Investigation of antifungal activity of surfactin against mycotoxigenic phytopathogenic fungus Fusarium moniliforme and its impact in seed germination and mycotoxicosis

https://doi.org/10.1016/j.pestbp.2019.01.010Get rights and content

Highlights

  • Surfactin inhibit the growth of Fusarium moniliforme in both in vitro and in vivo.

  • Surfactin prevent mycotoxigenic phytopathogenic fungi contamination on maize kernels.

  • Surfactin prevents F. moniliforme associated plant and animal diseases.

Abstract

The mycotoxigenic phytopathogenic fungus such as Fusarium moniliforme contamination in maize kernels may not only affect seed germination but also negatively cause mycotoxicosis in animals and humans. There is no effective fungicides to control the growth of F. moniliforme on maize kernels. Hence, effective bioactive compounds are needed to prevent plant and animal diseases associated with F. moniliforme contamination in cereals. Surfactin is an well-known antimicrobial lipopeptide has strong antifungal activities against several phytopathogenic fungi and may have potential uses in agriculture. So, in this present study the antifungal activity of surfactin extracted from Brevibacillus brevis KN8(2) was investigated against F. moniliforme, further its impact in seed germination and mycotoxicosis was also studied. Our results showed that surfactin inhibited and damaged the hyphae of F. moniliforme in in vitro. The agarose gel electrophoresis, SDS-PAGE analysis and biochemical assay presented that surfactin damaged the DNA, protein and reduced the GSH content in F. moniliforme. Furthermore, surfactin prevent maize seed germination problem and mycotoxicosis in animal model associated with F. moniliforme via prevention of F. moniliforme contamination on maize kernels. These findings revealed that surfactin could be an effective bio-fungicide in the plant disease management.

Introduction

Maize (Zea mays) is one of the most important food crops in the world that occupies nearly 100 million hectares and it provides 30% of food calories along with other crops to >4.5 billion peoples in developing countries; moreover, its demand as feed for both humans and their livestock has grown immensely (Shiferaw et al., 2011; Tan et al., 2017). As a result, several high yielding varieties of maize are introduced to fulfill the food demands; however, its yield and quality are severely affected by several biotic and abiotic factors. The phytopathogenic cum mycotoxigenic fungus such as Fusarium moniliforme induced fungal diseases in maize is an important devastating factor affecting not only the yield but also affecting the quality of maize grains due to its mycotoxins contamination in kernels (Hu et al., 2017; Pal et al., 2001). Fusarium moniliforme can invade in maize at different production stages especially during pre-harvest and post-harvest handling; moreover, maize kernels are the ideal part for the colonization/contamination that has been not properly dried or stored resulting in production of toxic secondary metabolites such as mycotoxins as its virulence factors during colonization/infection of maize kernels that leads to direct yield loss in agriculture via inhibition of seed viability, germination, seedling vigour etc., and indirect health loss such as mycotoxicosis in animals and humans by damaging specific metabolic pathways leading to damage of specific organs systems upon consumption of contaminated maize kernels (Liu et al., 2016; Abhishek et al., 2015; Munkvold, 2003; Pani et al., 2014; Adhikari et al., 2017; Pani et al., 2016). Management of F. moniliforme contamination in maize kernels can be difficult because of the lack of standard seed fungicide treatments (Zhou et al., 2018; Bacon et al., 2001).

