Biocontrol of Aflatoxins Using Non-Aflatoxigenic Aspergillus flavus: A Literature Review

Aflatoxins (AFs) are mycotoxins, predominantly produced by Aspergillus flavus, A. parasiticus, A. nomius, and A. pseudotamarii. AFs are carcinogenic compounds causing liver cancer in humans and animals. Physical and biological factors significantly affect AF production during the pre-and post-harvest time. Several methodologies have been developed to control AF contamination, yet; they are usually expensive and unfriendly to the environment. Consequently, interest in using biocontrol agents has increased, as they are convenient, advanced, and friendly to the environment. Using non-aflatoxigenic strains of A. flavus (AF−) as biocontrol agents is the most promising method to control AFs’ contamination in cereal crops. AF− strains cannot produce AFs due to the absence of polyketide synthase genes or genetic mutation. AF− strains competitively exclude the AF+ strains in the field, giving an extra advantage to the stored grains. Several microbiological, molecular, and field-based approaches have been used to select a suitable biocontrol agent. The effectiveness of biocontrol agents in controlling AF contamination could reach up to 99.3%. Optimal inoculum rate and a perfect time of application are critical factors influencing the efficacy of biocontrol agents.

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Biological Control of the Artillery Fungus, Sphaerobolus stellatus, with Trichoderma harzianum and Bacillus subtilis

Journal of Environmental Horticulture ◽

10.24266/0738-2898-19.1.21 ◽

2001 ◽

Vol 19 (1) ◽

pp. 21-23 ◽

Cited By ~ 1

Author(s):

Elizabeth A. Brantley ◽

Donald D. Davis ◽

Larry J. Kuhns

Keyword(s):

Biological Control ◽

Bacillus Subtilis ◽

Trichoderma Harzianum ◽

Biocontrol Agent ◽

Biocontrol Agents ◽

Biological Control Agents ◽

Oatmeal Agar ◽

Time Of Application ◽

Bacterium Bacillus Subtilis ◽

Bacterium Bacillus

Abstract Three strains of the fungus Trichoderma harzianum Rifai and two strains of the bacterium Bacillus subtilis (Ehrenberg) Cohn were evaluated for their ability to suppress colonization and sporulation of the artillery fungus (Sphaerobolus stellatus Tode:Pers.) on oatmeal agar. All five biological control agents inhibited growth of S. stellatus, but efficacy depended on time of application. Simultaneous inoculation of agar with S. stellatus and the biocontrol agents, as well as inoculation of biocontrol agents 14 days prior to S. stellatus, resulted in complete inhibition of S. stellatus. Inoculation of agar with biocontrol agents 14 days after inoculation with S. stellatus reduced, but did not completely suppress S. stellatus colonization and sporulation. In this experiment, gleba (spore masses) treated with all strains of T. harzianum and strain GBO3 of B. subtilis did not germinate, but 13% of gleba treated with strain MBI 600 of B. subtilis did germinate. Trichoderma harzianum was more effective than B. subtilis as a biocontrol agent.

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Use of Risk Analysis for Screening Weed Biocontrol Agents: Altica carduorum Guer. (Coleoptera: Chrysomelidae) from China as a Biocontrol Agent of Cirsium arvense (L.) Scop. in North America

Biocontrol Science and Technology ◽

10.1080/09583159730712 ◽

1997 ◽

Vol 7 (3) ◽

pp. 299-308 ◽

Cited By ~ 24

Author(s):

FANG-HAO WAN ◽

PETER HARRIS

Keyword(s):

North America ◽

Risk Analysis ◽

Biocontrol Agent ◽

Biocontrol Agents ◽

Cirsium Arvense ◽

Weed Biocontrol

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Streptomyces roseolus, A Promising Biocontrol Agent Against Aspergillus flavus, the Main Aflatoxin B1 Producer

Toxins ◽

10.3390/toxins10110442 ◽

2018 ◽

Vol 10 (11) ◽

pp. 442 ◽

Cited By ~ 7

Author(s):

Isaura Caceres ◽

Selma Snini ◽

Olivier Puel ◽

Florence Mathieu

Keyword(s):

Aspergillus Flavus ◽

Aflatoxin B1 ◽

Biocontrol Agent ◽

Cyclopiazonic Acid ◽

Over Expression ◽

Expression Of Genes ◽

B1 Gene ◽

Genes Encoding ◽

Molecular Mechanism Of Action ◽

Potential Use

Crop contamination by aflatoxin B1 is a current problem in tropical and subtropical regions. In the future, this contamination risk may be expanded to European countries due to climate change. The development of alternative strategies to prevent mycotoxin contamination that further contribute to the substitution of phytopharmaceutical products are thus needed. For this, a promising method resides in the use of biocontrol agents. Several actinobacteria strains have demonstrated to effectively reduce the aflatoxin B1 concentration. Nevertheless, the molecular mechanism of action by which these biological agents reduce the mycotoxin concentration has not been determined. The aim of the present study was to test the potential use of Streptomyces roseolus as a biocontrol agent against aflatoxin B1 contamination. Co-cultures with Aspergillus flavus were conducted, and the molecular fungal response was investigated through analyzing the q-PCR expression of 65 genes encoding relevant fungal functions. Moreover, kojic and cyclopiazonic acid concentrations, as well as morphological fungal changes were also analyzed. The results demonstrated that reduced concentrations of aflatoxin B1 and kojic acid were respectively correlated with the down-regulation of the aflatoxin B1 gene cluster and kojR gene expression. Moreover, a fungal hypersporulated phenotype and a general over-expression of genes involved in fungal development were observed in the co-culture condition.

