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. 2021 Mar 24:12:616937.
doi: 10.3389/fmicb.2021.616937. eCollection 2021.

Inhibitory Effects of Carbazomycin B Produced by Streptomyces roseoverticillatus 63 Against Xanthomonas oryzae pv. oryzae

Tingting Shi  1 , Xin Guo  1 , Jiali Zhu  1 , Lingming Hu  1 , Zhipeng He  1 , Donghua Jiang  1
Affiliations

Inhibitory Effects of Carbazomycin B Produced by Streptomyces roseoverticillatus 63 Against Xanthomonas oryzae pv. oryzae

Tingting Shi et al. Front Microbiol. .

Abstract

The present manuscript highlights the potential role of Streptomyces roseoverticillatus 63 (Sr-63) against Xanthomonas oryzae pv. oryzae (Xoo), which is the cause of a disastrous bacterial leaf blight disease with rice worldwide. The disease suppression was achieved under greenhouse conditions. A foliar spray of the fermentation broth of Sr-63 significantly reduced the leaf blight symptoms with rice in Xoo inoculated rice plants. Furthermore, we observed that the carbazomycin B, isolated from the fermentation broth of Sr-63, was demonstrated to have antibacterial activity against Xoo with a minimum inhibitory concentration (MIC) of 8 μg mL-1. The results indicated that carbzomycin B hampered the membrane formation of Xoo, reduced the production of xanthomonadin and extracellular polymeric substance (EPS). The fourier transform infrared spectroscopic (FT-IR) indicated that carbazomycin B changed the components of the cell membrane, then caused a change of the cell surface hydrophobicity of Xoo. Scanning electron microscopy revealed that the Xoo cells treated with carbazomycin B exhibited apparent structural deformation. The results also indicated that carbazomycin B had a negative impact on the metabolism of Xoo, carbazomycin B reduced the activity of malate dehydrogenase (MDH) activity and suppressed the protein expression of Xoo. Overall, our data suggests that Streptomyces roseoverticillatus 63 is a promising biocontrol agent that could be used to combat the bacterial leaf blight diseases of rice.

Keywords: Streptomyces roseoverticillatus; Xanthomonas oryzae pv. oryzae; antibacterial mechanism; biological control; carbazomycin B.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Carbazomycin B reduced the virulence of Xanthomonas oryzae pv. oryzae (Xoo). The untreated Xoo and Xoo treated with 4 × MIC for 4 h of carbazomycin B were inoculated on rice plants. The lesion length was measured after 14 days of inoculation. Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗∗p < 0.01).
FIGURE 2
FIGURE 2
Inhibitory effect of carbazomycin B on biofilm formation of Xanthomonas oryzae pv. oryzae (Xoo). Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗p < 0.05 and ∗∗p < 0.01).
FIGURE 3
FIGURE 3
Scanning electron microscopy of Xanthomonas oryzae pv. oryzae (Xoo) treated with phosphate buffered solution (control) and various concentration of carbazomycin B for 4 h. (A) Control, (B) 1 × MIC carbazomycin B, (C) 2 × MIC carbazomycin B, and (D) 4 × MIC carbazomycin B.
FIGURE 4
FIGURE 4
Fourier transform infrared spectroscopy (FTIR) showing the chemical modifications in Xanthomonas oryzae pv. oryzae (Xoo) after 4 h of carbzomycin B (1 × MIC and 2 × MIC) treatment. The black line indicates the shift in the IR spectra compared to untreated samples.
FIGURE 5
FIGURE 5
Hydrophobicity assay of Xanthomonas oryzae pv. oryzae (Xoo) treated with different concentration of carbazomycin B for 4 h. Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗p < 0.05 and ∗∗∗p < 0.001).
FIGURE 6
FIGURE 6
Inhibition rate of exopolysaccharide substance (EPS) production of Xanthomonas oryzae pv. oryzae (Xoo) by carbazomycin B treatment for 24 h. Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗p < 0.05, ∗∗p < 0.01, and ∗∗∗p < 0.001).
FIGURE 7
FIGURE 7
Reduction in xanthomonadin of Xanthomonas oryzae pv. oryzae (Xoo) after carbazomycin B treatment for 4 h. Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗∗p < 0.01 and ∗∗∗p < 0.001).
FIGURE 8
FIGURE 8
Effect of carbazomycin B on malate dehydrogenase (MDH) activity of Xanthomonas oryzae pv. oryzae (Xoo). The Xoo cells were treated with various concentration of carbazomycin B for 4 h. Results are means of three technical replicates and the bar indicates the standard deviation. Significant differences were determined by a post hoc test (∗∗∗p < 0.001).
FIGURE 9
FIGURE 9
SDS-PAGE analysis of the change of total proteins in Xoo after treating with carbazomycin B for 4 h. Lane 1, PBS treatment as a control; lane 2, 1/2 × MIC carbazomycin B treatment for 4 h; lane 3, 1 × MIC carbazomycin B treatment for 4 h. lane 4, 2 × MIC carbazomycin B treatment for 4 h. lane 5, 4 × MIC carbazomycin B treatment for 4 h. The black arrows indicate lost protein bands.
FIGURE 10
FIGURE 10
The proposed model depicting the potential mechanism of carbazomycin B against Xoo. The spherical red dot denotes the carbazomycin B.
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