRYSOGENUM; PHYLOGENY;

EID: 84904974407     PISSN: 00218820     EISSN: 18811469     Source Type: Journal    
DOI: 10.1038/ja.2014.26     Document Type: Article

References (66)

1. Roelfsema, W. A., Kuster, B. F. M., Heslinga, M. C., Pluim, H. & Verhage, M. in Lactose and Derivatives. Ullmann's Encyclopedia of Industrial Chemistry 7th edn (John S) Wiley & Sons, New York, NY, 2010).
2. Brüssow, H. Nutrition, population growth and disease: A short history of lactose. Environ. Microbiol. 15, 2154-2161 (2013).
3. Naz, S., Siddiqi, R., Dew, T. P. & Williamson, G. Epigallocatechin-3-gallate inhibits lactase but is alleviated by salivary proline-rich proteins. J. Agric. Food Chem. 59, 2734-2738 (2011).
4. Persson, I., Tjerneld, F. & Hahn-Hägerdal, B. Fungal cellulolytic enzyme production: A review. Process Biochem. 26, 65-74 (1991).
5. Brakhage, A. A. Molecular regulation of (Pubitemid 28415544)
6. Penttilä , M., Limón, C. & Nevalainen, H. in Handbook of Fungal Biotechnology Arora, D. K. (ed.) 413-427 (Marcel Dekker, New York, 2004).
7. Seiboth, B., Pakdaman, B. S., Hartl, L. & Kubicek, C. P. Lactose metabolism in filamentous fungi: How to deal with an unknown substrate. Fungal Biol. Rev. 21, 42-48 (2007). (Pubitemid 46946871)
8. Sheetz, R. M. & Dickson, R. C. LAC4 is the structural gene for b-galactosidase in Kluyveromyces lactis. Genetics 98, 729-745 (1981).
9. Riley, M. I., Sreekrishna, K., Bhairi, S. & Dickson, R. C. Isolation and characterization of mutants of Kluyveromyces lactis defective in lactose transport. Mol. Gen. Genet. 208, 145-151 (1987).
10. Lodi, T. & Donnini, C. Lactose-induced cell death of b-galactosidase mutants in Kluyveromyces lactis. FEMS Yeast Res. 5, 727-734 (2005). (Pubitemid 40558920)
11. Fekete, E. et al. Identification of a permease gene involved in lactose utilisation in Aspergillus nidulans. Fungal Genet. Biol. 49, 415-425 (2012).
12. Nevalainen, K. M. H. Induction, isolation, and characterization of Aspergillus niger mutant strains producing elevated levels of b-galactosidase. Appl. Environ. Microbiol. 41, 593-596 (1981). (Pubitemid 11158701)
13. Ó Connell, S. & Walsh, G. A novel acid-stable, acid-active b-galactosidase potentially suited to the alleviation of lactose intolerance. Appl. Microbiol. Biotechnol. 86, 517-524 (2010).
14. Gamauf, C. et al. Characterization of the bga1-encoded glycoside hydrolase family 35 b-galactosidase of Hypocrea jecorina with galacto-b-D-galactanase activity. FEBS J. 274, 1691-1700 (2007). (Pubitemid 46426904)
15. Ishikawa, E., Sakai, T., Ikemura, H., Matsumoto, H. & Abe, H. Identification, cloning, and characterization of a Sporobolomyces singularis b-galactosidase-like enzyme involved in galacto-oligosaccharide production. J. Biosci. Bioeng. 99, 331-339 (2005). (Pubitemid 40740582)
16. Bates, W. K. & Woodward, D. O. Neurospora b-galactosidase: Evidence for a second enzyme. Science 146, 777-778 (1964).
17. Houbraken, J., Frisvad, J. C. & Samson, R. A. Fleming's penicillin producing strain is not Penicillium chrysogenum but P. rubens. IMA Fungus 2, 87-95 (2011).
18. Van Den Berg, M. A. Impact of the Penicillium chrysogenum genome on industrial production of metabolites. Appl. Microbiol. Biotechnol. 92, 45-53 (2011).
19. Barreiro, C., Mart́n, J. F. & Garća-Estrada, C. Proteomics shows new faces for the old penicillin producer Penicillium chrysogenum. J. Biomed. Biotechnol. 2012, 105109 (2012).
20. Weber, S. S., Bovenberg, R. A. & Driessen, A. J. Biosynthetic concepts for the production of beta-lactam antibiotics in Penicillium chrysogenum. Biotechnol. J. 7, 225-236 (2012).
