| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
-galactosidase (Bga1) formation by D-galactose in Hypocrea jecorina is mediated by galactitol
1 Department of Genetics and Applied Microbiology, Faculty of Science, University of Debrecen, H-4010, PO Box 56, Debrecen, Hungary
2 Research Area Gene Technology and Applied Biochemistry, Institute of Chemical Engineering, TU Wien, Getreidemarkt 9/166-5, A-1060 Wien, Austria
Correspondence
Bernhard Seiboth
bseiboth{at}mail.zserv.tuwien.ac.at
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
-galactosidase, encoded by the bga1 gene. Previous studies, using batch or transfer cultures of pregrown cells, had shown that bga1 is induced by lactose and D-galactose, but to a lesser extent by galactitol. To test whether the induction level is influenced by the different growth rates attainable on these carbon sources, bga1 expression was compared in carbon-limited chemostat cultivations at defined dilution (=specific growth) rates. The data showed that bga1 expression by lactose, D-galactose and galactitol positively correlated with the dilution rate, and that galactitol and D-galactose induced the highest activities of -galactosidase at comparable growth rates. To know more about the actual inducer for -galactosidase formation, its expression in H. jecorina strains impaired in the first steps of the two D-galactose-degrading pathways was compared. Induction by D-galactose and galactitol was still found in strains deleted in the galactokinase-encoding gene gal1, which is responsible for the first step of the Leloir pathway of D-galactose catabolism. However, in a strain deleted in the aldose/D-xylose reductase gene xyl1, which performs the reduction of D-galactose to galactitol in a recently identified second pathway, induction by D-galactose, but not by galactitol, was impaired. On the other hand, induction by D-galactose and galactitol was not affected in an L-arabinitol 4-dehydrogenase (lad1)-deleted strain which is impaired in the subsequent step of galactitol degradation. These results indicate that galactitol is the actual inducer of Bga1 formation during growth on D-galactose in H. jecorina.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
-Galactosidase (EC 3.2.1.23) catalyses the hydrolysis of terminal non-reducing -D-galactose residues in -D-galactosides, including the disaccharide lactose (1,4-O--D-galactopyranosyl-D-glucose). Such enzymes can be classified as members of four different glycoside hydrolase (GH) families [GH1, GH2, GH35 and GH42; Carbohydrate Active Enzymes database: http://afmb.cnrs-mrs.fr/CAZY/ (Coutinho & Henrissat, 1999
)], indicating a structural and maybe also functional diversity. In biotechnology, -galactosidases are mainly employed for the hydrolysis of lactose to D-glucose and D-galactose in various products of the dairy industry (Gekas & Lopez-Leiva, 1985; Holsinger & Kligerman, 1991). In addition, -galactosidases catalyse transgalactosylation reactions, which have attracted considerable interest because of suggested beneficial effects on human health (Boon et al., 2000; Nakayama & Amachi, 1999).
The filamentous fungus Hypocrea jecorina (anamorph: Trichoderma reesei) is a potent producer of cellulolytic and hemicellulolytic enzymes (Penttilä et al., 2004; Persson et al., 1991). Lactose induces the formation of these enzymes and is today the major soluble carbon source for their production on a technical scale. Biochemical and genetic evidence is available that H. jecorina initiates lactose metabolism by first hydrolysing it extracellularly, and then taking up and metabolizing the hydrolysis products D-glucose and D-galactose, thus placing the extracellular -galactosidase in a central position for lactose metabolism in this fungus. H. jecorina contains one major extracellular GH family 35 -galactosidase (Seiboth et al., 2005). In 
bga1 strains, only minor -galactosidase activities are found, either cell wall bound or in the supernatant, but no intracellular -galactosidase activity is detectable during growth on lactose.
Regulation of Bga1 formation is less well understood. The bga1 transcript is most abundant during growth of H. jecorina on L-arabinose and L-arabinitol. Lower levels are present on lactose, but also on D-galactose and D-xylose, and their corresponding polyols. In addition, bga1 transcription is subject to Cre1-dependent carbon catabolite repression, which acts at the level of both its basal expression and induction by D-galactose or lactose (Seiboth et al., 2005). The induction by one of the end products of lactose hydrolysis, D-galactose, as well as the hemicellulose monomers D-xylose and L-arabinose, may indicate a cross-talk between the induction of -galactosidase and hemicellulases, but the mechanisms involved are not yet known.
