The Metabolite Profiling of Aspergillus fumigatus KMM4631 and Its Co-Cultures with Other Marine Fungi
Abstract
:1. Introduction
2. Materials and Methods
2.1. General
2.2. Fungal Strains
2.3. DNA Extraction and Amplification
2.4. Phylogenetic Analysis
2.5. Cultivation of Fungi
2.6. Extraction and HPLC MS Analysis
2.6.1. Extraction of Fungal Cultures
2.6.2. HPLC MS Analysis of Fungal Extracts
2.6.3. UHPLC-Q-TOF Data Analysis
2.7. Principal Component Analysis (PCA)
2.8. Bioassays
2.8.1. Urease Inhibition Assay
2.8.2. DPPH Radical Scavenger Assay
2.8.3. Cell Culture
2.8.4. Cell Viability Assay
2.8.5. Statistical Data Evaluation
3. Results
3.1. Molecular Identification of the Fungal Strain
3.2. Aspergillus fumigatus KMM 4631 Monoculture Metabolites
3.3. Aspergillus fumigatus KMM 4631 and Penicilliun hispanicum KMM 4689 Co-Culture Metabolites
3.4. Aspergillus fumigatus KMM 4631 and Amphichorda sp. KMM 4639 Co-Culture Metabolites
3.5. Aspergillus fumigatus KMM 4631 and Penicillium sp. KMM 4672 Co-Culture Metabolites
3.6. Aspergillus fumigatus KMM 4631 and Asteromyces cruciatus KMM 4696 Co-Culture Metabolites
3.7. PCA Analysis of the HPLC MS Chromatograms of Fungal Extracts
3.8. Influence of Co-Cultivation on the Biological Activity of Fungal Extracts
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
N | Name | Structure | RT | Exact Mass (Measured) | Exact Mass (Calcd) | Δ, ppm | Score | |
---|---|---|---|---|---|---|---|---|
1 | Af | verruculogen | 15.0 | 512.2414 [M+H]+ | 512.2391 | 4.5 | ||
2 | Af AfAs AfAc | fumitremorgin C | 10.1 | 380.1971 [M+H]+ | 380.1969 | 0.5 | ||
3 | Af AfAs | fumiquinazoline C | 9.0 | 444.1671 [M+H]+ | 444.1666 | 1.1 | ||
4 | Af AfAs | fumiquinazoline D | 9.2 | 444.1671 [M+H]+ | 444.1666 | 1.1 | 0.95 a | |
5 | Af AfAs AfPs AfAc | tryptoquivaline J | 8.0 | 403.1396 [M+H]+ | 403.1401 | −1.2 | ||
6 | Af AfAs AfAc | fumiquinazoline K | 10.2 | 357.1338 [M+H]+ | 357.1346 | −2.2 | ||
7 | Af | spirotriprostatin A | 10.4 | 396.1920 [M+H]+ | 396.1918 | 0.5 | ||
8 | Af AfAs AfAc | 6- methoxyspirotriprostatin B | 7.6 | 394.1754 [M+H]+ | 394.1761 | −1.8 | ||
9 | Af AfAs AfAc | tryptoquivaline F | 7.8 | 403.1396 [M+H]+ | 403.1401 | −1.2 | ||
10 | Af AfAs | fumiquinazoline F | 8.7 | 359.1494 [M+H]+ | 359.1503 | −2.5 | 0.83 a | |
11 | Af AfAs AfAc | pseurotin A | 7.1 | 432.1652 [M+H]+ | 432.1653 | −0.2 | 0.76 a, 0.95 b | |
12 | Af AfPh AfAs AfPs AfAc | conjugated linoleic acid (10E, 12Z) | 18.4 | 281.2487 | 281.2475 | 4.3 | 0.74 a | |
