CoChat
Sign Up
Cited by 71Mycotoxins in Agriculture and FoodAllelopathy and phytotoxic interactionsPlant-Microbe Interactions and Immunity

The DOI matches its Crossref record.

A proteomic investigation of Aspergillus carbonarius exposed to yeast volatilome or to its major component 2-phenylethanol reveals major shifts in fungal metabolism

Open access
Tilocca, Bruno, Balmas, Virgilio, Hassan, Zahoor Ul, Jaoua, Samir, Migheli, Quirico·2019·International Journal of Food Microbiology
DOI 10.1016/j.ijfoodmicro.2019.108265
Open this paper in CoChat — free accountOpen PDF

Abstract

The use of yeast-derived volatile organic compounds (VOCs) represents a promising strategy for the biological control of various plant pathogens, including mycotoxin-producing fungi. Previous studies demonstrated the efficacy of the low-fermenting yeast Candida intermedia isolate 253 in reducing growth, sporulation, and ochratoxin A biosynthesis by Aspergillus carbonarius MPVA566. This study aimed to investigate whether the inhibitory effect of the yeast volatilome is solely attributable to 2-phenylethanol, its major component, or if a synergistic effect of all volatilome components is required to achieve an effective control of the fungal growth and metabolism. Microbiological methods, HPLC measurements and a UPLC-MS/MS approach were used to investigate the metabolic profile of A. carbonarius MPVA566 at different growing conditions: standard incubation (control), exposed to C. intermedia 253 volatilome, and incubation in the presence of 2-phenylethanol. Both yeast volatilome and 2-phenylethanol succeeded in the macroscopic inhibition of the radial mycelial growth, along with a significant reduction of ochratoxin A production. Functional classification of the fungal proteome identified in the diverse growing conditions revealed a different impact of both yeast VOCs and 2-phenylethanol exposure on the fungal proteome. Yeast VOCs target an array of metabolic routes of fungal system biology, including a marked reduction in protein biosynthesis, proliferative activity, mitochondrial metabolism, and particularly in detoxification of toxic substances. Exposure to 2-phenylethanol only partially mimicked the metabolic effects observed by the whole yeast volatilome, with protein biosynthesis and proliferative activity being reduced when compared with the control samples, but still far from the VOCs-exposed condition. This study represents the first investigation on the effects of yeast-derived volatilome and 2-phenylethanol on the metabolism of a mycotoxigenic fungus by means of proteomics analysis. CHEMICAL COMPOUNDS STUDIED OR USED IN THIS ARTICLE: 2-Phenylethanol (PubChem CID: 6054); ochratoxin-A (PubChem CID: 442530); sodium dodecyl sulfate (PubChem CID: 3423265); dithiothreitol (PubChem CID: 446094); phenylmethylsulfonyl fluoride (PubChem CID: 4784); iodoacetamide (PubChem CID: 3727); ammonium bicarbonate (PubChem CID: 14013); acetic acid (PubChem CID: 176); and acetonitrile (PubChem CID: 6342).

Overview

Integrity signals

Registry

Crossref · 10.1016/j.ijfoodmicro.2019.108265

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • More than twenty different VOCs were identified in the volatilomes of selected biocontrol strains of Cyberlindnera jadinii, Candida friedrichii, C. intermedia, and Lachancea thermotolerans.

    “More than twenty different VOCs were identified in the volatilomes of selected biocontrol strains of Cyberlindnera jadinii, Candida friedrichii, C. intermedia, and Lachancea thermotolerans”

    From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Tilocca et al. 2019

  • 2-phenylethanol was the most abundant and responsible for the inhibition of both mycelial growth and ochratoxin A production by Aspergillus carbonarius and A. ochraceus.

    “2-phenylethanol was the most abundant and responsible for the inhibition of both mycelial growth and ochratoxin A production by Aspergillus carbonarius and A. ochraceus (Farbo et al. 2018; Fiori et al. 2014; Tilocca et al. 2019).”