We have recently provided evidence for a second pathway of D-galactose metabolism in fungi, which proceeds as a stowaway of the fungal D-xylose and L-arabinose catabolic pathway (Fekete et al., 2004; Seiboth et al., 2004; Fig. 1). In this paper, we tested the hypothesis that the operation of this pathway is essential for bga1 induction by D-galactose.
|
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
bga1 (Seiboth et al., 2005), gal1 (Seiboth et al., 2004), lad1 (Pail et al., 2004) and xyl1 (B. Seiboth and others, unpublished results) were maintained on malt extract agar. Strains were grown in 500 ml Erlenmeyer flasks on a rotary shaker (250 r.p.m.) at 30 °C in the following medium (pH 5.0): 8 g NH4H2PO4 l–1, 7 g Na2HPO4 l–1, 4 g KH2PO4 l–1, 1 g CaCl2 l–1, 1 g MgSO4 l–1, 0.1 g peptone l–1, 20 ml trace elements l–1 (250 mg FeSO4.7H2O l–1, 80 mg MnSO4.H2O l–1, 70 mg ZnSO4.7H2O l–1, 85 mg CoCl2 l–1) with 10 g l–1 of the respective carbon source. For chemostat cultivations, cultures were pre-grown with glycerol (10 g l–1) as carbon source, and the content (2x100 ml) of two exponential-phase shake-flask cultures was used as inoculum. Mycelia were harvested by filtration after 36 h, washed with cold tap water and then transferred into fresh medium with the respective carbon source without peptone. Chemostat cultivations were carried out in a 2.5 l glass bioreactor (Inel) with a working volume of 2 l, equipped with one six-blade Rushton disc turbine impeller. The operating conditions were pH 5.0, 30 °C, 300 r.p.m. and 0.3 volumes of air per volume of liquid per minute (v.v.m.). To minimize water and substrate losses, the waste gas was cooled in a reflux condenser connected to an external cooling bath (4 °C). The feeding medium contained 3 g l–1 carbon source, a concentration low enough to facilitate carbon-limited cultivation. Glass parts of the reactor were treated with the anti-adhesive agent Sigmacot (Sigma) to avoid fungal growth on reactor walls, and a few drops of the antifoam agent polypropylene glycol 2000 (Union Carbide Chemicals and Plastics) were injected daily into the reactor through a membrane filter (Millipore). Onset of steady state in the culture was established when no changes in biomass dry weight were observed in three successive samples taken over a period of three residence times [defined as the reciprocal of the dilution rate (D), e.g. 20 h for D=0.050 h–1].
For transfer cultures, H. jecorina strains were pregrown and washed as described above, and transferred into fresh medium supplemented with 10 g l–1 of the respective carbon source without peptone. After 14 h, maximal induction levels of -galactosidase were found. At this time point, the residual carbon-source concentration in the medium was between 6.5 and 8.0 g l–1.
Biomass determination.
Mycelial dry weight was determined by twice withdrawing 20 ml aliquots from the medium, suction filtration through a glass-wool filter, and drying to a constant weight at 80 °C. Data were averaged, and deviated by no more than 14 %. In the case of batch cultures, 5 ml aliquots twice were used.
-Galactosidase assay.
-Galactosidase activity was determined with ONPG as substrate. The supernatant was diluted to 700 µl with 0.1 M phosphate buffer (pH 5) and added to 300 µl 10 mM ONPG. After incubating for 10–60 min at 30 °C, the reaction was stopped by the addition of 2 ml 1 M Na2CO3. A405 was measured against a blank in which the reaction had been stopped at t=0. Enzyme activities were expressed as nkat (mg dry weight)–1. One nanokatal corresponds to the conversion of one nanomole of substrate per second under given conditions.
HPLC analysis.
