Current Status and Future Opportunities of Omics Tools in Mycotoxin Research
Abstract
:1. Introduction
2. Metabolomics Approach
Analytical Techniques Used in Mycotoxin Metabolomics Studies
3. Genomics Approach
Genomics Analysis for Mycotoxin Producing Fungi
4. Transcriptomics Approach
Transcriptional Profiling
5. Proteomics Approach
6. The Current Status of Omics Studies and Future Opportunities
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Mycotoxin | Structure | Fungal Species | IARC Classification | Ref. |
---|---|---|---|---|
Aflatoxin B1 | Aspergillus flavus, Aspergillus parasiticus, Aspergillus bombycis, Aspergillus A. coracles, Aspergillus nomius, Aspergillus pseudotamari | Group A carcinogen | [1,13,15,16,17] | |
Ochratoxin A | Aspergillus alliaceus, Aspergillus melleus, Aspergillus cabonarius, Aspergillus glaucus, Aspergillus niger, Penicillium viridicatum | Group 2B possible human carcinogen | [13,18,26] | |
Patulin | Penicillium expansum, Penicillium patulum, Penicillium crustosum | Group 3 | [19,25] |
Toxin | Crops | Detection Techniques (Targeted or Non-Targeted) | LoD * | LoQ * | Ref. |
---|---|---|---|---|---|
AFB1, G1 | Peanuts, corn, soy beans | Targeted and Non-targeted HPLC-ESI-MS-qTOF, ESI+ UHPLC-ESI-MS/MS, sSRM | 0.1–0.3 µg/kg | 0.2–0.9 µg/kg | [50] |
AFB1, B2, G1, G2, M1, OTA | Feed and feed raw materials (silage, maize, wheat, wheat by-products, barley, soy beans, sunflower seeds) | Targeted and Non-targeted LC-ESI-MS/MS (QTRAP) ESI+, ESI−, sSRM | n/a | n/a | [72] |
AFB1, B2, G1, G2, M1, M2, OTA, OTB, Patulin | Almonds, hazelnuts, peanuts, pistachio | Targeted UHPLC-ESI-MS/MS (qQq), ESI+, ESI−, sSRM | n/a | AFB1 3.0 µg/kg AFB2 10.0 µg/kg AFG1 10.0 µg/kg AFG2 8.2 µg/kg AFM1 7.9 µg/kg OTA 15.0 µg/kg OTB 9.9 µg/kg PAT n/a | [53] |
AFB1, B2, G1, G2, OTA | Barley | Targeted GC-MS/MS (qQq), EI, derivatizied, LC-ESI-MS/MS (QTRAP), ESI | AFs 2.0 ng/kg OTA 2.0 ng/kg | AFs 3.5 ng/kg OTA 3.5 ng/kg | [58] |
AFB1, B2, G1, G2 | Rice, sorghum | Targeted LC-ESI-MS/MS or UHPLC-ESI-MS/MS (tandem quadrupole), ESI+, sSRM | 0.1–1.0 µg/kg | 0.28–0.9 µg/kg | [73] |
AFB1, B2, G1, G2, OTA | Wheat, corn and rice cereals | Targeted UHPLC-ESI-MS/MS (tandem quadrupole) ESI+, sSRM | 0.1–5.0 µg/kg, (AFB1 0.03 µg/kg) | 0.1–25.0 µg/kg | [74] |
AFB1, B2, G1, G2, M1, OTA | Various foods and feed (24 types of corn feeds, peanut butter) | Targeted UHPLC-ESI-MS/MS (qQq tandem) ESI+, ESI−, sSRM | AFs 0.003 µg/kg AFG2 0.006 µg/kg OTA 0.064 µg/kg | AFs 0.01 µg/kg AFG2 0.02 µg/kg OTA 0.21 µg/kg | [75] |
AFB1, B2, G1, G2, OTA | Maize | Targeted LC-ESI-MS/MS (QTRAP qQq) ESI+, ESI−, sSRM | AFB1 0.6 µg/kg AFB2 0.3 µg/kg AFG1 0.4 µg/kg AFG2 0.8 µg/kg OTA 0.6 µg/kg | n/a | [76] |
AFB1, B2, G1, G2, OTA | Barley based breakfast cereals, maize, peanuts | Targeted UHPLC-ESI-MS/MS (QTRAP qQq) ESI+ ESI− (in single run), sSRM | AFs 0.05 µg/kg OTA 0.1 µg/kg | AFs 0.1 µg/kg OTA 0.25 µg/kg | [77] |
AFB1, B2, G1, G2, OTA | Durum wheat, corn flakes, maize and maize crackers | Targeted LC-ESI-MS/MS (QTRAP qQq) ESI+ ESI−, sSRM | n/a | AFs 1.0 µg/kg OTA 1.0 µg/mg | [78] |
AFB1, B2, G1, G2, OTA | Muesli, wheat flakes, oats, raisins, sultanas, whey powder, hazelnuts, whole meal bread | Targeted LC-ESI-MS/MS (tandem quadrupole) ESI+, sSRM | AFB1 0.05 ng/g AFB2 0.03 ng/g AFG1 0.03 ng/g AFG2 0.03 ng/g OTA 0.03 ng/g | AFB1 0.1 ng/g AFB2 0.05 ng/g AFG1 0.05 ng/g AFG2 0.05 ng/g OTA 0.4 ng/g | [79] |
AFB1, B2, G1, G2, OTA | Barley, corn, corn gluten, infant cereals, oat, rice, rye, wheat | Targeted LC-ESI-MS/MS (QTRAP qQq tandem mass) ESI+, ESI−, sSRM | n/a | AFs 1.0–10.0 µg/kg OTA 0.5–2.5 µg/kg | [80] |
