The Synthetic Potential of Fungal Feruloyl Esterases: A Correlation with Current Classification Systems and Predicted Structural Properties
Abstract
:1. Introduction
2. Results and Discussion
2.1. Synthesis of Aliphatic Esters
2.2. Synthesis of l-Arabinose Ferulate
2.3. Sugar Ester Synthesis by Two SF5 FAEs
2.4. Correlation with Phylogenetic Classification
2.5. Correlation with ABCD Classification
2.6. Factors Affecting Transesterification
3. Materials and Methods
3.1. Production of Enzymes in Myceliophthora thermophila C1
3.2. Production of Enzymes in Pichia pastoris
3.3. Enzymatic Assays
3.4. Transesterification Reactions
3.5. Quantitative Analysis of Hydroxycinnamates
3.6. Bioinformatic Tools
4. Conclusions
Supplementary Materials
Author Contributions
Acknowledgments
Conflicts of Interest
References
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Enzyme Sample | Origin | Expression | Calculated/Observed MW (kDa) | Calculated pI | N-Glycosylation | O-Glycosylation | FAE Content (% g FAE g−1 Protein) | Nucleophilic Elbow | SF a | Accession Number |
---|---|---|---|---|---|---|---|---|---|---|
Fungal FAEs | ||||||||||
Fae68 | Talaromyces wortmannii | Myceliophthora thermophila C1 | 58.7/58.8 | 4.96 | 10 | 11 | 10–15 | GCSTG | 1 | MF362596 |
AgFae1 | Aspergillus glaucus | Pichia pastoris | 55.8/75 | 5.49 | 7 | 1 | 31.3 | GCSTG | 1 | OJJ86166 |
AsFaeF | Aspergillus sydowii | Pichia pastoris | 55.4/75 | 4.89 | 6 | 1 | 67.5 | GCSTG | 1 | jgi|Aspsy1|293049 |
AnFaeB | Aspergillus niger | Pichia pastoris | 55.6/74 | 4.99 | 12 | 3 | 60.3 | GCSTG | 1 | Q8WZI8 |
FoFaeC | Fusarium oxysporum | Pichia pastoris | 62.0/62 | 6.39 | 6 | 3 | 86.7 | GCSTG | 2 | jgi|Fusox1|5438 |
AwFaeG | Aspergillus wentii | Pichia pastoris | 58.2/58 | 5.03 | 7 | 11 | 17.2 | GCSTG | 2 | jgi|Aspwe1|156253 |
AcarFaeB | Aspergillus carbonarius | Pichia pastoris | 56.0/58 | 5.02 | 5 | 2 | n/q | GCSFG | 3 | jgi|Aspca3|176503 |
Fae125 b | Talaromyces wortmannii | Myceliophthora thermophila C1 | 33.9/40 | 5.64 | 0 | 22 | 10 | GWSYG | 5 | MF362595 |
AtFaeD | Aspergillus terreus | Pichia pastoris | 26.5/43 | 4.22 | 0 | 1 | 10.7 | GWSWG | 5 | XP_001215822 |
C1FaeA1 | Myceliophthora thermophila C1 | Myceliophthora thermophila C1 | 27.2/29 | 6.15 | 0 | 2 | 33.7 | GWSYG | 5 | JF826027 |
AnidFAEC | Aspergillus nidulans | Pichia pastoris | 25.8/30 | 4.47 | 0 | 2 | 52.9 | GFSWG | 5 | EAA62427 |