The concentrations of D-galactose, D-glucose, galactitol and lactose in the medium were determined by HPLC analysis, using the H+ exchange column Aminex HPX-H+ (Bio-Rad). As mobile phase, 10 mM H2SO4 at 55 °C was employed, with isocratic elution and refractive index detection.
Reproducibility.
Results are the means of three to five measurements. The data were analysed by Sigmaplot (SPSS) and SDs determined. The SD values were always less than 14 % of the mean.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
-galactosidase activity as a reporter for bga1 gene expression in H. jecorina-galactosidase activity in the culture supernatant by over 90 % in batch and transfer cultures, thereby providing evidence that the bga1-encoded gene product is the main extracellular -galactosidase in H. jecorina on lactose (Seiboth et al., 2005). In order to see whether this conclusion was also valid for the other carbon sources used in this study, we recorded the extracellular -galactosidase activity [nkat (mg dry weight)–1] of the parental H. jecorina QM9414 and a bga1 strain on D-galactose and galactitol over the whole period of a batch cultivation for about 80 h. At each time point, the bga1 mutant exhibited a -galactosidase activity only 4–8 % of that of QM9414. Similar reductions of -galactosidase activity for the bga1 strain were later also found in chemostat cultures at D=0.075 and 0.030 h–1 under D-galactose- and galactitol-limiting conditions, respectively. We therefore consider the appearance of the extracellular -galactosidase activity in the medium as a reliable reporter for bga1 expression in H. jecorina, and we employed this approach throughout the study.
Growth-rate-dependent -galactosidase formation on lactose and D-galactose
As the carbon sources (lactose, D-galactose and galactitol) that induce -galactosidase result in strongly different growth rates in batch cultures, we investigated if these varying growth rates influenced the expression level of the -galactosidase. Accordingly, chemostat cultivations at five defined dilution rates were performed between 0.075 and 0.015 h–1 under D-galactose- or lactose-limiting conditions. These dilution rates were identical to those used in our earlier study on the regulation of cellulases by H. jecorina (Karaffa et al., 2006). As reported previously, four to five residence times were needed to achieve steady state under these conditions. The residual steady-state concentrations of D-galactose and lactose in the medium were 0.10–0.12 mM and 0.09–0.12 mM, respectively, and the steady-state biomass concentration was 1.48±0.20 g l–1 for both carbon sources. Table 1 shows that D-galactose-supported growth resulted in a significantly higher -galactosidase activity than lactose-supported growth at the same growth rate (0.015–0.042 h–1). Higher dilution rates on lactose led to washing out of the mycelia and were only achievable with D-galactose as carbon source. A D-galactose-grown culture at D=0.075 h–1 yielded an activity of 100 nkat (mg dry weight)–1, which was about a fivefold increase over the activity obtained at the lowest dilution rate. This indicates that -galactosidase induction by D-galactose is growth-rate associated in H. jecorina.
|
-galactosidase formation on galactitol). However, galactitol is a poor carbon source for H. jecorina, and results in only slow growth rates, thus making a quantitative comparison of these results difficult. Consequently, we performed chemostat cultivations at defined growth rates with galactitol as the limiting carbon source. As previously reported (Karaffa et al., 2006), galactitol only allows the use of dilution rates between 0.03 and 0.05 h–1. The steady-state biomass concentration was somewhat lower (1.36±0.17 g l–1) than on D-galactose or lactose, and the residual steady-state concentration of galactitol was 0.08–0.09 mM. At the three dilution rates employed, however, -galactosidase activities were even higher than on D-galactose, and increased with increasing dilution rate (Table 1
), again indicating the growth-rate-associated nature of the extracellular -galactosidase formation in H. jecorina. Performing the same chemostat cultivations with an equimolar mixture of D-galactose and galactitol resulted in slightly reduced -galactosidase activities at dilution rates of 0.03 and 0.042 h–1 than with galactitol alone. We conclude that galactitol, at the same growth rate, can induce -galactosidase formation at least as well as D-galactose.
