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Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time

BACKGROUND: The primary and secondary metabolites of fungi are critical for adaptation to environmental stresses, host pathogenicity, competition with other microbes, and reproductive fitness. Drought-derived reactive oxygen species (ROS) have been shown to stimulate aflatoxin production and regulat...

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Autores principales: Fountain, Jake C., Yang, Liming, Pandey, Manish K., Bajaj, Prasad, Alexander, Danny, Chen, Sixue, Kemerait, Robert C., Varshney, Rajeev K., Guo, Baozhu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727485/
https://www.ncbi.nlm.nih.gov/pubmed/31488075
http://dx.doi.org/10.1186/s12866-019-1580-x
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author Fountain, Jake C.
Yang, Liming
Pandey, Manish K.
Bajaj, Prasad
Alexander, Danny
Chen, Sixue
Kemerait, Robert C.
Varshney, Rajeev K.
Guo, Baozhu
author_facet Fountain, Jake C.
Yang, Liming
Pandey, Manish K.
Bajaj, Prasad
Alexander, Danny
Chen, Sixue
Kemerait, Robert C.
Varshney, Rajeev K.
Guo, Baozhu
author_sort Fountain, Jake C.
collection PubMed
description BACKGROUND: The primary and secondary metabolites of fungi are critical for adaptation to environmental stresses, host pathogenicity, competition with other microbes, and reproductive fitness. Drought-derived reactive oxygen species (ROS) have been shown to stimulate aflatoxin production and regulate in Aspergillus flavus, and may function in signaling with host plants. Here, we have performed global, untargeted metabolomics to better understand the role of aflatoxin production in oxidative stress responses, and also explore isolate-specific oxidative stress responses over time. RESULTS: Two field isolates of A. flavus, AF13 and NRRL3357, possessing high and moderate aflatoxin production, respectively, were cultured in medium with and without supplementation with 15 mM H(2)O(2), and mycelia were collected following 4 and 7 days in culture for global metabolomics. Overall, 389 compounds were described in the analysis which encompassed 9 biological super-pathways and 47 sub-pathways. These metabolites were examined for differential accumulation. Significant differences were observed in both isolates in response to oxidative stress and when comparing sampling time points. CONCLUSIONS: The moderately high aflatoxin-producing isolate, NRRL3357, showed extensive stimulation of antioxidant mechanisms and pathways including polyamines metabolism, glutathione metabolism, TCA cycle, and lipid metabolism while the highly aflatoxigenic isolate, AF13, showed a less vigorous response to stress. Carbohydrate pathway levels also imply that carbohydrate repression and starvation may influence metabolite accumulation at the later timepoint. Higher conidial oxidative stress tolerance and antioxidant capacity in AF13 compared to NRRL3357, inferred from their metabolomic profiles and growth curves over time, may be connected to aflatoxin production capability and aflatoxin-related antioxidant accumulation. The coincidence of several of the detected metabolites in H(2)O(2)-stressed A. flavus and drought-stressed hosts also suggests their potential role in the interaction between these organisms and their use as markers/targets to enhance host resistance through biomarker selection or genetic engineering. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-019-1580-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-67274852019-09-12 Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time Fountain, Jake C. Yang, Liming Pandey, Manish K. Bajaj, Prasad Alexander, Danny Chen, Sixue Kemerait, Robert C. Varshney, Rajeev K. Guo, Baozhu BMC Microbiol Research Article BACKGROUND: The primary and secondary metabolites of fungi are critical for adaptation to environmental stresses, host pathogenicity, competition with other microbes, and reproductive fitness. Drought-derived reactive oxygen species (ROS) have been shown to stimulate aflatoxin production and regulate in Aspergillus flavus, and may function in signaling with host plants. Here, we have performed global, untargeted metabolomics to better understand the role of aflatoxin production in oxidative stress responses, and also explore isolate-specific oxidative stress responses over time. RESULTS: Two field isolates of A. flavus, AF13 and NRRL3357, possessing high and moderate aflatoxin production, respectively, were cultured in medium with and without supplementation with 15 mM H(2)O(2), and mycelia were collected following 4 and 7 days in culture for global metabolomics. Overall, 389 compounds were described in the analysis which encompassed 9 biological super-pathways and 47 sub-pathways. These metabolites were examined for differential accumulation. Significant differences were observed in both isolates in response to oxidative stress and when comparing sampling time points. CONCLUSIONS: The moderately high aflatoxin-producing isolate, NRRL3357, showed extensive stimulation of antioxidant mechanisms and pathways including polyamines metabolism, glutathione metabolism, TCA cycle, and lipid metabolism while the highly aflatoxigenic isolate, AF13, showed a less vigorous response to stress. Carbohydrate pathway levels also imply that carbohydrate repression and starvation may influence metabolite accumulation at the later timepoint. Higher conidial oxidative stress tolerance and antioxidant capacity in AF13 compared to NRRL3357, inferred from their metabolomic profiles and growth curves over time, may be connected to aflatoxin production capability and aflatoxin-related antioxidant accumulation. The coincidence of several of the detected metabolites in H(2)O(2)-stressed A. flavus and drought-stressed hosts also suggests their potential role in the interaction between these organisms and their use as markers/targets to enhance host resistance through biomarker selection or genetic engineering. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12866-019-1580-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-09-05 /pmc/articles/PMC6727485/ /pubmed/31488075 http://dx.doi.org/10.1186/s12866-019-1580-x Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Fountain, Jake C.
Yang, Liming
Pandey, Manish K.
Bajaj, Prasad
Alexander, Danny
Chen, Sixue
Kemerait, Robert C.
Varshney, Rajeev K.
Guo, Baozhu
Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title_full Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title_fullStr Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title_full_unstemmed Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title_short Carbohydrate, glutathione, and polyamine metabolism are central to Aspergillus flavus oxidative stress responses over time
title_sort carbohydrate, glutathione, and polyamine metabolism are central to aspergillus flavus oxidative stress responses over time
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727485/
https://www.ncbi.nlm.nih.gov/pubmed/31488075
http://dx.doi.org/10.1186/s12866-019-1580-x
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