For the past few decades control of plant diseases caused by F. moniliforme and its insect vectors can be achieved with synthetic chemical fungicides/pesticides. The huge usage of chemical fungicides to control/prevent plant diseases is inadequate owing to the development of resistance in the pathogens and its harmful effects on human beings as well as other beneficial organisms due to its residual effects (Zalila-Kolsi et al., 2016; Passone et al., 2012; Herrera et al., 2016). Therefore, there is an urgent need to find the environmentally and toxicologically safe as well as effective bioactive compounds to prevent F. moniliforme contamination in maize kernels to prevent seed related diseases and mycotoxicosis associated with F. moniliforme. It has been long recognized that natural bioactive compounds especially antimicrobial peptide or antimicrobial lipopeptide from antagonistic microorganisms towards plant pathogens is one of the best alternative for synthetic fungicides to control plant diseases (Simonetti et al., 2015; Klich et al., 1991; Pathak and Keharia, 2014). Surfactin is a well-known antimicrobial lipopeptide have received great attention recently not only for its antimicrobial activities against human pathogens but also its antimicrobial activities against plant pathogens (Cao et al., 2018; Jiang et al., 2016; Zhao et al., 2014). However, a few studies have been conducted on the antifungal activity of surfactin against mycotoxigenic phytopathogenic fungus such as F. moniliforme associated mycotoxicosis and its bio-pesticide potential remains unexplored. Hence, the present study was conducted to investigate the antifungal activity of surfactin extracted from Brevibacillus brevis KN8(2) against F. moniliforme in in vitro as well as in vivo and its impact in seed pretreatments to prevent seed related diseases and mycotoxicosis associated with F. moniliforme. Our results showed that the antifungal potential of surfactin prevents F. moniliforme contamination in maize kernels and prevents plant disease and mycotoxicosis in animal model associated with F. moniliforme.

Section snippets

Preparation of surfactin

The bacterium Brevibacillus brevis KN8(2) (NCBI Accession No. JX971445.1) was used for the production of surfactin. Surfactin was extracted using the culture filtrate of B. brevis KN8(2) by following our previous method (Krishnan et al., 2018) with slight modification. The B. brevis KN8(2) was grown in nutrient broth for 7 days at 37 °C. The fermentation broth was then acidified to pH 4.5 by using 1 N HCl and it was heated for 5 min at 50–60 °C. Then the culture broth was centrifuged at

In vitro antifungal assay

In view of the known properties of surfactin, we have now studied the feasibility of developing surfactin as bio-fungicide to control the mycotoxigenic phytopathogenic fungus such as F. moniliforme contamination in maize kernels to prevent its associated diseases in plants and animals. The antagonistic rhizosphere soil bacterium Brevibacillus brevis KN8(2) antagonistic to F. moniliforme (Fig. 1) which was isolated from rice rhizosphere soils by our research group (Krishnan et al., 2018) and

Conclusion

To conclude, the results of our present study revealed that surfactin extracted from B. brevis KN8(2) has strong antifungal activity against F. moniliforme. Further, the antifungal potential of surfactin inhibited the growth of F. moniliforme in maize kernels leads to the prevention of plant and animal diseases associated with F. moniliforme contamination in maize kernels. On the basis of these findings, surfactin extracted from B. brevis KN8(2) provides an effective bio-fungicide to prevent F.

Disclosure statement

The authors declare that they have no conflict of interest.

References (36)

  • M. Adhikari et al.

    T-2 mycotoxin: toxicological effects and decontamination strategies

    Oncotarget

    (2017)
  • C.W. Bacon et al.

    Biological control of Fusarium moniliforme in maize

    Environ. Health Perspect.

    (2001)
  • Y. Cao et al.

    Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum

    Sci. Rep.

    (2018)
  • A.E. Desjardins et al.

    Mycotoxins in plant pathogenesis

    MPMI

    (1997)
  • A. Hanano et al.

    A caleosin-like protein with peroxygenase activity mediates Aspergillus flavus development, aflatoxin accumulation, and seed infection

    Appl. Environ. Microbiol.

    (2015)
  • S.D. Herrera et al.

    Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum

    Microbiol. Res.

    (2016)
  • X. Hu et al.

    Genome-wide proteomic profiling reveals the role of dominance protein expression in heterosis in immature maize ears

    Sci. Rep.

    (2017)
  • J. Jiang et al.

    Identification of novel surfactin derivatives from NRPS modification of Bacillus subtilis and its antifungal activity against Fusarium moniliforme

    BMC Microbiol.

    (2016)
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