Growth-rate-dependent -galactosidase formation on D-glucose
Growth-rate-dependent -galactosidase formation could be in conflict with our earlier observations on regulation by the carbon catabolite repressor Cre1. In order to investigate whether carbon catabolite repression in fact influences -galactosidase formation by H. jecorina, we performed chemostat cultivations with D-glucose as the limiting nutrient at low dilution rates. Such a condition has recently been shown to cause carbon catabolite derepression in H. jecorina (Karaffa et al., 2006) and Aspergillus nidulans (Ilyés et al., 2004). -Galactosidase activity was found at D=0.015 h–1, which corresponded to about 55 and 30 % of that observed at the same growth rate on lactose and D-galactose, respectively. In contrast to the results obtained with D-galactose or lactose, no -galactosidase activity was detected with D-glucose as a carbon source at D=0.03 h–1 or higher (Table 2). The residual steady-state biomass concentration was 1.48±0.20 g l–1 and the D-glucose concentration was 0.08–0.10 mM. Chemostat cultivation on an equimolar mixture of D-glucose and D-galactose resulted in even higher -galactosidase activities at a dilution rate of 0.015 h–1, and still noticeable activities at 0.03 h–1, but no activity at all at higher dilution rates (Table 2), indicating that D-glucose interferes with the effect of D-galactose. Thus, the presence of D-glucose, consistent with our previous findings (Seiboth et al., 2005), clearly exerts carbon catabolite repression at higher growth rates; however, it aids in the induction by D-galactose at carbon-catabolite-derepressing growth rates.
|
-Galactosidase formation is induced via the second pathway of D-galactose catabolism). The enzyme catalysing the reversible reduction/oxidation of D-galactose/galactitol is the xyl1-encoded aldose/D-xylose reductase (B. Seiboth and others, unpublished results). In order to investigate whether D-galactose itself is the inducer for -galactosidase expression or the inducer is formed within one of these two pathways, we tested the induction by D-galactose and galactitol in strains which are defective in the first step of the leloir pathway (
gal1) or the second pathway of D-galactose degradation (xyl1). Since these gene deletions lead to an altered maximal growth rate of the investigated strains on the two carbon sources, and in addition it is to be expected that these deletions will also change the composition of the intracellular accumulating metabolites of the two D-galactose pathways, a quantitative comparison of -galactosidase activity based on chemostat cultures could not be performed. Therefore, the following experiments were done in transfer cultures. As can be seen from Table 3, in a xyl1 strain induction of -galactosidase activity during growth on galactitol reached the same level as in the parent strain QM9414, thus ruling out that catabolism of galactitol via the Leloir pathway would be necessary for the induction. In contrast, almost no -galactosidase activity was produced during growth on D-galactose by the xyl1 strain, indicating that the D-galactose to galactitol conversion is essential for this process. From these results it can also be excluded that the Xyl1 protein – apart from its enzymic conversion of D-galactose to galactitol – is needed for the induction process, because growth on galactitol alone induced -galactosidase in a xyl1 strain. This effect was also not due to a general interference of this deletion with growth or D-galactose metabolism, because the xyl1 mutant of H. jecorina was able to grow on both galactitol and D-galactose. A H. jecorina gal1 (galactokinase) strain induced -galactosidase activity on galactitol and – albeit with lower efficacy – on D-galactose, thus ruling out that the galactokinase itself or a metabolite formed in the Leloir pathway was necessary for the induction. The fact that the -galactosidase activity formation on D-galactose was decreased in the gal1 strain relative to QM9414 is most likely due to the strongly reduced growth rate of this strain (Seiboth et al., 2004). Taken together, these data indicate that D-galactose metabolism via the leloir pathway is dispensable for -galactosidase induction by D-galactose in H. jecorina.
