Co-Occurrence of Regulated and Emerging Mycotoxins in Corn Silage: Relationships with Fermentation Quality and Bacterial Communities
Abstract
:1. Introduction
2. Results
2.1. Cluster Analysis Results
2.2. Alternaria Produced Mycotoxin in Corn Silages
2.3. Aspergillus Produced Mycotoxin in Corn Silages
2.4. Fusarium Produced Mycotoxin in Corn Silages
2.5. Penicillium Produced Mycotoxin in Corn Silages
2.6. Other Mycotoxigenic Fungi Strain Produced Mycotoxin in Corn Silages
2.7. Corn Silage Characteristics
2.8. Corn Silage Bacterial Communities
3. Discussion
3.1. Corn Silage Clusterization
3.2. Alternaria and Aspergillus Produced Mycotoxins in Corn Silages
3.3. Fusarium Produced Mycotoxins in Corn Silages
3.4. Penicillium Produced Mycotoxins in Corn Silages
3.5. Other Fungi Strain Produced Metabolites in Corn Silages
3.6. Corn Silages Chemical Characterization
3.7. Corn Silage Bacterial Communities
3.7.1. Lactobacillaceae Community in Corn Silages
3.7.2. Acetobacteriaceae Community in Corn Silages
3.7.3. Other Bacterial Family Community in Corn Silages
3.8. Priorities for Future Investigations
4. Conclusions
5. Materials and Methods
5.1. Sample Collection, Preparation and Analysis
5.2. Bacterial Genomic DNA Extraction and Bioinformatics
5.3. Statistical Analyzes
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
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Items | Cluster 1 | Cluster 2 | Cluster 3 | Cluster 4 | Cluster 5 | √MSE | p Value |
---|---|---|---|---|---|---|---|
n = 24 | n = 22 | n = 2 | n = 9 | n = 7 | |||
Counts of mycotoxins | 24.7 | 23.5 | 42.5 | 25.4 | 32.7 | 5.93 | <0.05 |
Aspergillus toxins | 3.1 | 2.6 | 4.0 | 2.2 | 4.1 | 0.99 | <0.05 |
Alternaria toxins | 1.0 | 0.2 | 2.5 | 0.3 | 1.1 | 1.07 | <0.05 |
Zearalenoneand its metabolites | 0.4 | 0.2 | 2.0 | 0.2 | 0.6 | 0.55 | <0.05 |
Trichothecenes type B | 0.8 | 0.7 | 1.5 | 1.0 | 0.9 | 0.56 | 0.256 |
Fumonisins and their metabolites | 4.8 | 5.8 | 6.5 | 6.7 | 7.7 | 1.46 | <0.05 |
Enniatins | 0.8 | 0.3 | 3.5 | 0.2 | 1.0 | 1.18 | <0.05 |
Beauvericin | 0.8 | 1.0 | 1.0 | 1.0 | 1.0 | 0.24 | 0.133 |
Other Fusarium toxins | 6.5 | 6.9 | 11.5 | 7.2 | 8.9 | 1.62 | <0.05 |
Penicillium toxins | 4.6 | 4.5 | 6.5 | 5.4 | 6.3 | 1.10 | <0.05 |
Other fungi toxins | 0.6 | 0.1 | 1.5 | 0.0 | 0.9 | 0.97 | 0.103 |
Unspecified fungi toxins | 0.8 | 0.1 | 3.0 | 0.0 | 0.7 | 0.79 | <0.05 |
Sums of mycotoxins | |||||||
Aspergillus toxins | 147.0 | 84.5 | 565.2 | 70.3 | 186.7 | 104.04 | <0.05 |
Alternaria toxins | 5.8 | 4.4 | 18.7 | 29.6 | 18.7 | 32.67 | 0.308 |
Zearalenoneand its metabolites | 8.8 | 4.0 | 152.8 | 0.5 | 41.4 | 46.27 | <0.05 |
Trichothecenes type B | 28.8 | 15.4 | 192.6 | 33.5 | 57.6 | 41.67 | <0.05 |