    From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Tilocca et al. 2019

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 52

  1. Andrade, 1995, HEAT repeats in the Huntington's disease protein, Nat. Genet., 11, 115, 10.1038/ng1095-115 · DOI
  2. Barford, 1999, The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs, Cell, 96, 99, 10.1016/S0092-8674(00)80963-0 · DOI · Paper page
  3. Ben-Shem, 2011, The structure of the eukaryotic ribosome at 3.0 Å resolution, Science, 334, 1524, 10.1126/science.1212642 · DOI
  4. Bondy, 2000, Immunomodulation by fungal toxins, J. Toxicol. Environ. Heal. - Part B Crit. Rev., 3, 109, 10.1080/109374000281113 · DOI
  5. Bork, 1994, A new family of carbon-nitrogen hydrolases, Protein Sci., 3, 1344, 10.1002/pro.5560030821 · DOI
  6. Bourquin, 2010, Structure and function of sphingosine-1-phosphate lyase, a key enzyme of sphingolipid metabolism, Structure, 18, 1054, 10.1016/j.str.2010.05.011 · DOI
  7. Bragulat, 2001, An easy screening method for fungi producing ochratoxin A in pure culture, Int. J. Food Microbiol., 71, 139, 10.1016/S0168-1605(01)00581-5 · DOI
  8. Bray, 2006, An ordination of the upland forest communities of southern Wisconsin, Ecol. Monogr., 27, 325, 10.2307/1942268 · DOI
  9. Bui-Klimke, 2015, Ochratoxin A and human health risk: a review of the evidence, Crit. Rev. Food Sci. Nutr., 55, 1860, 10.1080/10408398.2012.724480 · DOI
  10. Cashman, 1995, Structural and catalytic properties of the mammalian flavin-containing monooxygenase, Chem. Res. Toxicol., 8, 165, 10.1021/tx00044a001 · DOI
  11. Chang, 2015, Suppression of aflatoxin biosynthesis in Aspergillus flavus by 2-phenylethanol is associated with stimulated growth and decreased degradation of branched-chain amino acids, Toxins, 7, 3887, 10.3390/toxins7103887 · DOI
  12. Clarke, 1993, Non-parametric multivariate analyses of changes in community structure, Aust. J. Ecol., 18, 117, 10.1111/j.1442-9993.1993.tb00438.x · DOI
  13. Deising, 2008, Mechanisms and significance of fungicide resistance, Braz. J. Microbiol., 39, 286, 10.1590/S1517-83822008000200017 · DOI
  14. Duarte, 2011, Human ochratoxin A biomarkers—from exposure to effect, Crit. Rev. Toxicol., 41, 187, 10.3109/10408444.2010.529103 · DOI
  15. Dubois, 2012, Transcriptome database resource and gene expression atlas for the rose, BMC Genomics, 13, 638, 10.1186/1471-2164-13-638 · DOI
  16. Erzberger, 2006, Evolutionary relationships and structural mechanisms of AAA+ proteins, Annu. Rev. Biophys. Biomol. Struct., 35, 93, 10.1146/annurev.biophys.35.040405.101933 · DOI
  17. Eswaramoorthy, 2006, Mechanism of action of a flavin-containing monooxygenase, Proc. Natl. Acad. Sci., 103, 9832, 10.1073/pnas.0602398103 · DOI
  18. Farbo, 2018, Effect of yeast volatile organic compounds on ochratoxin A-producing Aspergillus carbonarius and A. ochraceus, Int. J. Food Microbiol., 284, 1, 10.1016/j.ijfoodmicro.2018.06.023 · DOI · Paper page
  19. Fazekas, 2005, Ochratoxin A content of urine samples of healthy humans in Hungary, Acta Vet. Hung., 53, 35, 10.1556/avet.53.2005.1.4 · DOI
  20. Fialho, 2016, Proteomic response of the phytopathogen Phyllosticta citricarpa to antimicrobial volatile organic compounds from Saccharomyces cerevisiae, Microbiol. Res., 183, 1, 10.1016/j.micres.2015.11.002 · DOI
  21. Fiori, 2014, Biocontrol activity of four non- and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice, Int. J. Food Microbiol., 189, 45, 10.1016/j.ijfoodmicro.2014.07.020 · DOI · Paper page