C1FaeA2 | Myceliophthora thermophila C1 | Myceliophthora thermophila C1 | 29.1/36 | 5.05 | 1 | 8 | 15.0 | GFSYG | 5 | JF826028 |
AnFaeC | Aspergillus niger | Pichia pastoris | 28.2/30 | 4.44 | 1 | 1 | 47.3 | GFSWG | 5 | An12g02550 |
AsFaeC | Aspergillus sydowii | Pichia pastoris | 25.9/30 | 4.44 | 0 | 0 | 83.2 | GFSWG | 5 | jgi|Aspsy1|154482 |
C1FaeB2 c | Myceliophthora thermophila C1 | Myceliophthora thermophila C1 | 28.4/33 | 4.57 | 2 | 1 | 10.0 | GFSSG | 6 | JF826029 |
MtFae1a c | Myceliophthora thermophila ATCC 42464 | Pichia pastoris | 28.4/39 | 4.57 | 2 | 1 | 42.2 | GFSSG | 6 | AEO62008 |
C1FaeB1 | Myceliophthora thermophila C1 | Myceliophthora thermophila C1 | 28.3/29 | 5.74 | 1 | 2 | 50.0 | GGSSG | 6 | API68922 |
AsFaeE | Aspergillus sydowii | Pichia pastoris | 29.5/32 | 4.24 | 2 | 1 | 70.0 | GSSSG | 6 | jgi|Aspsy1|1158585 |
Fae7262 b | Talaromyces wortmannii | Myceliophthora thermophila C1 | 35.8/43 | 5.23 | 2 | 23 | 15–25 | GSSSG | 6 | MF362597 |
AnFaeA | Aspergillus niger | Pichia pastoris | 28.4/36 | 4.21 | 1 | 0 | 89.6 | GHSLG | 7 | CAA70510 |
AcFaeB | Aspergillus clavatus | Pichia pastoris | 39.1/40 | 6.23 | 4 | 1 | n/q | GHSFG | 8 | jgi|Aspcl1|3045 |
AsFaeG | Aspergillus sydowii | Pichia pastoris | 57.6/60 | 4.99 | 7 | 1 | 45.0 | GCSTG | 9 | jgi|Aspsy1|41271 |
AnFaeJ | Aspergillus niger | Pichia pastoris | 58.3/100 | 4.88 | 9 | 2 | 61.2 | GCSTG | 9 | An15g05280 |
CsTan1 | Ceriporiopsis subvermispora | Pichia pastoris | 57.6/90 | 4.67 | 7 | 4 | 48.5 | GCSTG | 9 | jgi|Cersu1|89153 |
AgFae2 | Aspergillus glaucus | Pichia pastoris | 53.2/75 | 5.55 | 7 | 5 | 16.6 | GCSTG | 10 | OJJ88972 |
AnFaeE | Aspergillus niger | Pichia pastoris | 55.0/88 | 4.11 | 8 | 14 | 71.2 | GCSTG | 10 | An11g01220 |
GmFae2 | Galerina marginata | Pichia pastoris | 57.0/59 | 6.49 | 5 | 4 | n/q | GESAG | 12 | jgi|Galma1|254175 |
AsFaeI | Aspergillus sydowii | Pichia pastoris | 59.4/55 | 4.90 | 5 | 5 | n/q | GESAG | 13 | jgi|Aspsy1|160668 |
Enzyme Sample | Type | Relative Hydrolytic Activity (%) | SF a | Reference | ||||
---|---|---|---|---|---|---|---|---|
MFA | MCA | MSA | MpCA | pNP-Fe | ||||
Fungal FAEs | ||||||||
Fae68 | B | 4.10 | 3.39 | 0 | 5.84 | n/d | 1 | This work |
AgFae1 | C | 0.031 | 0.047 | 0.005 | 0.020 | 0.025 | 1 | This work |
AsFaeF | B | 60.12 | 65.88 | 0 | 100 | 1.552 | 1 | [21] |
AnFaeB | B | 1.131 | 1.486 | 0 | 1.930 | 0.00074 | 1 | [21,26] |