|
-galactosidase formation in H. jecorina). In order to discriminate whether galactitol itself or a further catabolite formed in the later part of this pathway is responsible for the induction of the extracellular -galactosidase, we made use of a lad1 strain: this strain does not grow on galactitol but exhibits only a slightly reduced growth on D-galactose. Table 3 shows that -galactosidase activity formation was basically similar to that of QM9414, except that it was even higher on galactitol. This result, together with those obtained with the xyl1 and the gal1 strains, clearly indicates that galactitol itself, formed via the reduction of D-galactose, is able to induce the expression of bga1 in H. jecorina. |
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
-galactosidase-encoding bga1 on lactose and D-galactose in H. jecorina is in fact caused by galactitol, thereby partially revising and extending some of our earlier findings. By employing deletion strains in the aldose/D-xylose reductase- and galactokinase-encoding genes, we were able to show that D-galactose conversion to galactitol by the xyl1-encoded aldose reductase is obligatory for the expression of bga1. By the aid of a lad1 strain, which is impaired in the further conversion of galactitol, we additionally showed that the further steps in galactitol catabolism are dispensable for bga1 induction on D-galactose. The previously reported low efficacy of galactitol to induce -galactosidase in transfer cultures may therefore be related to the difficulty for the fungal cell to efficiently metabolize this polyol, as evidenced by the higher maintenance energy on galactitol than on D-galactose (Karaffa et al., 2006) and the in general poor biomass formation on galactitol (Druzhinina et al., 2006). In any case, our data show that it is important to use comparable growth rates when comparing different carbon compounds for their inducing potential. Induction of -galactosidase by galactitol further indicates that the alternative pathway of D-galactose degradation is apparently of major importance for the degradation of lactose by H. jecorina. We have recently discussed the fact that this may be due to the necessity of catabolizing the anomer of D-galactose, which arises from lactose hydrolysis by the action of Bga1 (Karaffa et al., 2006).
For A. nidulans it has previously been shown that induction of the intracellular -galactosidase activity by D-galactose also occurs in the galactokinase mutant gale and therefore does not require D-galactose phosphorylation. Accordingly, Fantes & Roberts (1973) and Fekete et al. (2002) speculated that the inducer for intracellular -galactosidase expression was produced via an at that time unknown alternative pathway for D-galactose catabolism. It still remains to be proven that galactitol is indeed the actual inducer for this -galactosidase also, but support for this assumption comes from the fact that the intracellular -galactosidase activity is not affected in the A. nidulans L-arabinitol 4-dehydrogenase mutant araa1 during growth on D-galactose (E. Fekete & L. Karaffa, unpublished results). It is noteworthy that the intracellular A. nidulans -galactosidase belongs to the GH2 family, while the H. jecorina Bga1 is a GH35 family member. In contrast to the induction by galactitol, it has been reported that the Kluyveromyces lactis GH2 family -galactosidase is induced by D-galactose (Cardinali et al., 1997). The reason for this might be that yeasts, including Saccharomyces cerevisiae and K. lactis, use the Leloir pathway exclusively for D-galactose catabolism (Frey, 1996).
-Galactosidases can also be induced by L-arabinose and L-arabinitol, and this cross-induction is also observed for several glycosidases acting on 
- as well as -linked carbohydrates (de Vries et al., 1999a, 2002; Kristufek et al., 1994; Nikolaev & Vinetski, 1998; Seiboth et al., 2005). Earlier authors have suggested that this may be due to the stereochemical similarity of L-arabinose and D-galactose. However, in view of the present results, it is also likely that the fungus catabolizes the different monomeric components (L-arabinose, D-galactose and D-xylose) released from the heterogeneous hemicelluloses via the same (i.e. the interconnected L-arabinose and D-xylose) pathway, and therefore ensures that the different inducers can be formed within this pathway to induce the full array of enzyme activities needed to degrade these complex hemicelluloses. It should be noted that lactose does not occur in the natural environment of the saprobic ascomycete H. jecorina. It is more likely that plant polysaccharides with -galactosidic linkages such as L-arabino-D-(--)-galactans are the original substrates for the -galactosidase. If true, a cross-induction mechanism such as this would have clear advantages. The ability of galactitol to induce -galactosidase also (Kristufek et al., 1994) would support this hypothesis. However, while galactitol does induce -galactosidase, we must admit that the involvement of the second pathway for D-galactose catabolism in this induction has not yet been proven, and may in theory still depend on its oxidation back to D-galactose.