  22. Frickey, 2004, Phylogenetic analysis of AAA proteins, J. Struct. Biol., 146, 2, 10.1016/j.jsb.2003.11.020 · DOI
  23. Gevaudant, 2007, Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance, Plant Physiol., 144, 1763, 10.1104/pp.107.103762 · DOI
  24. Haighton, 2012, A reassessment of risk associated with dietary intake of ochratoxin A based on a lifetime exposure model, Crit. Rev. Toxicol., 42, 147, 10.3109/10408444.2011.636342 · DOI
  25. Huang, 2011, Control of postharvest botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia, Phytopathology, 101, 859, 10.1094/PHYTO-09-10-0255 · DOI · Paper page
  26. Kogkaki, 2015, Effect of interaction between Aspergillus carbonarius and non-ochratoxigenic grape-associated fungal isolates on growth and ochratoxin A production at different water activities and temperatures, Food Microbiol., 46, 521, 10.1016/j.fm.2014.09.014 · DOI
  27. Krueger, 2005, Mammalian flavin-containing monooxygenases: structure/function, genetic polymorphisms and role in drug metabolism, Pharmacol. Ther., 106, 357, 10.1016/j.pharmthera.2005.01.001 · DOI
  28. Liu, 2011, Effect of heat shock treatment on stress tolerance and biocontrol efficacy of Metschnikowia fructicola, FEMS Microbiol. Ecol., 76, 145, 10.1111/j.1574-6941.2010.01037.x · DOI
  29. Liu, 2011, Glycine betaine improves oxidative stress tolerance and biocontrol efficacy of the antagonistic yeast Cystofilobasidium infirmominiatum, Int. J. Food Microbiol., 146, 76, 10.1016/j.ijfoodmicro.2011.02.007 · DOI
  30. Liu, 2013, Review: utilization of antagonistic yeasts to manage postharvest fungal diseases of fruit, Int. J. Food Microbiol., 167, 153, 10.1016/j.ijfoodmicro.2013.09.004 · DOI · Paper page
  31. Liu, 2014, Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits, BMC Microbiol., 14, 242, 10.1186/s12866-014-0242-2 · DOI
  32. Lucas, 2015, The evolution of fungicide resistance, Adv. Appl. Microbiol., 90, 29, 10.1016/bs.aambs.2014.09.001 · DOI
  33. McMahon, 2004, COP and clathrin-coated vesicle budding: different pathways, common approaches, Curr. Opin. Cell Biol., 16, 379, 10.1016/j.ceb.2004.06.009 · DOI
  34. Melin, 2007, Optimisation and comparison of liquid and dry formulations of the biocontrol yeast Pichia anomala J121, Appl. Microbiol. Biotechnol., 73, 1008, 10.1007/s00253-006-0552-x · DOI
  35. Nishino, 2012, CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold, Cell, 148, 487, 10.1016/j.cell.2011.11.061 · DOI
  36. Nunes, 2012, Biological control of postharvest diseases of fruit, Eur. J. Plant Pathol., 133, 181, 10.1007/s10658-011-9919-7 · DOI
  37. Olsen, 2005, Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap, Mol. Cell. Proteomics, 4, 2010, 10.1074/mcp.T500030-MCP200 · DOI
  38. Oskouian, 2004, Death and taxis: what non-mammalian models tell us about sphingosine-1-phosphate, Semin. Cell Dev. Biol., 15, 529, 10.1016/j.semcdb.2004.05.009 · DOI
  39. Pfaller, 2004, Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus, J. Clin. Microbiol., 42, 4419, 10.1128/JCM.42.10.4419-4431.2004 · DOI
  40. Poulsen, 1995, Multisubstrate flavin-containing monooxygenases: applications of mechanism to specificity, Chem. Biol. Interact., 96, 57, 10.1016/0009-2797(94)03583-T · DOI
  41. Rappsilber, 2007, Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips, Nat. Protoc., 2, 1896, 10.1038/nprot.2007.261 · DOI · Paper page