FoFaeC | C | 0.247 | 0.389 | 0.013 | 0.457 | n/d | 2 | [21,27] This work |
AwFaeG | n/a | 0.00012 | 0 | 0 | 0 | 0.0016 | 2 | [21] |
AcarFaeB | n/a | 0 | 0.0024 | 0 | 0 | 0.0006 | 3 | [21] |
Fae125 | A | 0.059 | 0.024 | 0.047 | 0.023 | n/d | 5 | This work |
AtFaeD | C | 0.00022 | 0.00007 | 0.00022 | 0.00011 | 0.0172 | 5 | [28] |
C1FaeA1 | A | 0.127 | 0.057 | 0.114 | 0.059 | n/d | 5 | [29] |
AnidFAEC | C or D | 2.53 | 1.07 | 1.18 | 2.48 | 0.555 | 5 | [21] |
C1FaeA2 | A/B | 0.076 | 0.045 | 0.031 | 0.064 | n/d | 5 | [29] |
AnFaeC | C | 0.998 | 0.466 | 0.555 | 0.887 | n/d | 5 | [30] |
AsFaeC | C or D | 3.84 | 1.71 | 1.51 | 3.50 | 0.555 | 5 | [21] |
C1FaeB2 c | B | 0.616 | 0.458 | 0.096 | 0.794 | n/d | 6 | [29] |
MtFae1a c | B | 0.0010 | 0.0056 | 0 | 0 | 0.060 | 6 | [21,31] |
C1FaeB1 | B | 0.596 | 1.50 | 0 | 0.981 | n/d | 6 | [28] |
AsFaeE | C or D | 7.03 | 3.75 | 4.19 | 6.70 | 1.44 | 6 | [21] |
Fae7262 | B | 0.377 | 0.290 | 0 | 0.576 | n/d | 6 | This work |
AnFaeA | A | 1.708 | 0 | 1.375 | 0 | 0.0015 | 7 | [21,32] |
AcFaeB b | n/a | ~0 | ~0 | ~0 | ~0 | ~0 | 8 | [21] |
AsFaeG d | n/a | 0 | 0 | 0 | 0 | 0 | 9 | [21] |
AnFaeJ d | n/a | 0 | 0 | 1.52 | 0.149 | 0.0023 | 9 | [21] |
CsTan1 d | n/a | 0 | 0 | 0 | 0 | 0 | 9 | [21] |
AgFae2 | C | 0.0019 | 0.0007 | 0.0019 | 0.0015 | 0.0077 | 10 | This work |
AnFaeE | C | 0.011 | 0.040 | 0.009 | 0.001 | n/d | 10 | [21] |
GmFae2 | n/a | 0 | 0 | 0 | 0 | 0.0007 | 12 | [21] |
AsFaeI | B | 58.85 | 64.22 | 0 | 98.56 | 1.353 | 13 | [21] |
SF a | Query | Subject | Sequence Alignment Results (pBLAST) | Correlation between Primary Sequence Identity and Transesterification Rate b | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Query Cover (%) | Identities (%) | Positives (%) | Gaps (%) | E-Value | PFA | BFA | GFA | AFA | |||
1 | Fae68 | AgFae1 | 96 | 57 | 74 | 3 | 0.0 | 0.9956 | 0.9933 | 0.9955 | 0.9833 |
AsFaeF | 96 | 54 | 71 | 3 | 0.0 | ||||||
AnFaeB | 97 | 52 | 71 | 3 | 0.0 | ||||||
5 | Fae125 | ATEG_Fae | 77 | 57 | 72 | 0 | 6 × 10−109 | 0.9774 | 0.9866 | 0.8199 | 0.9170 |
C1FaeA1 | 82 | 51 | 67 | 1 | 2 × 10−90 | ||||||
AnidFAEC | 77 | 46 | 63 | 6 | 7 × 10−79 | ||||||
C1FaeA2 | 78 | 44 | 61 | 7 | 5 × 10−75 | ||||||
AnFaeC | 77 | 44 | 61 | 6 | 6 × 10−75 | ||||||
AsFaeC | 77 | 43 | 58 | 4 | 3 × 10−73 | ||||||
6 | C1FaeB2 | C1FaeB1 | 100 | 68 | 81 | 0 | 6 × 10−144 | 0.9044 | 0.7886 | 0.8741 | 0.8699 |