AFB1, B2, G1, G2, OTA | Maize, rice, wheat | Targeted LC-ESI-MS/MS (qQq tandem) ESI+, sSRM | AFB1 0.12–0.21 g/kg AFB2 0.06–0.7 µg/kg AFG1 0.07–2.3 µg/kg AFG2 0.11–2.2 µg/kg OTA 0.18–3.2 µg/kg | AFB1 0.12–0.21 µg/kg AFB2 0.06–0.7 µg/kg AFG1 0.07–2.3 µg/kg AFG2 0.11–2.2 µg/kg OTA 0.18–3.2 µg/kg | [81] |
AFs, OTA | Black pepper, infant food (apple baby food), paprika, sunflower seed, wheat flour | Targeted UHPLC-ESI-MS/MS (QTRAP tandem) ESI+, ESI−, sSRM, Non-targeted UHPLC-ESI-HRMS (TOF) ESI+ ESI− | n/a | n/a | [82] |
AFB1, B2, G1, G2, OTA, OTB, OTC, Patulin | Maize, wheat | Targeted HPLC-ESI-MS/MS (QTRAP qQq), ESI+, ESI−, sSRM | 0.03–220 µg/kg | n/a | [83] |
AFB1, B2, G1, G2, M1, OTA, Patulin | Apple puree, green pepper, hazelnut, maize | Targeted UHPLC-ESI-MS/MS (QTRAP) ESI+, ESI−, sSRM | AFB1 0.6 µg/kg AFB2 0.6 µg/kg AFG1 1.2 µg/kg AFG2 2.3 µg/kg AFM1 0.6 µg/kg OTA 1.2 µg/kg PAT 35.9 µg/kg | AFB1 1.9 µg/kg AFB2 4.0 µg/kg AFG1 7.6 µg/kg AFG2 8.7 µg/kg AFM1 2.1 µg/kg OTA 3.7 µg/kg PAT 119.7 µg/kg | [65] |
AFB1, B2, G1, G2, OTA | Barley | Targeted UHPLC-HRMS (Orbitrap) Heated EPI (HEPI), HEPI+, HEPI− | n/a | n/a | [84] |
OTA | Barley | Targeted UHPLC-FTHRMS HEPI, HEPI+, HEPI− | n/a | n/a | [85] |
AFB1, B2, G1, G2, OTA | Black radish, Ginkgo biloba, garlic, soy | Targeted UHPLC-ESI-MS/MS (qQq), ESI+, sSRM | AFs 6.0 ng/g OTA 1.0 ng/g | AFs 2.0 ng/g OTA 0.3 ng/g | [86] |
AFB1, B2, G1, G2, M1, OTA, OTB | Maize, groundnut, sorghum, millet, rice, wheat, soy, dried fruits, infant foods, other processed food, animal feed | Targeted HPLC-ESI-MS/MS (QTRAP) ESI+, ESI−, sSRM | AFB1 3.0 µg/kg AFB2 6.0 µg/kg AFG1 8.0 µg/kg AFG2 8.0 µg/kg AFM1 4.0 µg/kg OTA, OTB 5.0 µg/kg | n/a | [87] |
AFB1, B2, G1, G2, M1, OTA | Breakfast cereals (maize, wheat, rice, multigrain, chocolate) | Targeted HPLC-fluorescence detector-EI-MS/MS, sSRM | AFB1 0.003 µg/kg AFB2 0.001 µg/kg AFG1 0.006 µg/kg AFG2 n/a AFM1 0.011 µg/kg OTA 0.006 µg/kg | AFB1 0.009 µg/kg AFB2 0.004 µg/kg AFG1 0.018 µg/kg AFG2 n/a AFM1 0.032 µg/kg OTA 0.019 µg/kg | [88] |
OTA | Wheat flour, coffee, spices, wine, beer | Targeted HPLC-MS/MS (ion trap), (1) ESI+ (2) APCI, sSRM | 0.5 µg/kg | 1.4 µg/kg | [89] |
AFB1, B2, G1, G2 | Peanut, peanut butter, spices, figs | Targeted LC-APCI-MS/MS (qQq), APCI+, sSRM, targeted | 0.1 µg/kg | n/a | [90] |
Patulin | Wheat, rice, spelt, oat, soy, tapioca based cereals (cassava), pasta, infant food | Targeted GC-MS/MS (qQq), electron impact ion source (EI), SRM, derivatizied, targeted | n/a | 5–10 µg/kg | [56] |
Genomic Tools | Mycotoxins | Crops | Comments | Ref. |
---|---|---|---|---|
Ion Torrent Personal Genome Machine (PGM) | Aflatoxins | — | Whole genome sequencing | [99] |
Microarray analysis, quantitative reverse transcription-PCR (qRT-PCR) | Aflatoxins | — | Aflatoxin biosynthesis | [100] |
Microarray analysis | Aflatoxins | — | Whole genome sequencing | [101] |
Microarray analysis | Aflatoxins | — | Gene expression profiles | [102] |
Whole genome sequencing | — | Identify genes differentially expressed in wild-type veA and veA mutant strains that could be involved in aflatoxin production. | [92] | |
RT-PCR and reverse-transcription PCR | Peanuts | Develop a screening method | [96] | |
PCR and LAMP-based group specific | Rice, nuts, raisins, dried figs | Develop a screening method to detect several aflatoxin producing species in a single analysis | [103] | |
Microarray | Aflatoxins, ochratoxin A | Wheat grain | Rapid detection for mycotoxins | [104] |