FB and their metabolites | 215.4 | 339.1 | 475.3 | 473.5 | 1944.9 | 289.56 | <0.05 |
Enniatins | 0.6 | 0.3 | 3.1 | 0.5 | 5.7 | 4.46 | 0.075 |
Beauvericin | 4.1 | 8.5 | 30.8 | 19.7 | 27.1 | 13.15 | <0.05 |
Other Fusarium toxins | 229.9 | 755.3 | 619.7 | 1564.8 | 675.1 | 172.65 | <0.05 |
Penicillium toxins | 154.6 | 91.6 | 708.2 | 87.3 | 142.2 | 107.34 | <0.05 |
Other fungi toxins | 1.1 | 0.1 | 4.3 | 0.0 | 4.0 | 2.85 | 0.013 |
Unspecified fungi toxins | 17.8 | 1.8 | 102.0 | 0.0 | 26.0 | 23.51 | <0.05 |
Items | Cluster 1 | Cluster 2 | Cluster 3 | Cluster 4 | Cluster 5 | √MSE | p Value |
---|---|---|---|---|---|---|---|
n = 24 | n = 22 | n = 2 | n = 9 | n = 7 | |||
Alternaria mycotoxin count, n | 1 | 0.2 | 2.5 | 0.3 | 1.1 | 1.07 | 0.007 |
Altersetin | 6.8 (20.8) | nd (-) | 6.9 (50.0) | nd (-) | 16.4 (28.6) | 7.4 | 0.358 |
Alternariol | 1.9 (20.8) | nd (-) | 1.2 (100) | nd (-) | nd (-) | 1.41 | 0.659 |
Alternariol, methyl-ether | 1.3 (33.3) | 0.6 (4.5) | 0.9 (100) | nd (-) | 2.9 (14.3) | 0.84 | 0.267 |
Tentoxin | 18.2 (4.2) | 46.2 (9.1) | nd (-) | 88.9 (33.3) | 34.3 (14.3) | 111.55 | 0.929 |
4Z-Infectopyron | 15.6 (16.7) | 3.9 (4.5) | 27.5 (50.0) | nd | 15.3 (57.1) | 12.04 | 0.617 |
Aspergillus mycotoxin count, n | 3.1 | 2.6 | 4 | 2.2 | 4.1 | 0.99 | <0.05 |
Rugulusovin | 65 (100) | 31.1 (100) | 310.7 (100) | 24.6 (100) | 34.7 (100) | 53.56 | <0.05 |
Emodin | 4.9 (50) | 1.6 (31.8) | 7.2 (100) | 1 (11.1) | 3.7 (57.1) | 2.79 | 0.066 |
Brevianamide F | 74.3 (95.8) | 30.6 (95.5) | 246.4 (100) | 40.5 (88.9) | 100.1 (100) | 65.65 | <0.05 |
Kojic acid | 44.1 (16.7) | 104 (22.7) | nd (-) | 83.5 (11.1) | 105.0 (42.9) | 86.31 | 0.734 |
3-Nitropropionic acid | 5.2 (12.5) | 1.3 (4.5) | nd (-) | 2 (11.1) | 6.8 (57.1) | 6.25 | 0.824 |
Averufin | 0.3 (4.2) | nd (-) | nd (-) | nd (-) | nd (-) | - | - |
Bis(methylthio)gliotoxin | nd (-) | nd (-) | nd (-) | nd (-) | 3 (14.3) | - | - |
Asperphenamate | nd (-) | 0.3 (4.5) | nd (-) | nd (-) | 1.7 (14.3) | - | - |
Items | Cluster 1 | Cluster 2 | Cluster 3 | Cluster 4 | Cluster 5 | √MSE | p Value |
---|---|---|---|---|---|---|---|
n = 24 | n = 22 | n = 2 | n = 9 | n = 7 | |||
Fumonisins mycotoxins count, n | 4.8 | 5.7 | 6.5 | 6.7 | 7.7 | 1.46 | <0.05 |
Fumonisin B1 2 | 155 (95.8) | 228.7 (100) | 181.8 (100) | 321.9 (100) | 1382.2 (100) | 216.24 | <0.05 |
Fumonisin B2 2 | 36.6 (95.8) | 67.7 (95.5) | 139.1 (100) | 96.1 (100) | 285 (100) | 74.58 | <0.05 |
Fumonisin B3 | 16.3 (75) | 19.1 (100) | 69 (100) | 28.2 (100) | 149.6 (100) | 39.05 | <0.05 |
Fumonisin B4 | 10.1 (70.8) | 17 (95.5) | 28.9 (100) | 14.9 (100) | 68.6 (100) | 21.14 | <0.05 |