AsFaeE | 100 | 48 | 68 | 0 | 4 × 10−99 | ||||||
Fae7262 | 99 | 47 | 64 | 0 | 1 × 10−93 | ||||||
9 | AsFaeG | AnFaeJ | 99 | 46 | 64 | 2 | 7 × 10−173 | 0.6162 | 0.2161 | 0.9925 | - |
CsTan1 | 93 | 37 | 56 | 4 | 1 × 10−100 |
Enzyme | Fae68 | AgFae1 | AsFaeF | AnFaeB | FoFaeC | AwFaeG | C1FaeB2 | C1FaeB1 | Fae7262 | AsFaeE | AnFaeA a |
---|---|---|---|---|---|---|---|---|---|---|---|
SF | 1 | 1 | 1 | 1 | 2 | 2 | 6 | 6 | 6 | 6 | 7 |
Protein size (kDa) | 57.7 | 55.5 | 55.4 | 55.5 | 56.1 | 55.9 | 30.5 | 30.2 | 31.2 | 30.2 | 28.4 |
Protein volume (Å3) | 62,063 | 60,284 | 59,722 | 60,410 | 60,107 | 59,908 | 32,825 | 32,506 | 33,286 | 32,281 | 301,120 |
Catalytic triad (Ser-His-Asp) | 214-469-429 | 187-440-400 | 187-439-399 | 185-437-397 | 201-452-412 | 190-442-402 | 136-275-219 | 137-277-221 | 136-276-220 | 137-277-221 | 133-247-194 |
Molecular Surface (Å2) | |||||||||||
Protein | |||||||||||
Lipophilic (%) | 33.5 | 30.6 | 32.9 | 31.2 | 30.6 | 33.6 | 35.6 | 38.8 | 32.3 | 35.3 | 26.8 |
Non-polar (%) | 40.0 | 36.9 | 39.8 | 38.0 | 38.3 | 40.6 | 44.2 | 47.0 | 47.8 | 43.6 | 32.3 |
Neutral (%) | 42.1 | 41.9 | 36.4 | 42.9 | 35.4 | 39.1 | 44.2 | 37.9 | 54.2 | 38.3 | 48.5 |
Acidic (%) | 11.4 | 11.6 | 14.6 | 13.1 | 12.7 | 12.6 | 11.5 | 8.6 | 6.0 | 16.1 | 16.4 |
Basic (%) | 12.7 | 15.5 | 15.5 | 14.3 | 20.9 | 14.5 | 8.3 | 14.3 | 7.2 | 9.9 | 8.1 |
Distance < 15 Å around the catalytic serine | |||||||||||
Lipophilic (%) | 38.9 | 30.4 | 36.2 | 26.4 | 32.7 | 29.2 | 45.4 | 43.7 | 33.5 | 43.8 | 30.2 |
Non-polar (%) | 48.2 | 38.8 | 43.6 | 38.9 | 43.7 | 38.8 | 56.9 | 53.4 | 41.5 | 51.5 | 37.3 |
Neutral (%) | 42.1 | 49.6 | 43.5 | 49.3 | 43.3 | 46.4 | 47.0 | 38.2 | 52.9 | 36.2 | 44.5 |
Acidic (%) | 8.2 | 7.2 | 11.4 | 14.2 | 9.7 | 10.3 | 5.4 | 3.8 | 4.7 | 6.3 | 12.7 |
Basic (%) | 10.0 | 12.2 | 8.2 | 9.5 | 13.4 | 13.4 | 6.7 | 13.6 | 8.4 | 13.2 | 11.9 |
Lid b | |||||||||||
Lipophilic (%) | 39.2 | 33.5 | 38.1 | 37.7 | 36.9 | 37.0 | - | - | - | - | 16.4 |
Non-polar (%) | 44.7 | 38.1 | 44.4 | 44.7 | 45.5 | 44.1 | 27.6 | ||||
Neutral (%) | 39.9 | 43.7 | 35.9 | 38.0 | 37.8 | 41.5 | 41.3 | ||||
Acidic (%) | 11.9 | 7.8 | 10.8 | 14.1 | 12.2 | 8.6 | 24.1 | ||||
Basic (%) | 8.6 | 15.6 | 14.6 | 9.8 | 12.7 | 12.5 | 1.6 |
Receptor | SF a | Mean Binding Energy of Cluster (kcal/mol) | Highest Binding Energy in Cluster (kcal/mol) | Distance b | Genetic Runs in Cluster c | Residue(s) in Vicinity with Vinyl Moiety in Cluster |