13 | Af Ph AfPh AfPs | 2-chloroemodin | 13.8 | 305.0200 | 305.0211 | −3.6 | 1.00 b | |
14 | Af AfPh AfAs AfPs AfAc | scytalone | 3.2 | 195.0649 | 195.0652 | −1.5 | 0.84 b | |
15 | Af AfAs AfPs AfAc | pseurotin D | 7.2 | 432.1650 | 432.1653 | −0.7 | 1.00 b | |
16 | Af AfPh AfAs AfPs AfAc | agroclavine | 4.8 | 239.1519 | 239.1543 | −10.4 | 1.00 b | |
17 | Af AfAs AfPs | fumigaclavine A | 4.4 | 299.1749 | 299.1754 | −1.7 | 1.00 b | |
18 | Af AfAs AfPs AfAc | pyripyropene A | 11.9 | 584.2507 | 584.2490 | 2.9 | 1.00 b | |
19 | Af AfAs AfPs AfAc | fumiquinazoline G | 9.4 | 359.1480 | 359.1503 | −6.4 | 0.80 b | |
20 | Af, Ph As, Ps Ac AfPh AfAs AfPs AfAc | ergosterol peroxide | 20.4 | 429.3348 | 429.3363 | −3.5 | 0.85 a | |
24 | Ph AfPh | 16α-hydroxy-17β-methoxy-deoxydihydroisoaustamide | 7.3 | 396.1921 [M+H]+ | 396.1918 | 0.8 | ||
25 | Ph AfPh | 16β-hydroxy-17α-methoxy-deoxydihydroisoaustamide | 7.3 | 396.1921 [M+H]+ | 396.1918 | 0.8 | ||
26 | Ph AfPh | 16α-hydroxy-17α-methoxy-deoxydihydroisoaustamide | 7.3 | 396.1921 [M+H]+ | 396.1918 | 0.8 | ||
27 | Ph AfPh | 16,17-dihydroxy-deoxydihydroisoaustamide | 6.2 | 382.1748 [M+H]+ | 382.1761 | −3.4 | ||
28 | Ph AfPh | 16β,17α-dihydroxy-deoxydihydroisoaustamide | 6.0 | 382.1748 [M+H]+ | 382.1761 | −3.4 | ||
29 | Ph AfPh | 16α,17α-dihydroxy-deoxydihydroisoaustamide | 6.6 | 382.1748 [M+H]+ | 382.1761 | −3.4 | ||
30 | Ph AfPh | 3β-hydroxydeoxyisoaustamide | 2.9 | 364.1655 [M+H]+ | 364.1656 | −0.3 | ||
31 | Ph AfPh | deoxy-14,15-dehydroisoaustamide | 10.8 | 346.1544 [M+H]+ | 346.1550 | −1.7 | ||
32 | Ph AfPh | (+)-deoxyisoaustamide | 7.7 | 348.1713 [M+H]+ | 348.1707 | 1.7 | ||
33 | Ph AfPh | desoxybrevianamide E | 9.6 | 352.2019 [M+H]+ | 352.2020 | −0.3 | ||
34 | Ph AfPh | brevianamide F | 5.0 | 284.1388 [M+H]+ | 284.1394 | −2.1 | ||
35 | Ph AfPh | austamide | 5.3 | 364.1635 [M+H]+ | 364.1656 | −5.8 | 0.97 a | |
36 | Ph AfPh | citreorosein | 8.8 | 287.0539 [M+H]+ | 287.0550 | −3.8 | ||
37 | Ph AfPh | 2-chlorocitreorosein | 10.2 | 321.015 [M+H]+ | 321.0160 | −3.1 | ||
38 | Ph AfPh | endocrocin | 8.1 | 315.0488 [M+H]+ | 315.0499 | −3.5 | 0.86 a | |
21 | Ph AfPh AfAc | emodin | 13.0 | 271.0605 | 271.0601 | 1.5 | 0.95 b | |
39 | Ph AfPh | nephrolaevigatin A | 15.5 | 579.0665 [M+H]+ | 579.0608 | 9.8 | ||
40 | Ph AfPh | nephrolaevigatin B | 15.7 | 579.0626 [M+H]+ | 579.0608 | 3.1 | ||
41 | Ph AfPh | nephrolaevigatin C | 15.3 | 545.1005 [M+H]+ | 545.0998 | −1.3 | ||