Fumonisin B6 | 2.9 (8.3) | 4.2 (13.6) | nd (-) | 2.5 (22.2) | 4.2 (71.4) | 1.73 | 0.607 |
Fumonisin A1 | 4 (54.2) | 4.4 (77.3) | 9.9 (100) | 4.5 (100) | 18.1 (100) | 6.78 | <0.05 |
Fumonisin A2 | 2.5 (16.7) | 4.3 (40.9) | 5.6 (50) | 2.9 (66.7) | 12.4 (100) | 3.45 | <0.05 |
Masked Fumonisin A1 | 16.3 (58.3) | 8.8 (54.5) | 43.8 (100) | 7 (77.8) | 26 (100) | 13.66 | <0.05 |
Zearalenone metabolites count, n | 0.4 | 0.2 | 2 | 0.2 | 0.6 | 0.55 | 0.001 |
Zearalenone 2 | 4.1 (29.2) | 22 (18.2) | 7.1 (100) | 2.5 (22.2) | 1.7 (42.9) | 19.04 | 0.579 |
Zearalenone-sulfone | 91.2 (8.3) | nd (-) | 145.7 (100) | nd (-) | 284.9 (14.3) | 132.85 | 0.584 |
Trichothecenes type-B count, n | 0.8 | 0.7 | 1.5 | 1 | 0.9 | 0.56 | 0.256 |
Deoxynivalenol 2 | 38.4 (62.5) | 22.6 (68.2) | 151.7 (100) | 33.5 (100) | 73.8 (71.4) | 41.69 | 0.002 |
Nivalenol | 55 (8.3) | nd (-) | 81.9 (50) | nd (-) | 34.4 (14.3) | 27.73 | 0.635 |
Deoxynivalenol-3-glucoside | 6.7 (4.2) | nd | nd | nd | nd | - | - |
other Fusarium mycotoxins count, n | 6.5 | 6.9 | 11.5 | 7.2 | 8.9 | 1.62 | <0.05 |
Siccanol | 30 (58.3) | 464.4 (100) | 210 (100) | 1269.2 (100) | 255.8 (100) | 208.26 | <0.05 |
Monocerin | 3.9 (16.7) | 5.4 (40.9) | 19.9 (100) | 5.2 (33.3) | 3.3 (57.1) | 6.726 | 0.088 |
Moniliformin | 10.9 (95.8) | 9 (95.5) | 39.9 (100) | 16.8 (100) | 39 (100) | 16.53 | <0.05 |
Equisetin | 8.7 (91.7) | 17.7 (90.9) | 141.1 (100) | 5.4 (100) | 8.9 (100) | 29.09 | <0.05 |
Epiequisetin | 8.4 (79.2) | 15.1 (90.9) | 123.4 (100) | 5.1 (100) | 9.4 (100) | 24.48 | <0.05 |
Culmorin | 25.7 (42.7) | 14.3 (50) | 47.5 (100) | 14.6 (55.6) | 44.2 (71.4) | 19.46 | <0.05 |
15-Hydroxyculmorin | 4.7 (4.2) | nd (-) | nd (-) | nd (-) | nd (-) | - | - |
Butenolide | 12.9 (33.3) | nd (-) | 17.8 (50) | nd (-) | 17.9 (28.6) | 1.92 | <0.05 |
Bikaverin | 10 (91.7) | 18.1 (90.9) | 19.4 (100) | 15.2 (100) | 49.4 (100) | 12.75 | <0.05 |
Apicidin | nd (-) | nd (-) | 4.2 (50) | nd (-) | 1.3 (14.3) | - | - |
Antibiotic Y | 11 (12.5) | 1.3 (4.5) | 15.1 (50) | nd (-) | 18.5 (28.6) | 15.7 | 0.833 |
7-Hydroxykaurenolide | 2 (8.3) | 2.4 (4.5) | 7.8 (100) | nd (-) | 3.5 (14.3) | 4.76 | 0.681 |
Aurofusarin | 8.5 (16.7) | 7 (22.7) | 5.5 (100) | 6.3 (33.3) | 6 (71.4) | 5.68 | 0.963 |
Fusaric acid | 159.3 (100) | 225.0 (100) | 195.5 (100) | 241 (100) | 263.7 (100) | 155.94 | 0.428 |
Enniatins-Beauvericin count, n | 1.7 | 1.3 | 4.5 | 1.2 | 2 | 1.21 | <0.05 |
Enniatin A | 3.2 (8.3) | 0.4 (4.5) | nd (-) | nd (-) | nd (-) | 4.03 | 0.676 |
Enniatin A1 | 0.3 (12.5) | 0.5 (4.5) | 0.3 (100) | nd (-) | 0.6 (14.3) | 0.09 | 0.176 |
Enniatin B | 0.6 (33.3) | 0.9 (9.1) | 0.8 (100) | 2.6 (11.1) | 3.7 (28.6) | 1.44 | 0.15 |
Enniatin B1 | 1 (29.2) | 2.2 (9.1) | 1.5 (100) | 1.8 (11.1) | 15.2 (28.6) | 6.69 | 0.202 |