21. Nagy, Z., Kiss, T., Szentirmai, A. & Biró, S. b-Galactosidase of Penicillium chrysogenum: Production, purification, and characterization of the enzyme. Protein Expr. Purif. 21, 24-29 (2001). (Pubitemid 32614492)
22. Nagy, Z., Keresztessy, Z., Szentirmai, A. & Biró , S. Carbon source regulation of b-galactosidase biosynthesis in Penicillium chrysogenum. J. Basic. Microbiol. 41, 351-362 (2001). (Pubitemid 34067555)
23. D́ez, B., Rodŕguez-Sáiz, M., de la Fuente, J.L., Moreno, M. Á. & Barredo, J. L. The nagA gene of Penicillium chrysogenum encoding b-N-acetylglucosaminidase. FEMS Microbiol. Lett. 242, 257-264 (2005). (Pubitemid 40038397)
24. Ike, M. et al. Cloning and heterologous expression of the exo-b-D-glucosamini dase-encoding gene (gls93) from a filamentous fungus, Trichoderma reesei PC-3-7. Appl. Microbiol. Biotechnol. 72, 687-695 (2006). (Pubitemid 44454928)
25. Nikolaev, I. V. & Vinetski, Y. P. L-Arabinose induces synthesis of secreted b-galactosidase in the filamentous fungus Penicillium canescens. Biochemistry (Mosc.) 63, 1294-1298 (1998).
26. Cruz, R. et al. Production of transgalactosylated oligosaccharides (TOS) by galactosyltransferase activity from Penicillium simplicissimum. Bioresour. Technol. 70, 165-171 (1999). (Pubitemid 29253529)
27. Raper, K. B., Alexander, D. F. & Coghill, R. D. Penicillin. II. Natural variation and penicillin production in Penicillium notatum and allied species. J. Bacteriol. 487, 639-659 (1944).
28. Newbert, R. W., Barton, B., Greaves, P., Harper, J. & Turner, G. Analysis of a commercially improved Penicillium chrysogenum strain series: Involvement of recombinogenic regions in amplification and deletion of the penicillin biosynthesis gene cluster. J. Ind. Microbiol. Biotechnol. 19, 18-27 (1997). (Pubitemid 27467128)
29. Barredo, J. L., D́ez, B., Alvarez, E. & Mart́n, J. F. Large amplification of a 35kb DNA fragment carrying two penicillin biosynthetic genes in high pencillin producing strains of Penicillium chrysogenum. Curr. Genet. 16, 453-459 (1989).
30. Haas, H., Angermayr, K., Zadra, I. & Stöffler, G. Overexpression of nreB, a new GATA factor-encoding gene of Penicillium chrysogenum, leads to repression of the nitrate assimilatory gene cluster. J. Biol. Chem. 272, 22576-22582 (1997). (Pubitemid 27386070)
31. Pirt, S. J. Principles of Microbe and Cell Cultivation. 156-170 (Blackwell Scientific Publications, Oxford, UK, 1975).
32. Sambrook, J. & Russell, D. W. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory, New York, 2001).
33. Linz, J. E., Lira, L. M. & Sypherd, P. S. The primary structure and the functional domains of an elongation factor-1a from Mucor racemosus. J. Biol. Chem. 261, 15022-15029 (1986). (Pubitemid 17218068)
34. van den Berg, M. A. et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161-1168 (2008).
35. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997). (Pubitemid 27359211)
36. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL-W-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positionspecific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (1994). (Pubitemid 24354800)
37. Nicholas, K. B. & Nicholas, H. B. GeneDock: A tool for editing and annotating multiple sequence alignements. www.psc.edu/biomed/genedoc (2007)
38. Tamura, K. et al. Mega 5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
39. Saitou, N. & Nei, M. The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).
40. Peterson, G. L. Determination of total protein. Methods Enzymol. 91, 86-105 (1983).
41. Hugget, A. S. & Nixon, D. A. Use of glucose oxidase, peroxidase, and O-dianisidine in determination of blood and urinary glucose. Lancet 273, 368-370 (1957).
42. MacCabe, A. P., Miro, P., Ventura, L. & Ramon, D. Glucose uptake in germinating Aspergillus nidulans conidia: Involvement of the creA and sorA genes. Microbiology 149, 2129-2136 (2003). (Pubitemid 37038418)
43. Seiboth, B. et al. Role of the bga1-encoded extracellular b-galactosidase of Hypocrea jecorina in cellulase induction by lactose. Appl. Environ. Microbiol. 71, 851-857 (2005). (Pubitemid 40223572)
44. Fekete, E. et al. Regulation of formation of the intracellular beta-galactosidase activity of Aspergillus nidulans. Arch. Microbiol. 179, 7-14 (2002).
