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      Interacting Abiotic Factors Affect Growth and Aflatoxin B 1 Production Profiles of Aspergillus flavus Strains on Pistachio-Based Matrices and Pistachio Nuts

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          Abstract

          Pistachio nuts are an economically important commodity produced by many countries. They can be colonized by mycotoxigenic fungi, especially Aspergillus flavus, resulting in contamination with aflatoxins (AFs), especially aflatoxin B 1 (AFB 1), a Class 1a carcinogen. The objectives were to examine the effect of interactions between the two key abiotic factors, temperature and water activity (a w ) on (a) in vitro growth and AFB 1 production by four strains of A. flavus isolated from pistachio nuts, on a milled pistachio nut medium modified ionically (NaCl) and non-ionically (glycerol) in the range 20–35°C and 0.995–0.85 a w , (b) colonization of layers of raw pistachio nuts stored at different interacting temperature x a w conditions and on relative AFB 1 production and (c) develop models to produce contour maps of the optimal and marginal boundary conditions for growth and AFB 1 production by up to 4 strains of this species. On pistachio nut-based media, optimum growth of four strains of A. flavus was at 0.98–0.95 a w and 30–35°C. Optimum AFB 1 production was at 30–35°C and 0.98 a w . No significant differences in growth was found on ionic and non-ionically modified media. Colonization of layers of raw pistachio nuts was slower and contamination with AFB 1 significantly less than in in vitro studies. Contour maps based on the pooled data for up to four strains ( in vitro, in situ) showed the optimum and marginal conditions for growth and AFB 1 production. These data can be used to identify those conditions which represent a high, intermediate or low risk of colonization and AFB 1 contamination in the pistachio nut processing chain. These results are discussed in the context of the development of appropriate intervention strategies to minimize AFB 1 contamination of this economically important commodity.

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          Most cited references24

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          Climate change, food security and mycotoxins: Do we know enough?

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            A systems approach to model the relationship between aflatoxin gene cluster expression, environmental factors, growth and toxin production by Aspergillus flavus.

            A microarray analysis was used to examine the effect of combinations of water activity (a(w), 0.995-0.90) and temperature (20-42°C) on the activation of aflatoxin biosynthetic genes (30 genes) in Aspergillus flavus grown on a conducive YES (20 g yeast extract, 150 g sucrose, 1 g MgSO(4)·7H(2)O) medium. The relative expression of 10 key genes (aflF, aflD, aflE, aflM, aflO, aflP, aflQ, aflX, aflR and aflS) in the biosynthetic pathway was examined in relation to different environmental factors and phenotypic aflatoxin B(1) (AFB(1)) production. These data, plus data on relative growth rates and AFB(1) production under different a(w) × temperature conditions were used to develop a mixed-growth-associated product formation model. The gene expression data were normalized and then used as a linear combination of the data for all 10 genes and combined with the physical model. This was used to relate gene expression to a(w) and temperature conditions to predict AFB(1) production. The relationship between the observed AFB(1) production provided a good linear regression fit to the predicted production based in the model. The model was then validated by examining datasets outside the model fitting conditions used (37°C, 40°C and different a(w) levels). The relationship between structural genes (aflD, aflM) in the biosynthetic pathway and the regulatory genes (aflS, aflJ) was examined in relation to a(w) and temperature by developing ternary diagrams of relative expression. These findings are important in developing a more integrated systems approach by combining gene expression, ecophysiological influences and growth data to predict mycotoxin production. This could help in developing a more targeted approach to develop prevention strategies to control such carcinogenic natural metabolites that are prevalent in many staple food products. The model could also be used to predict the impact of climate change on toxin production.
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              Osmotic coefficients and water potentials of sodium chloride solutions from 0 to 40°C

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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                20 January 2021
                2020
                : 11
                : 624007
                Affiliations
                [1] 1Department of Biology, College of Science, Taif University , Taif, Saudi Arabia
                [2] 2Applied Mycology Group, Environment and AgriFood Theme, Cranfield University , Cranfield, United Kingdom
                Author notes

                Edited by: Lin Lin, Jiangsu University, China

                Reviewed by: Zuzana Hruska, Mississippi State University, United States; Massimo Reverberi, Sapienza University of Rome, Italy; Abhishek Kumar Dwivedy, Banaras Hindu University, India

                *Correspondence: Naresh Magan, n.magan@ 123456cranfield.ac.uk

                Present address: Esther Garcia-Cela, School of Life and Medical Sciences, University of Hertfordshire, Hatfield, United Kingdom

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.624007
                7855869
                33552034
                2301d67c-0fd6-412d-b71a-71b7af6cdb9b
                Copyright © 2021 Baazeem, Garcia-Cela, Medina and Magan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 October 2020
                : 17 December 2020
                Page count
                Figures: 8, Tables: 0, Equations: 1, References: 25, Pages: 12, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                water relations,growth,mycotoxins,boundary conditions,optimum conditions,aflatoxins,pistachios

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