Enniatin B2 | nd (-) | nd (-) | 0.9 (50) | nd (-) | 0.6 (28.6) | 0.33 | 0.562 |
Beauvericin | 4.9 (83.3) | 8.5 (100) | 30.8 (100) | 19.7 (100) | 27.2 (100) | 13.57 | p < 0.05 |
Items | Cluster 1 | Cluster 2 | Cluster 3 | Cluster 4 | Cluster 5 | √MSE | p Value |
---|---|---|---|---|---|---|---|
n = 24 | n = 22 | n = 2 | n = 9 | n = 7 | |||
Penicillium mycotoxins count, n | 4.6 | 4.5 | 6.5 | 5.4 | 6.3 | 1.1 | 0.001 |
Skyrin | nd (-) | nd (-) | nd (-) | nd (-) | 6.2 (14.3) | - | - |
Asperglaucide | nd (-) | nd (-) | nd (-) | 1.2 (11.1) | nd (-) | - | - |
Secalonic acid | 4.1 (29.2) | 5.3 (50) | nd (-) | 7.3 (33.3) | 17.9 (57.1) | 10.78 | 0.214 |
7-Hydroxypestalonic | 1.2 (4.2) | 1.4 (22.7) | nd (-) | 1.7 (44.4) | 2.6 (28.6) | 0.42 | 0.045 |
Chlorocitreorosein | nd (-) | nd (-) | 1.3 (50) | nd (-) | nd (-) | - | - |
Pestalotin | 3.4 (45.8) | 3.9 (27.3) | 26.5 (100) | 3 (100) | 5.2 (85.7) | 4.29 | - |
Oxaline | 5.7 (62.5) | 8 (63.6) | 3.8 (100) | 4.8 (55.6) | 9.9 (85.7) | 5.23 | 0.314 |
Flavoglaucin | 10.4 (8.3) | 2.5 (9.1) | nd (-) | nd (-) | nd (-) | 9.46 | 0.488 |
Cyclopenin | 1 (25) | nd (-) | 1 (100) | nd (-) | nd (-) | 0.58 | 0.972 |
Fellutanine A | 109.1 (100) | 54 (100) | 577.6 (100) | 49.9 (100) | 55.5 (100) | 79.6 | - |
Mycophenolic acid | 5.7 (4.2) | nd (-) | nd (-) | nd (-) | 43.5 (28.6) | 21.52 | 0.388 |
Mycophenolic acid IV | 0.5 (4.2) | nd (-) | nd (-) | nd (-) | 2.3 (28.6) | 2.09 | 0.6 |
Phenopyrrozin | 23.3 (100) | 18.1 (95.5) | 47.1 (100) | 10 (100) | 15.6 (100) | 24.67 | 0.339 |
Questiomycin A | 18.3 (79.2) | 12.7 (86.4) | 51.7 (100) | 18.4 (100) | 33.2 (100) | 17.67 | 0.015 |
Metabolites from different fungal strains count, n | 0.6 | 0.1 | 1.5 | - | 0.9 | 0.97 | 0.103 |
Ilicicolin A | 0.8 (4.2) | 0.3 (4.5) | nd (-) | nd (-) | nd (-) | - | - |
Ilicicolin B | 1.1 (4.2) | nd (-) | nd (-) | nd (-) | 1.7 (14.3) | - | - |
Citreorosein | 3.4 (12.5) | nd (-) | 3.9 (50) | nd (-) | 4.6 (28.6) | 1.74 | 0.775 |
Ascochlorin | 1.3 (20.8) | 1.4 (4.5) | 3.9 (50) | nd (-) | 7.7 (14.3) | 0.88 | 0.011 |
Bassianolide | 5.2 (4.2) | nd (-) | nd (-) | nd (-) | 6.3 (14.3) | - | - |
Ascofuranone | 0.5 (12.5) | 0.4 (4.5) | 0.8 (50) | nd (-) | 3.2 (14.3) | 0.24 | 0.028 |
Macrosporin | 1.5 (12.5) | nd (-) | nd (-) | nd (-) | nd (-) | - | - |
Unspecific Metabolites count, n | 0.8 | 0.1 | 3 | nd | 0.7 | 0.79 | <0.05 |
Iso-rhodoptilometrin | 0.8 (33.3) | 1.1 (4.5) | 1.8 (100) | nd (-) | 0.8 (28.6) | 0.63 | 0.294 |
Norlichexanthone | 1 (8.3) | nd (-) | 2 (100) | nd (-) | 5.4 (14.3) | 0.64 | 0.059 |
Items | Cluster 1 | Cluster 2 | Cluster 3 | Cluster 4 | Cluster 5 | √MSE | p Value |
---|---|---|---|---|---|---|---|