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Acarine biocontrol agents Neoseiulus californicus sensu Athias-Henriot (1977) and N. barkeri Hughes (Mesostigmata: Phytoseiidae) redescribed, their synonymies assessed, and the identity of N. californicus (McGregor) clarified based on examination of types

Zootaxa ◽

10.11646/zootaxa.4500.4.1 ◽

2018 ◽

Vol 4500 (4) ◽

pp. 451 ◽

Cited By ~ 3

Author(s):

FRÉDÉRIC BEAULIEU ◽

JENNIFER J. BEARD

Keyword(s):

Biocontrol Agent ◽

Species Concept ◽

Biocontrol Agents ◽

International Commission ◽

Neoseiulus Californicus ◽

Zoological Nomenclature ◽

Male And Female ◽

Crop Pests ◽

Type Host ◽

Single Sex

In 1954, McGregor described two species of phytoseiids from lemon, in California, USA: Typhlodromus californicus McGregor and T. mungeri McGregor, the former represented by one male, and the latter by two females. Since its description, T. mungeri was synonymised under T. californicus, and the name T. (now Neoseiulus) californicus has been used extensively to represent a species that is now commonly used as a biocontrol agent of crop pests worldwide. However, the true identity of the biocontrol agent is uncertain because the original descriptions of T. californicus and T. mungeri were not adequate enough to allow an irrefutable identification, with each description being based on specimens of a single sex. An examination of the types of N. californicus and N. mungeri revealed that they are morphologically identical to the male and female of N. barkeri Hughes, 1948, respectively, and that they are in fact junior synonyms of N. barkeri—and are therefore distinct from the biocontrol agent globally called N. californicus (sensu Athias-Henriot, 1977; see Griffiths, 2015). This is further supported by a comparison with male and female syntypes of N. barkeri, as well as other specimens of N. barkeri including some collected from the type host in the vicinity of the type location (i.e. lemon in southern California, 1952–1958). We redescribe the male and female of both N. barkeri and N. californicus sensu Athias-Henriot (1977), based on representative specimens from at least 14 and 19 populations, respectively. Based on examination of types, we confirm the synonymy of N. mckenziei (Schuster & Pritchard, 1963), N. picketti (Specht, 1968), and N. oahuensis (Prasad, 1968) with N. barkeri, and that the names N. chilenensis (Dosse, 1958b) and N. wearnei (Schicha, 1987) represent the same species as N. californicus sensu Athias-Henriot (1977). We also provide a hypothesis as to why Chant (1959) had erroneously synonymised T. californicus and T. mungeri under T. marinus (Willmann). Finally, we suggest maintaining the prevailing usage of the name N. californicus (McGregor) for the species concept of Athias-Henriot (1977) as followed by subsequent authors, through submission of a separate application to the International Commission of Zoological Nomenclature (ICZN). In the meantime, the current meaning of N. californicus should be maintained until a ruling by the ICZN is made on the application.

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Laboratory tests for assessing efficacy of atoxigenic Aspergillus flavus strains as biocontrol agents

International Journal of Food Microbiology ◽

10.1016/j.ijfoodmicro.2011.02.020 ◽

2011 ◽

Vol 146 (3) ◽

pp. 235-243 ◽

Cited By ~ 32

Author(s):

Francesca Degola ◽

Elettra Berni ◽

Francesco M. Restivo

Keyword(s):

Aspergillus Flavus ◽

Laboratory Tests ◽

Biocontrol Agents

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Aspergillus flavus NRRL 35739, a Poor Biocontrol Agent, May Have Increased Relative Expression of Stress Response Genes

Journal of Fungi ◽

10.3390/jof5020053 ◽

2019 ◽

Vol 5 (2) ◽

pp. 53 ◽

Cited By ~ 2

Author(s):

Kayla K. Pennerman ◽

Guohua Yin ◽

Joan W. Bennett ◽

Sui-Sheng T. Hua

Keyword(s):