42 | AfPh | nephrolaevigatin D | 15.0 | 545.0992 [M+H]+ | 545.0998 | −1.1 | ||
43 | Ph AfPh | 7-hydroxy-3-(2-hydroxypropyl)-5-methylisochromen-1-one | 5.2 | 235.0949 [M+H]+ | 235.0965 | −6.8 | ||
44 | AfPh | 3,4-dimethoxycinnamic acid | 4.9 | 209.0805 [M+H]+ | 209.0804 | 0.5 | ||
45 | As AfAs | oxirapentyn B | 9.7 | 335.1487 [M+H]+ | 335.1489 | −0.6 | ||
46 | As AfAs | oxirapentyn E | 7.2 | 275.1279 [M-H2O+H]+ | 275.1278 | 0.4 | ||
47 | As AfAs | oxirapentyn F | 7.1 | 353.1587 [M+H]+ | 353.1595 | −2.3 | ||
48 | AfAs | oxirapentyn G | 2.2 | 311.1504 [M+H]+ | 311.1489 | 4.8 | ||
49 | As AfAs | oxirapentyn H | 2.9 | 371.1704 [M+H]+ | 371.1700 | 1.1 | ||
50 | As AfAs | oxirapentyn I | 2.9 | 371.1704 [M+H]+ | 371.1700 | 1.1 | ||
51 | As AfAs | oxirapentyn J | 6.2 | 353.1587 [M+H]+ | 353.1595 | −2.3 | ||
52 | As AfAs | isariketide A | 5.7 | 313.0910 [M+H]+ | 313.0918 | −2.6 | ||
53 | As AfAs | acremine S | 3.7 | 207.1014 [M+H]+ | 207.1016 | −1.0 | ||
54 | As AfAs | diorcin | 10.4 | 231.1009 [M+H]+ | 231.1016 | −3.0 | ||
55 | As AfAs | isaridin E | 13.7 | 656.4010 [M+H]+ | 656.4018 | −1.2 | 0.81 a | |
56 | As AfAs | isaridin B | 13.5 | 596.3997 [M+H]+ | 596.4018 | −3.5 | ||
57 | As AfAs | isarfelin A | 14.0/14.1 | 670.4187 [M+H]+ | 670.4174 | 1.9 | ||
58 | As AfAs | isariin | 16.0 | 638.4495 [M+H]+ | 638.4487 | 1.3 | ||
59 | AfAs | isariin C | 11.8 | 568.3692 [M+H]+ | 568.3705 | −2.3 | ||
60 | As AfAs | psuedodestruxin C | 14.0/14.1 | 670.4187 [M+H]+ | 670.4174 | 1.9 | ||
61 | As AfAs | desmethylisaridin E | 12.8/13.2 | 642.3870 [M+H]+ | 642.3861 | 1.4 | ||
62 | As AfAs | isaridin F | 12.8/13.2 | 642.3870 [M+H]+ | 642.3861 | 1.4 | ||
63 | As AfAs | 1,4a-dimethyl-9-oxo-7-propan-2-yl-3,4,10,10a-tetrahydro-2H-phenanthrene-1-carboxylic acid | 14.4 | 315.1947 [M+H]+ | 315.1955 | −2.5 | 0.96 a | |
64 | As | viridicatol | 7.5 | 254.0795 [M+H]+ | 254.0812 | −6.7 | 0.77 a | |
65 | AfAs | isariin D | 9.7 | 540.3395 [M+H]+ | 540.3392 | −0.6 | ||
66 | Ps AfPs | quinolactacide | 5.4 | 237.0670 [M+H]+ | 237.0659 | 4.6 | ||
67 | Ps AfPs | 3,5-dimethyl-8-methoxy-3,4-dihydro-1H-isochromene-6-ol | 8.7 | 209.1175 [M+H]+ | 209.1172 | 1.4 | ||
68 | Ps AfPs | anserinone B | 4.6 | 193.0856 [M−H2O+H]+ | 193.0859 | −1.6 | ||
69 | Ps | formylanserinone B | 7.5 | 239.0913 [M+H]+ | 239.0914 | −0.4 | ||
70 | Ps AfPs | (6-methyl curvulinic acid | 5.3 | 207.0651 [M−H2O+H]+ | 207.0652 | −0.5 | ||