---|---|---|---|---|---|---|
Fae68 | 1 | 6.0457 ± 0.3754 | 6.5580 | 2.823 | 3 | Ile358 |
AgFae1 | 4.6875 ± 0.2963 | 5.3330 | 3.814 | 15 | Gly108 | |
AsFaeF | 5.5160 ± 0.1797 | 5.7610 | 2.842 | 3 | Gly108 | |
AnFaeB | 5.1805 ± 0.1125 | 5.2930 | 2.745 | 2 | Gly106 | |
FoFaeC | 2 | 5.6489 ± 0.3975 | 6.4670 | 4.188 | 8 | Gly122 |
AwFaeG | 5.6604 ± 0.4224 | 6.3690 | 2.953 | 12 | Gly111 | |
C1FaeB1 | 6 | 4.9831 ± 0.2644 | 5.3670 | 2.955 | 8 | Pro57 |
4.7887 ± 0.2200 | 5.0730 | 3.968 | 3 | Leu223 | ||
C1FaeB2 | 5.2065 ± 0.7067 | 6.1220 | 3.969 | 10 | Leu221 | |
4.6880 ± 0.0000 | 4.6880 | 2.567 | 1 | Pro56 | ||
Fae7262 | 4.8974 ± 0.1512 | 5.1510 | 4.387 | 5 | Pro56 | |
AsFaeE | 4.7585 ± 0.1881 | 4.9000 | 2.978 | 4 | Leu59 | |
AnFaeA | 7 | 5.8980 ± 0.6567 | 6.7200 | 5.767 | 4 | Thr68 |
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Antonopoulou, I.; Dilokpimol, A.; Iancu, L.; Mäkelä, M.R.; Varriale, S.; Cerullo, G.; Hüttner, S.; Uthoff, S.; Jütten, P.; Piechot, A.; et al. The Synthetic Potential of Fungal Feruloyl Esterases: A Correlation with Current Classification Systems and Predicted Structural Properties. Catalysts 2018, 8, 242. https://doi.org/10.3390/catal8060242
Antonopoulou I, Dilokpimol A, Iancu L, Mäkelä MR, Varriale S, Cerullo G, Hüttner S, Uthoff S, Jütten P, Piechot A, et al. The Synthetic Potential of Fungal Feruloyl Esterases: A Correlation with Current Classification Systems and Predicted Structural Properties. Catalysts. 2018; 8(6):242. https://doi.org/10.3390/catal8060242
Chicago/Turabian StyleAntonopoulou, Io, Adiphol Dilokpimol, Laura Iancu, Miia R. Mäkelä, Simona Varriale, Gabriella Cerullo, Silvia Hüttner, Stefan Uthoff, Peter Jütten, Alexander Piechot, and et al. 2018. "The Synthetic Potential of Fungal Feruloyl Esterases: A Correlation with Current Classification Systems and Predicted Structural Properties" Catalysts 8, no. 6: 242. https://doi.org/10.3390/catal8060242
APA StyleAntonopoulou, I., Dilokpimol, A., Iancu, L., Mäkelä, M. R., Varriale, S., Cerullo, G., Hüttner, S., Uthoff, S., Jütten, P., Piechot, A., Steinbüchel, A., Olsson, L., Faraco, V., Hildén, K. S., De Vries, R. P., Rova, U., & Christakopoulos, P. (2018). The Synthetic Potential of Fungal Feruloyl Esterases: A Correlation with Current Classification Systems and Predicted Structural Properties. Catalysts, 8(6), 242. https://doi.org/10.3390/catal8060242