Stress Response ◽

Aspergillus Flavus ◽

Genetic Basis ◽

Biocontrol Agent ◽

Success Rates ◽

Lower Stress ◽

Relative Expression ◽

Stress Response Genes ◽

Variable Success ◽

Aflatoxin Accumulation

Biocontrol of the mycotoxin aflatoxin utilizes non-aflatoxigenic strains of Aspergillus flavus, which have variable success rates as biocontrol agents. One non-aflatoxigenic strain, NRRL 35739, is a notably poor biocontrol agent. Its growth in artificial cultures and on peanut kernels was found to be slower than that of two aflatoxigenic strains, and NRRL 35739 exhibited less sporulation when grown on peanuts. The non-aflatoxigenic strain did not greatly prevent aflatoxin accumulation. Comparison of the transcriptomes of aflatoxigenic and non-aflatoxigenic A. flavus strains AF36, AF70, NRRL 3357, NRRL 35739, and WRRL 1519 indicated that strain NRRL 35739 had increased relative expression of six heat shock and stress response proteins, with the genes having relative read counts in NRRL 35739 that were 25 to 410 times more than in the other four strains. These preliminary findings tracked with current thought that aflatoxin biocontrol efficacy is related to the ability of a non-aflatoxigenic strain to out-compete aflatoxigenic ones. The slower growth of NRRL 35739 might be due to lower stress tolerance or overexpression of stress response(s). Further study of NRRL 35739 is needed to refine our understanding of the genetic basis of competitiveness among A. flavus strains.

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Identification of Aspergillus flavus Isolates as Potential Biocontrol Agents of Aflatoxin Contamination in Crops

Journal of Food Protection ◽

10.4315/0362-028x.jfp-12-436 ◽

2013 ◽

Vol 76 (6) ◽

pp. 1051-1055 ◽

Cited By ~ 5

Author(s):

L. J. ROSADA ◽

J. R. SANT'ANNA ◽

C. C. S. FRANCO ◽

G. N. M. ESQUISSATO ◽

P. A. S. R. SANTOS ◽

...

Keyword(s):

Biological Control ◽

Aspergillus Flavus ◽

Filamentous Fungus ◽

Microscopic Examination ◽

Genetic Recombination ◽

Aflatoxin Contamination ◽

Biocontrol Agents ◽

Biological Control Agents ◽

Nit Mutants ◽

The Stability

Aspergillus flavus, a haploid organism found worldwide in a variety of crops, including maize, cottonseed, almond, pistachio, and peanut, causes substantial and recurrent worldwide economic liabilities. This filamentous fungus produces aflatoxins (AFLs) B1 and B2, which are among the most carcinogenic compounds from nature, acutely hepatotoxic and immunosuppressive. Recent efforts to reduce AFL contamination in crops have focused on the use of nonaflatoxigenic A. flavus strains as biological control agents. Such agents are applied to soil to competitively exclude native AFL strains from crops and thereby reduce AFL contamination. Because the possibility of genetic recombination in A. flavus could influence the stability of biocontrol strains with the production of novel AFL phenotypes, this article assesses the diversity of vegetative compatibility reactions in isolates of A. flavus to identify heterokaryon self-incompatible (HSI) strains among nonaflatoxigenic isolates, which would be used as biological controls of AFL contamination in crops. Nitrate nonutilizing (nit) mutants were recovered from 25 A. flavus isolates, and based on vegetative complementation between nit mutants and on the microscopic examination of the number of hyphal fusions, five nonaflatoxigenic (6, 7, 9 to 11) and two nontoxigenic (8 and 12) isolates of A. flavus were phenotypically characterized as HSI. Because the number of hyphal fusions is reduced in HSI strains, impairing both heterokaryon formation and the genetic exchanges with aflatoxigenic strains, the HSI isolates characterized here, especially isolates 8 and 12, are potential agents for reducing AFL contamination in crops.

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Nannocystis exedens: A Potential Biocompetitive Agent against Aspergillus flavus and Aspergillus parasiticus

Journal of Food Protection ◽

10.4315/0362-028x-64.7.1030 ◽

2001 ◽

Vol 64 (7) ◽

pp. 1030-1034 ◽

Cited By ~ 25

Author(s):

WILLIE J. TAYLOR ◽

FRANCES A. DRAUGHON

Keyword(s):

Aspergillus Flavus ◽

Yeast Extract ◽

Biocontrol Agent ◽

Aspergillus Parasiticus ◽

Extract Agar ◽

Potential Biocontrol Agent ◽

Aflatoxigenic Fungi ◽

Close Proximity ◽

Zones Of Inhibition ◽

Yeast Extract Agar

This study examined the potential for controlling toxigenic Aspergillus flavus and Aspergillus parasiticus by biological means using a myxobacterium commonly found in soil. The ability of Nannocystis exedens to antagonize A. flavus ATCC 16875, A. flavus ATCC 26946, and A. parasiticus NRRL 3145 was discovered. Cultures of aflatoxigenic fungi were grown on 0.3% Trypticase peptone yeast extract agar for 14 days at 28°C. When N. exedens was grown in close proximity with an aflatoxigenic mold, zones of inhibition (10 to 20 mm) developed between the bacterium and mold colony. A flattening of the mold colony on the sides nearest N. exedens and general stunting of growth of the mold colony were also observed. When N. exedens was added to the center of the cross-streak of a mold colony, lysis of the colony by the bacterium was observed after 24 h. Microscopic observations revealed that N. exedens grew on spores, germinating spores, hyphae, and sclerotia of the molds. These results indicate that N. exedens may be a potential biocontrol agent against A. flavus and A. parasiticus.

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