In a similar manner to A. nidulans, the growth rate on D-glucose apparently determines carbon catabolite repression in H. jecorina also, and below a certain growth rate, carbon catabolite derepression occurs (Ilyés et al., 2004). Importantly, while an equimolar mixture of D-galactose and D-glucose at repressing growth rates resulted in the repression of bga1, their combined effect at derepressing (e.g. very low) growth rates resulted in the cumulative formation of extracellular -galactosidase activity. This observation underlines our previous claim (Seiboth et al., 2005) that the carbon catabolite repressor Cre1 (Strauss et al., 1995) exerts its influence at two distinct levels, e.g. at the basal and the induced level of bga1 expression. Interference of carbon catabolite regulation with gene expression at multiple regulatory levels is not unknown in fungi, and such ‘double-lock mechanisms' have already been reported in A. nidulans for alcA regulation (Mathieu & Felenbok, 1994) and -galactosidase formation (Fekete et al., 2002), and also in Aspergillus niger for xylanase biosynthesis (de Vries et al., 1999b). Chemostat-type continuous cultivations (Ilyés et al., 2004; Karaffa et al., 2006; Pakula et al., 2005) are a useful means to investigate such interfering mechanisms.
|
ACKNOWLEDGEMENTS |
|---|
Edited by: J.-R. Xu
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Cardinali, G., Vollenbroich, V., Jeon, M. S., de Graaf, A. A. & Hollenberg, C. P. (1997). Constitutive expression in gal7 mutants of Kluyveromyces lactis is due to internal production of galactose as an inducer of the Gal/Lac regulon. Mol Cell Biol 17, 1722–1730.[Abstract]
Coutinho, P. M. & Henrissat, B. (1999). Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering, pp. 3–12. Edited by H. J. Gilbert, G. Davies, B. Henrissat & B. Svensson. Cambridge: Royal Society of Chemistry.
de Vries, R. P., van den Broeck, H. C., Dekkers, E., Manzanares, P., de Graaff, L. H. & Visser, J. (1999a). Differential expression of three -galactosidase genes and a single -galactosidase gene from Aspergillus niger. Appl Environ Microbiol 65, 2453–2460.
de Vries, R. P., Visser, J. & de Graaff, L. H. (1999b). CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res Microbiol 150, 281–285.[Medline]
de Vries, R. P., Jansen, J., Aguilar, G., Parenicova, L., Joosten, V., Wulfert, F., Benen, J. A. & Visser, J. (2002). Expression profiling of pectinolytic genes from Aspergillus niger. FEBS Lett 530, 41–47.[CrossRef][Medline]
Druzhinina, I. S., Schmoll, M., Seiboth, B. & Kubicek, C. P. (2006). Global carbon utilization profiles of wild-type, mutant, and transformant strains of Hypocrea jecorina. Appl Environ Microbiol 72, 2126–2133.
Fantes, P. A. & Roberts, C. F. (1973). -Galactosidase activity and lactose utilization in Aspergillus nidulans. J Gen Microbiol 77, 417–486.
Fekete, E., Karaffa, L., Sandor, E., Seiboth, B., Biro, S., Szentirmai, A. & Kubicek, C. P. (2002). Regulation of formation of the intracellular -galactosidase activity of Aspergillus nidulans. Arch Microbiol 179, 7–14.[CrossRef][Medline]
Fekete, E., Karaffa, L., Sandor, E., Banyai, I., Seiboth, B., Gyemant, G., Sepsi, A., Szentirmai, A. & Kubicek, C. P. (2004). The alternative D-galactose degrading pathway of aspergillus nidulans proceeds via L-sorbose. Arch Microbiol 181, 35–44.[CrossRef][Medline]
Frey, P. A. (1996). The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. FASEB J 10, 461–470.[Abstract]
Gekas, V. & Lopez-Leiva, M. (1985). Hydrolysis of lactose: a literature review. Process Biochem 20, 2–12.
Holsinger, V. H. & Kligerman, A. E. (1991). Application of lactase in dairy foods and other foods containing lactose. Food Technol 45, 92–95.