n = 24 | n = 22 | n = 2 | n = 9 | n = 7 | |||
Chemical parameters (% DM) | |||||||
DM (% fresh matter) | 34.7 | 34.3 | 37.9 | 33.5 | 31.3 | 4.56 | 0.342 |
Ash | 5.7 | 5.7 | 5.7 | 6.0 | 5.8 | 0.53 | 0.553 |
CP | 8.1 | 8.2 | 7.7 | 8.4 | 8.9 | 0.87 | 0.230 |
EE | 2.9 | 3.0 | 3.0 | 2.8 | 3.0 | 0.21 | 0.351 |
NDF | 37.7 | 37.1 | 35.5 | 39.0 | 36.9 | 2.40 | 0.180 |
ADF | 25.2 | 24.7 | 23.3 | 25.8 | 24.7 | 1.86 | 0.389 |
ADL | 2.8 | 2.9 | 3.2 | 3.1 | 3.0 | 0.32 | 0.281 |
NDIP | 1.1 | 1.1 | 0.8 | 1.1 | 1.0 | 0.25 | 0.507 |
ADIP | 0.8 | 0.8 | 0.6 | 0.7 | 0.8 | 0.16 | 0.441 |
24 h NDFD (% NDF) | 52.1 | 50.9 | 47.6 | 51.9 | 50.7 | 3.19 | 0.303 |
Starch | 31.2 | 31.5 | 36.1 | 28.7 | 30.2 | 3.44 | 0.067 |
Fermentative parameters (% DM) | |||||||
pH (dmnl) | 3.67 | 3.76 | 3.84 | 4.02 | 3.83 | 0.331 | 0.156 |
Acetic acid | 3.42 | 2.87 | 3.28 | 2.54 | 3.82 | 1.30 | 0.223 |
Propionic acid | 0.14 | 0.13 | 0.04 | 0.17 | 0.41 | 0.19 | <0.05 |
Butyric acid | 0.008 | 0.003 | 0.001 | 0.005 | 0.006 | 0.011 | 0.750 |
Lactic acid | 3.29 | 4.02 | 1.91 | 3.06 | 3.78 | 1.612 | 0.246 |
Lactic to Acetic | 1.2 | 2.2 | 0.6 | 1.5 | 1.1 | 1.70 | 0.273 |
Ethanol | 0.6 | 0.5 | 0.6 | 0.6 | 0.3 | 0.48 | 0.779 |
Lactic to (Acetic/Ethanol) | 0.91 | 1.78 | 0.50 | 1.30 | 0.99 | 1.57 | 0.376 |
1,2 propanediol | 0.60 | 0.49 | 0.73 | 0.50 | 0.17 | 0.289 | <0.05 |
N-NH3 (% TN) | 11.38 | 11.71 | 7.78 | 7.85 | 13.58 | 7.737 | 0.569 |
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Gallo, A.; Ghilardelli, F.; Atzori, A.S.; Zara, S.; Novak, B.; Faas, J.; Fancello, F. Co-Occurrence of Regulated and Emerging Mycotoxins in Corn Silage: Relationships with Fermentation Quality and Bacterial Communities. Toxins 2021, 13, 232. https://doi.org/10.3390/toxins13030232
Gallo A, Ghilardelli F, Atzori AS, Zara S, Novak B, Faas J, Fancello F. Co-Occurrence of Regulated and Emerging Mycotoxins in Corn Silage: Relationships with Fermentation Quality and Bacterial Communities. Toxins. 2021; 13(3):232. https://doi.org/10.3390/toxins13030232
Chicago/Turabian StyleGallo, Antonio, Francesca Ghilardelli, Alberto Stanislao Atzori, Severino Zara, Barbara Novak, Johannes Faas, and Francesco Fancello. 2021. "Co-Occurrence of Regulated and Emerging Mycotoxins in Corn Silage: Relationships with Fermentation Quality and Bacterial Communities" Toxins 13, no. 3: 232. https://doi.org/10.3390/toxins13030232
APA StyleGallo, A., Ghilardelli, F., Atzori, A. S., Zara, S., Novak, B., Faas, J., & Fancello, F. (2021). Co-Occurrence of Regulated and Emerging Mycotoxins in Corn Silage: Relationships with Fermentation Quality and Bacterial Communities. Toxins, 13(3), 232. https://doi.org/10.3390/toxins13030232