Fungal Strains | Genomic Size (Mbp *) | Mycotoxin | Mycotoxigenic | Ref. |
---|---|---|---|---|
LOAM00000000 flavus | 36.0 | Aflatoxin | Yes | [108] |
LIZI00000000 flavus | 36.4 | Aflatoxin | Yes | |
LIZJ00000000 flavus | 36.3 | Aflatoxin | Yes | |
LOAK00000000 flavus | 35.9 | Aflatoxin | Yes | |
LOAL00000000 flavus | 35.8 | Aflatoxin | Yes | |
LOAP00000000 parasiticus | 30.1 | Aflatoxin | Yes | |
NRRL 13137 nominus | 36.1 | Aflatoxin | Yes | [99] |
Aspergillus korhogoensis | N/a | Aflatoxin | Yes | [116] |
Aspergillus westerdijkiae | 36.1 | Ochratoxin A | Yes | [111] |
Aspergillus carbonarius | 36 | Ochratoxin A | Yes | [110] |
Penicillium expansum | 33.52 | Patulin | Yes | [115] |
Penicillium italicum | 28.99 | Patulin | Yes | [115] |
Mycotoxin | Studies | Outcomes | Ref. |
---|---|---|---|
Aflatoxin B1 | Identification of essential transcription factors for adequate DNA damage response after benzo (a) pyrene and aflatoxin B1 exposure by combining transcriptomics with functional genomics. | Transcriptomics and functional genomics tools used to investigate the genotoxicity of aflatoxin B1. | [132] |
Aflatoxin B1 induces persistent epigenomic effects in primary human hepatocytes associated with hepatocellular carcinoma. | Transcriptomics and epigenome studies used to understand the mechanisms of hepatocellular carcinoma development. | [8] | |
Quercetin tests negative for genotoxicity in transcriptome analyses of liver and small intestine of mice. | Genotoxicity related pathways in mice liver and small intestine. | [133] | |
Combined cytotoxicity of aflatoxin B1 and deoxynivalenol to hepatoma HepG2/C3A cells. | Different cytotoxicity pathways and their apoptotic process might be the mechanism of the synergistic cytotoxicity of HepG2/C3A carcinoma cells. | [134] | |
Integrated analysis of transcriptomics and metabolomics profiles in aflatoxin B1-induced hepatotoxicity in rat. | Gluconeogenesis, lipid metabolism disorder, and induced hepatotoxicity affect majorly after the acute AFB1 exposure. | [122] | |
Identification of early target genes of aflatoxin B1 in human hepatocytes, inter-individual variability and comparison with other genotoxic compounds. | Gene subset from AFB1 induced human hepatocytes identified several genes which are potential biomarkers of genotoxic compounds. | [135] | |
Aflatoxins | Use of functional genomics to assess the climate change impact on Aspergillus flavus and aflatoxin production. | Global temperature, water availability and rising CO2 levels affect the expression of the aflatoxin biosynthetic regulatory gene aflR. | [109] |
Ochratoxin A | Different toxicity mechanisms for citrinin and ochratoxin A revealed by transcriptomic analysis in yeast. | OTA deregulates developmental genes. | [136] |
Disruption of liver development and coagulation pathway by ochratoxin A in embryonic zebrafish. | OTA exposure led to a deficiency of coagulation factors. | [137] | |
Transcriptomic alterations induced by OTA in rat and human renal proximal tubular in vitro models and comparison to rat in vivo model. | The study provided a non-genotoxic mechanism of OTA-induced carcinogenicity. | [138] | |
Patulin | Transcriptomic responses of the basidiomycete Sporobolomyces sp. to the mycotoxin patulin. | Exposure to PAT directed the changes in gene expression in Sporobolomyces sp. This finding may lead to develop a bio-detoxification process. | [139] |
Mycotoxin | Fungal Strains | Study | Analysis Techniques | Outcome | Ref. |
---|---|---|---|---|---|