  42. Regodón Mateos, 2006, Influence of Saccharomyces cerevisiae yeast strain on the major volatile compounds of wine, Enzym. Microb. Technol., 40, 151, 10.1016/j.enzmictec.2005.10.048 · DOI
  43. Snelders, 2008, Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism, PLoS Med., 5, e219, 10.1371/journal.pmed.0050219 · DOI
  44. Spadaro, 2004, State of the art and future prospects of the biological control of postharvest fruit diseases, Int. J. Food Microbiol., 91, 185, 10.1016/S0168-1605(03)00380-5 · DOI
  45. Suda, 2003, Saccharomyces cerevisiae QNS1 codes for NAD+ synthetase that is functionally conserved in mammals, Yeast, 20, 995, 10.1002/yea.1008 · DOI
  46. Tagami, 2004, Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis, Cell, 116, 51, 10.1016/S0092-8674(03)01064-X · DOI
  47. Tilocca, 2016, Variations of phosphorous accessibility causing changes in microbiome functions in the gastrointestinal tract of chickens, PLoS One, 11, 10.1371/journal.pone.0164735 · DOI
  48. Tribe, 2006, Biological control of plant pathogens, J. Appl. Ecol., 12, 983, 10.2307/2402104 · DOI
  49. Voglmaier, 2007, Do different endocytic pathways make different synaptic vesicles?, Curr. Opin. Neurobiol., 17, 374, 10.1016/j.conb.2007.04.002 · DOI
  50. Wu, 2011, WebMGA: a customizable web server for fast metagenomic sequence analysis, BMC Genomics, 12, 444, 10.1186/1471-2164-12-444 · DOI
  51. Yan, 2011, Isolation and identification of a putative scent-related gene RhMYB1 from rose, Mol. Biol. Rep., 38, 4475, 10.1007/s11033-010-0577-1 · DOI
  52. Young, 2003, Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70, Cell, 112, 41, 10.1016/S0092-8674(02)01250-3 · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Tilocca, B., Balmas, V., Hassan, Z. U., Jaoua, S., & Migheli, Q.
Affiliations
  • University of Sassari (IT)
  • Qatar University (QA)
Corresponding author
Migheli, Quirico
ORCID
Venue
International Journal of Food Microbiology
Publisher
Elsevier BV
Published
2019-10
Volume
306
Pages
108265
ISSN
0168-1605 (ISSN-L)
DOI
10.1016/j.ijfoodmicro.2019.108265
OpenAlex
W2956505105
Cited by
71
References
0
Citations by year
2026: 4 · 2025: 10 · 2024: 11 · 2023: 17 · 2022: 10 · 2021: 9 · 2020: 8 · 2019: 2
FWCI
5.35
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Food Microbiology (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • UnissResearch (Università degli Studi di Sassari) (submittedVersion, cc-by-nc-nd)
  • Figshare (submittedVersion, cc-by-nc-nd)
  • UnissResearch (Università degli Studi di Sassari) (submittedVersion)
  • Qatar University QSpace (Qatar University) (submittedVersion)
Funders
Qatar Foundation
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycotoxins in Agriculture and Food
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Allelopathy and phytotoxic interactions
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
Keywords
Aspergillus carbonarius, Candida intermedia, 2-phenylethanol, volatile organic compounds, biological control, mycotoxin production, ochratoxin A, fungal proteome, fungal metabolism, protein synthesis, mitochondrial metabolism, detoxification, mycelial growth inhibition, wine spoilage
MeSH terms
Aspergillus, Candida, Chromatography, Liquid, Fermentation, Mycotoxins, Ochratoxins, Phenylethyl Alcohol, Proteome, Proteomics, Tandem Mass Spectrometry, Volatile Organic Compounds

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review