45. De Vries, R. P. & Visser, J. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 65, 497-522 (2001). (Pubitemid 33123516)
46. Houbraken, J. & Samson, R. A. Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud. Mycol. 70, 1-51 (2011).
47. Kumar, V., Ramakrishnan, S., Teeri, T. T., Knowles, J. K. C. & Hartley, B. S. Saccharomyces cerevisiae cells secreting an Aspergillus niger beta-galactosidase grow on whey permeate. Biotechnology (NY) 10, 82-85 (1992).
48. Pel, H. J. et al. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 25, 221-231 (2007). (Pubitemid 46227122)
49. Wilson, C.J., Zhan, H., Swint-Kruse, L. & Matthews, K.S. The lactose repressor system: Paradigms for regulation, allosteric behavior and protein folding. Cell. Mol. Life Sci.64, 3-16 (2007). (Pubitemid 46164491)
50. Rodicio, R. & Heinisch, J. J. Yeast on the milky way: Genetics, physiology and biotechnology of Kluyveromyces lactis. Yeast 30, 165-177 (2013).
51. Comp, P. C. & Lester, G. Properties of an extracellular beta-galactosidase secreted by Neurospora crassa. J. Bacteriol. 107, 162-167 (1971).
52. Anumukonda, P. & Tadimalla, P. Screening of b-galactosidase producing fungi from marine samples. Biomed. Pharmacol. J. 3, 81-86 (2010).
53. ÓConnell, S. & Walsh, G. Application relevant studies of fungal b-galactosidase with potential application in the alleviation of lactose intolerance. Appl. Biochem. Biotechnol. 149, 129-138 (2008).
54. Isobe, K., Takahashi, N., Chiba, S., Yamashita, M. & Koyama, T. Acidophilic fungus, Teratosphaeria acidotherma AIU BGA-1, produces multiple forms of intracellular b-galactosidase. J. Biosci. Bioeng. 116, 171-174 (2013).
55. Hasan, N. & Durr, I. F. Induction of beta-galactosidase in Lactobacillus plantarum. J. Bacteriol. 120, 66-73 (1974).
56. De Vries, R. P. et al. Differential expression of three a-galactosidase genes and a single b-galactosidase gene from Aspergillus niger. Appl. Environ. Microbiol. 65, 2453-2460 (1999).
57. Chulkin, A. M., Vavilova, E. A. & Benevolenskii, S. V. Mutational analysis of carbon catabolite repression in filamentous fungus Penicillium canescens. Mol. Biol. 45, 804-810 (2011).
58. Ilyés, H et al. CreA-mediated carbon catabolite repression of beta-galactosidase formation in Aspergillus nidulans is growth rate dependent. FEMS Microbiol. Lett. 235, 147-151 (2004). (Pubitemid 38668649)
59. Du, Y. & Kong, F. Synthesis, conformation and glycosylation reaction of substituted2,6-dioxabicyclo[3.1.1]heptanes:1,3-anhydro-2,4-di-O-benzyl-a-L- arabinopyrano-se. Carbohydr. Res. 275, 259-273 (1995).
60. Galazka, J. M. et al. Cellodextrin transport in yeast for improved biofuel production. Science 330, 84-86 (2010).
61. Ivanova, C., Ba°a° th, J. A., Seiboth, B. & Kubicek, C. P. Systems analysis of lactose metabolism in Trichoderma reesei identifies a lactose permease that is essential for cellulase induction. PLoS One 8, e62631 (2013).
62. Seiboth, B. et al. The galactokinase of Hypocrea jecorina is essential for cellulase induction by lactose but dispensable for growth on D-galactose. Mol. Microbiol. 51, 1015-1025 (2004). (Pubitemid 38270796)
63. Fekete, E., Seiboth, B., Kubicek, C. P., Szentirmai, A. & Karaffa, L. Lack of aldose 1-epimerase in Hypocrea jecorina (anamorph Trichoderma reesei): A key to cellulase gene expression on lactose. Proc. Natl Acad. Sci. USA 105, 7141-7146 (2008). (Pubitemid 351754445)
64. Karaffa, L. et al. The intracellular galactoglycome in Trichoderma reesei during growth on lactose. Appl. Microbiol. Biotechnol. 97, 5447-5456 (2013).
65. Espeso, E. A. & Peñ alva, M. A. In vitro binding of the two-finger repressor CreA to several consensus and non-consensus sites at the ipnA upstream region is context dependent. FEBS Lett. 342, 43-48 (1994).
66. Flipphi, M. et al. Onset of carbon catabolite repression in Aspergillus nidulans: Parallel involvement of hexokinase and glucokinase in sugar signaling. J. Biol. Chem. 278, 11849-11857 (2003). (Pubitemid 36800155)