Ilyés, H., Fekete, E., Karaffa, L., Fekete, É., Sándor, E., Szentirmai, A. & Kubicek, C. P. (2004). CreA-mediated carbon catabolite repression of -galactosidase formation in Aspergillus nidulans is growth rate dependent. FEMS Microbiol Lett 235, 147–151.[Medline]
Karaffa, L., Fekete, E., Gamauf, C., Szentirmai, A., Kubicek, C. P. & Seiboth, B. (2006). D-Galactose induces cellulase gene expression in Hypocrea jecorina at low growth rates. Microbiology 152, 1507–1514.
Kristufek, D., Hodits, R. & Kubicek, C. P. (1994). Coinduction of -L-arabinofuranosidase and -D-galactosidase formation in Trichoderma reesei RUT C-30. FEMS Microbiol Lett 115, 259–264.
Mathieu, M. & Felenbok, B. (1994). The Aspergillus nidulans CREA protein mediates glucose repression of the ethanol regulon at various levels through competition with the ALCR-specific transactivator. EMBO J 13, 4022–4027.[Medline]
Nakayama, T. & Amachi, T. (1999). -Galactosidase, enzymology. In Encyclopedia of Bioprocess Technology – Fermentation, Biocatalysis, and Bioseparation, pp. 1291–1305. Edited by M. C. Flickinger & S. W. Drew. New York: Wiley.
Nikolaev, I. V. & Vinetski, Y. P. (1998). L-Arabinose induces synthesis of secreted -galactosidase in the filamentous fungus Penicillium canescens. Biochemistry 63, 1294–1298.
Pail, M., Peterbauer, T., Seiboth, B., Hametner, C., Druzhinina, I. & Kubicek, C. P. (2004). The metabolic role and evolution of L-arabinitol 4-dehydrogenase of Hypocrea jecorina. Eur J Biochem 271, 1864–1872.[Medline]
Pakula, T. M., Salonen, K., Uusitalo, J. & Penttilä, M. (2005). The effect of specific growth rate on protein synthesis and secretion in the filamentous fungus Trichoderma reesei. Microbiology 151, 135–143.
Penttilä, M., Limon, C. & Nevalainen, H. (2004). Molecular biology of Trichoderma and biotechnological applications. In Handbook of Fungal Biotechnology, pp. 413–427. Edited by D. K. Arora. New York: Marcel Dekker.
Persson, I., Tjerneld, F. & Hahn-Hägerdal, B. (1991). Fungal cellulolytic enzyme production: a review. Process Biochem 26, 65–74.[CrossRef]
Seiboth, B., Hartl, L., Pail, M., Fekete, E., Karaffa, L. & Kubicek, C. P. (2004). The galactokinase of Hypocrea jecorina is essential for cellulase induction by lactose but dispensable for growth on D-galactose. Mol Microbiol 51, 1015–1025.[CrossRef][Medline]
Seiboth, B., Hartl, L., Salovuori, N., Lanthaler, K., Robson, G. D., Vehmaanperä, J., Penttilä, M. E. & Kubicek, C. P. (2005). Role of the bga1-encoded extracellular -galactosidase of Hypocrea jecorina in cellulase induction by lactose. Appl Environ Microbiol 71, 851–857.
Strauss, J., Mach, R. L., Zeilinger, S., Hartler, G., Stöffler, G., Wolschek, M. & Kubicek, C. P. (1995). Cre1, the carbon catabolite repressor protein from Trichoderma reesei. FEBS Lett 376, 103–107.[CrossRef][Medline]
Received 21 August 2006;
revised 9 November 2006;
accepted 15 November 2006.
This article has been cited by other articles:
|
|
 |
|
  L. Hartl, C. P. Kubicek, and B. Seiboth Induction of the gal Pathway and Cellulase Genes Involves No Transcriptional Inducer Function of the Galactokinase in Hypocrea jecorina J. Biol. Chem., June 22, 2007; 282(25): 18654 - 18659. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| INT J SYST EVOL MICROBIOL | MICROBIOLOGY | J GEN VIROL |
| J MED MICROBIOL | ALL SGM JOURNALS | |
