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. 2024 Apr 2;12(4):e0400823.
doi: 10.1128/spectrum.04008-23. Epub 2024 Mar 7.

Antifungal potential of lipopeptides produced by the Bacillus siamensis Sh420 strain against Fusarium graminearum

Sarfaraz Hussain #  1   2 , Bowen Tai #  1 , Maratab Ali  2 , Israt Jahan  1 , Suha Sakina  3 , Gang Wang  1 , Xinlong Zhang  4 , Yixuan Yin  4 , Fuguo Xing  1
Affiliations

Antifungal potential of lipopeptides produced by the Bacillus siamensis Sh420 strain against Fusarium graminearum

Sarfaraz Hussain et al. Microbiol Spectr. .

Abstract

Biological control is a more sustainable and environmentally friendly alternative to chemical fungicides for controlling Fusarium spp. infestations. In this work, Bacillus siamensis Sh420 isolated from wheat rhizosphere showed a high antifungal activity against Fusarium graminearum as a secure substitute for fungicides. Sh420 was identified as B. siamensis using phenotypic evaluation and 16S rDNA gene sequence analysis. An in vitro antagonistic study showed that Sh420's lipopeptide (LP) extract exhibited strong antifungal properties and effectively combated F. graminearum. Meanwhile, lipopeptides have the ability to decrease ergosterol content, which has an impact on the overall structure and stability of the plasma membrane. The PCR-based screening revealed the presence of antifungal LP biosynthetic genes in this strain's genomic DNA. In the crude LP extract of Sh420, we were able to discover several LPs such as bacillomycin, iturins, fengycin, and surfactins using ultra-high-performance liquid chromatography-quadrupole time-of-flight mass spectrometry. Microscopic investigations (fluorescent/transmission electron microscopy) revealed deformities and alterations in the morphology of the phytopathogen upon interaction with LPs. Sh420 LPs have been shown in grape tests to be effective against F. graminearum infection and to stimulate antioxidant activity in fruits by avoiding rust and gray lesions. The overall findings of this study highlight the potential of Sh420 lipopeptides as an effective biological control agent against F. graminearum infestations.IMPORTANCEThis study addresses the potential of lipopeptide (LP) extracts obtained from the strain identified as Bacillus siamensis Sh420. This Sh420 isolate acts as a crucial player in providing a sustainable and environmentally friendly alternative to chemical fungicides for suppressing Fusarium graminearum phytopathogen. Moreover, these LPs can reduce ergosterol content in the phytopathogen influencing the overall structure and stability of its plasma membrane. PCR screening provided confirmation regarding the existence of genes responsible for biosynthesizing antifungal LPs in the genomic DNA of Sh420. Several antibiotic lipopeptide compounds were identified from this bacterial crude extract using ultra-high-performance liquid chromatography-quadrupole time-of-flight mass spectrometry. Microscopic investigations revealed deformities and alterations in the morphology of F. graminearum upon interaction with LPs. Furthermore, studies on fruit demonstrated the efficacy of Sh420 LPs in mitigating F. graminearum infection and stimulating antioxidant activity in fruits, preventing rust and gray lesions.

Keywords: Bacillus siamensis; Fusarium graminearum; antifungal activity; antioxidant activity; ergosterol; lipopeptides.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig 1
Fig 1
Antifungal activity of B. siamensis Sh420 against F. graminearum in dual culture plate on PDA media at sixth of incubation at 28°C. (A) CK, a 5-mm agar plug of F. graminearum at the center of PDA plate and (B) front side of plate where Sh420 is inoculated on two sites that are 2.5 cm apart from the F. graminearum colony. (C) Back side of the dual culture plate.
Fig 2
Fig 2
Morphological features of B. siamensis Sh420. (A) Colony morphology. (B) Bacterial cells in chain form. (C) Single bacterium cells.
Fig 3
Fig 3
Antifungal activity of B. siamensis Sh420 lipopeptides against F. graminearum. Assessment of different concentrations of LPs against fungal growth: reverse side of Petri plates showing inhibition zones and control in the same plate: (A) 5 mg mL−1 LPs, (B) 4 mg mL−1 LPs, and (C) 2 mg mL−1 LPs.
Fig 4
Fig 4
MIC and MFC of lipopeptides from Sh420. +CK (positive control) medium inoculated with amphotericin B for fungal growth inhibition, while −CK (negative control) PDB inoculated with spore suspension without any treatment.
Fig 5
Fig 5
Spectrometric analysis of ergosterol profile of F. graminearum at various concentrations of lipopeptides.
Fig 6
Fig 6
TOF-MS ES + TIC of Sh420 LPs with their molecular weight (m/z) and Rt.
Fig 7
Fig 7
Effects of lipopeptides on F. graminearum. Control mycelia and spores (A). Treated mycelia and spores (B). Treated fungi showed deformation, swelling, and bulging in hyphae and spores, which are clearly visible in bright field burst or swelled portions of the hyphae, or spores had blurred images as compared to controls. TEM photographs of treated F. graminearum where red arrows showed the abnormal membranes and cell structure as compared to untreated mycelia.
Fig 8
Fig 8
Lipopeptides from Sh420 inhibited disease severity in grapes. Disease severity of gray mold on grapes. (A) Grapes treated with sterile water (negative control). (B) Grapes treated with LPs. (C) Grapes infected with Fusarium. (D) Grapes infected with both F. graminearum and LPs. (E) Graphical representation of disease severity in all four groups.
Fig 9
Fig 9
Antioxidant activity evaluated with the FRAP assay (A) and total phenols (B) of grapes treated with LPs. Control (CK), Sh420 (lipopeptide-treated), F. graminearum (Fg), and LPs+Fg. Values followed by the same letters did not differ significantly according to Duncan’s multiple range test (P < 0.05). Vertical lines represent the standard errors of the mean.
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