71 | Ps AfPs | 4-methoxyisoquinolin-1(2H)-one | 2.6 | 176.0702 [M+H]+ | 176.0706 | −2.3 | ||
72 | Ps AfPs | N,N-diethyl-3-methylbenzamide | 9.7 | 192.1390 [M+H]+ | 192.1383 | 3.6 | ||
73 | Ps AfPs | 4-hydroxy-3,6-dimethyl-2-pyrone | 2.7 | 141.0548 [M+H]+ | 141.0546 | 1.4 | ||
74 | Ps AfPs | hydroxy-N-acetyl-β-oxotriptamine | 2.4 | 233.0925 [M+H]+ | 233.0921 | 1.7 | ||
75 | Ps AfPs | citriperazine D | 4.4 | 339.0979 [M−H2O+H]+ | 339.0976 | 0.9 | ||
76 | Ps AfPs | pretrichodermamide C | 5.4 | 513.0988 [M+H]+ | 513.1996 | −1.6 | ||
77 | Ps AfPs | N-methylpretrichodermamide B | 8.1 | 531.0662 [M+H]+ | 531.0657 | 0.9 | ||
78 | Ps AfPs | pretrichodermamide D | 5.9 | 513.0988 [M+H]+ | 513.0996 | −1.6 | ||
79 | Ps AfPs | 4-hydroxyscytalone | 2.2 | 211.0603 [M+H]+ | 211.0601 | 1.0 | ||
80 | Ps AfPs | 4-hydroxy-6-dehydroxyscytalone | 3.0 | 195.0654 [M+H]+ | 195.0652 | 1.0 | ||
81 | AfPs | 3-methylorsellinic acid | 2.6 | 183.0659 | 183.0652 | 3.8 | ||
82 | Ac | acruciquinone A | 6.4 | 277.1063 [M+H]+ | 277.1071 | −2.9 | ||
83 | Ac | acruciquinone C | 4.6 | 279.1226 [M+H]+ | 279.1227 | −0.4 | ||
84 | Ac | pleosporon | 3.8 | 291.0853 [M+H]+ | 291.0863 | −3.4 | ||
85 | Ac | coniothyrinone D | 4.9 | 279.1226 [M+H]+ | 279.1227 | −0.4 | ||
86 | Ac | coniothyrinone B | 7.0 | 263.1272 [M+H]+ | 263.1278 | −2.3 | ||
87 | Ac | rubrumol | 5.2 | 277.1062 [M+H]+ | 277.1071 | −3.2 | ||
88 | Ac | 9,10-anthracenedione | 10.1 | 255.0652 [M+H]+ | 255.0652 | 0 | ||
89 | Ac AfAc | trans-3,4-dihydroxy-3,4-dihydroanofinic acid | 4.9 | 239.0895 [M+H]+ | 239.0914 | −8.0 | ||
90 | Ac | quadricinctapyran A | 7.8 | 221.0819 [M+H]+ | 221.0808 | 5.0 | ||
91 | Ac AfAc | 7-hydroxymethyl-1,2-naphthalenediol | 6.2 | 191.0707 [M+H]+ | 191.0703 | 2.1 | ||
92 | Ac | gliovictin | 8.3 | 355.1160 [M+H]+ | 355.1145 | 4.2 | ||
93 | Ac | acrucipentyn A | 4.1 | 231.0777 [M+H]+ | 231.0782 | −2.2 | ||
94 | Ac AfAc | indolelactic acid | 4.6 | 206.0810 [M+H]+ | 206.0812 | −1.0 | 0.98 a | |
22 | AfAc | cyclotryprostatin B | 7.3 | 426.2035 [M+H]+ | 426.2024 | 2.6 | ||
23 | AfAc | bisdethiobis(methylthio)gliotoxin | 7.4 | 357.0936 [M+H]+ | 357.0937 | −0.3 |
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Species | Strain Number | GenBank Accession Number | |||
---|---|---|---|---|---|
ITS | BenA | CaM | RPB2 | ||
Aspergillus takakii | CBS 137454T | MN431378 | AB787221 | AB787566 | MN969097 |
Aspergillus laciniosus | CBS 117721T | AB299413 | AY870756 | AY870716 | MN969080 |