Aflatoxin B1 | Aspergillus flavus | Proteomic analysis reveals an aflatoxin-triggered immune response in cotyledons of Arachis hypogaea infected with Aspergillus flavus. | 2-D gel electrophoresis and MALDI-TOF/TOF mass spectrometer. | Three grades of the immune response in A. hypogaea during infection with toxigenic A. flavus were identified. PAMP-triggered immunity, effector-triggered immunity and metabolite-triggered immunity. | [162] |
Aspergillus flavus | Comparative leaf proteomics of drought-tolerant and-susceptible peanut in response to water stress. | 2-D gel electrophoresis and MALDI-TOF/TOF mass spectrometer. | 42 unique proteins showed interactions in the tolerant cultivar. | [167] | |
Aspergillus flavus | Insight into the global regulation of laeA in Aspergillus flavus based on proteomic profiling | Protein extraction, trypsin digestion, TMT-labelling and HPLC fractionation and LC-MS/MS | laeA gene affects cell morphology and contributes to the production of aflatoxin production. | [168] | |
Aspergillus flavus | Proteome analysis of A. flavus isolate-specific responses to oxidative stress in relationship to aflatoxin production capability. | Protein digestion and iTRAQ * labelling | 1173 proteins were identified, and 220 were differentially expressed. | [163] | |
Ochratoxin A | Aspergillus carbonarius | Proteome analysis of the fungus Aspergillus carbonarius under ochratoxin A producing conditions. | 2-D gel electrophoresis and MALDI-TOF/TOF mass spectrometer. | Nine differential proteins were identified by MALDI-MS/MS and MASCOT. Identified proteins were involved in regulation, amino acid metabolism, oxidative stress and sporulation. A protein with 126.5 fold higher abundance in high OTA-producing strain showed homology with CipC. | [155] |
Arabidopsis thaliana | iTRAQ mitoproteome Analysis reveals mechanisms of programmed cell death in Arabidopsis thaliana induced by ochratoxin A | iTRAQ * Analysis | The study investigated the toxicity mechanism of OTA on the host plant; their results indicated that OTA induced PCD in A. thaliana. 42 and 43 proteins were identified within 8 and 24 h. those proteins were mainly involved in perturbation of the mitochondrial electron transport chain, interfering with ATP synthesis and inducing PCD | [169] | |
Patulin | Penicillium expansum | Identification of differentially expressed genes involved in spore germination of Penicillium expansum by comparative transcriptome and proteome approaches. | RNA-seq (RNA sequencing) and iTRAQ * (isobaric tags for relative and absolute quantitation) approaches. | A total of 3026 differentially expressed genes, 77 differentially expressed predicted transcription factors and 489 differentially expressed proteins identified. Posttranscriptional regulation and modification serve essential roles in the management of fungal germination. | [164] |
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Eshelli, M.; Qader, M.M.; Jambi, E.J.; Hursthouse, A.S.; Rateb, M.E. Current Status and Future Opportunities of Omics Tools in Mycotoxin Research. Toxins 2018, 10, 433. https://doi.org/10.3390/toxins10110433
Eshelli M, Qader MM, Jambi EJ, Hursthouse AS, Rateb ME. Current Status and Future Opportunities of Omics Tools in Mycotoxin Research. Toxins. 2018; 10(11):433. https://doi.org/10.3390/toxins10110433
Chicago/Turabian StyleEshelli, Manal, M. Mallique Qader, Ebtihaj J. Jambi, Andrew S. Hursthouse, and Mostafa E. Rateb. 2018. "Current Status and Future Opportunities of Omics Tools in Mycotoxin Research" Toxins 10, no. 11: 433. https://doi.org/10.3390/toxins10110433