Aspergillus spinosus | CBS 483.65T | EF669988 | EF669844 | EF669914 | EF669775 |
Aspergillus fumisynnematus | CBS 141446T | AB250779 | AB248076 | AB259968 | MN969073 |
Aspergillus lentulus | CBS 117885T | EF669969 | EF669825 | EF669895 | EF669756 |
Aspergillus fumigatiaffinis | CBS 117186T | MN431367 | DQ094885 | DQ094891 | MN969072 |
Aspergillus oerlinghausenensis | CBS 139183T | KT359601 | KT359603 | KT359605 | MN969162 |
Aspergillus fumigatus | CBS 133.61T | EF669931 | EF669791 | EF669860 | EF669719 |
Aspergillus fumigatus | KMM 4631 | OR578448 | OQ466614 | OR600992 | OR600993 |
Aspergillus fischeri | CBS 544.65T | EF669936 | EF669796 | EF669865 | EF669724 |
Aspergillus novofumigatus | CBS 117520T | MN431372 | DQ094886 | DQ094893 | MN969083 |
Talaromyces marneffei | CBS 388.87T | JN899344 | JX091389 | KF741958 | KM023283 |
Fungal Culture | Sample Code | Mass of Crude Extract, mg |
---|---|---|
Aspergillus fumigatus KMM 4631 | Af | 21.1 |
Aspergillus fumigatus KMM 4631+ Amphichorda sp. KMM 4639 | AfAs | 14.5 |
Amphichorda sp. KMM 4639 | As | 12.7 |
Aspergillus fumigatus KMM 4631+ Penicillium sp. KMM 4672 | AfPs | 87.0 |
Penicillium sp. KMM 4672 | Ps | 102.1 |
Aspergillus fumigatus KMM 4631+ Penicillium hispanicum KMM 4689 | AfPh | 365.0 |
Penicillium hispanicum KMM 4689 | Ph | 233.1 |
Aspergillus fumigatus KMM 4631+ Asteromyces cruciatus KMM 4696 | AfAc | 39.5 |
Asteromyces cruciatus KMM 4696 | Ac | 56.3 |
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Yurchenko, A.N.; Nesterenko, L.E.; Popov, R.S.; Kirichuk, N.N.; Chausova, V.E.; Chingizova, E.A.; Isaeva, M.P.; Yurchenko, E.A. The Metabolite Profiling of Aspergillus fumigatus KMM4631 and Its Co-Cultures with Other Marine Fungi. Metabolites 2023, 13, 1138. https://doi.org/10.3390/metabo13111138
Yurchenko AN, Nesterenko LE, Popov RS, Kirichuk NN, Chausova VE, Chingizova EA, Isaeva MP, Yurchenko EA. The Metabolite Profiling of Aspergillus fumigatus KMM4631 and Its Co-Cultures with Other Marine Fungi. Metabolites. 2023; 13(11):1138. https://doi.org/10.3390/metabo13111138
Chicago/Turabian StyleYurchenko, Anton N., Liliana E. Nesterenko, Roman S. Popov, Natalya N. Kirichuk, Viktoria E. Chausova, Ekaterina A. Chingizova, Marina P. Isaeva, and Ekaterina A. Yurchenko. 2023. "The Metabolite Profiling of Aspergillus fumigatus KMM4631 and Its Co-Cultures with Other Marine Fungi" Metabolites 13, no. 11: 1138. https://doi.org/10.3390/metabo13111138