Comparative Genomic and Functional Analysis of c-di-GMP Metabolism and Regulatory Proteins in Bacillus velezensis LQ-3
<p>Strain LQ-3 could serve as a potential biocontrol agent against <span class="html-italic">R. cerealis</span>. (<b>A</b>,<b>B</b>) The antagonistic activity of both the strain LQ-3 (<b>A</b>) and its fermentation broth (<b>B</b>) toward <span class="html-italic">R. cerealis</span>. (<b>C</b>,<b>D</b>) The biocontrol strain LQ-3 (<b>C</b>) and fermentation broth (<b>D</b>) significantly inhibited the growth of mycelia. (<b>E</b>) The biocontrol effect of LQ-3 toward <span class="html-italic">R. cerealis</span> under different concentrations (10<sup>6</sup>, 10<sup>7</sup>, and 10<sup>8</sup> CFU/mL) on the plate. (<b>F</b>) The disease index of control and LQ-3 (10<sup>6</sup>, 10<sup>7</sup>, and 10<sup>8</sup> CFU/mL) in plate experiments. (<b>G</b>) The biocontrol effect of LQ-3 (10<sup>7</sup> CFU/mL) toward <span class="html-italic">R. cerealis</span> in a greenhouse experiment. (<b>H</b>) The disease index of control and LQ-3 (1 × 10<sup>7</sup> CFU/mL) in greenhouse experiments. Error bars indicate ± SD of three replicates. The statistical analysis was performed using GraphPad Prism 8 software by <span class="html-italic">t</span>-test and one-way ANOVA (<span class="html-italic">p</span> < 0.05). ****, <span class="html-italic">p</span> < 0.0001, and **, <span class="html-italic">p</span> < 0.01).</p> "> Figure 2
<p>Phylogenetic analysis of <span class="html-italic">B. velezensis</span> LQ-3. (<b>A</b>) The ML tree of different <span class="html-italic">Bacillus</span> strains was generated based on 806 single-copy core genes using RAxML 8.2.10. <span class="html-italic">P. polymyxa</span> M1 was used as the out-group. Percent bootstrap values (from 100 replicates) are indicated at the nodes. (<b>B</b>) Heat map of ANI values among different <span class="html-italic">Bacillus</span> strains. The numbers represent the size of ANI values.</p> "> Figure 3
<p>Pan-genomes of <span class="html-italic">B. velezensis</span> strains. (<b>A</b>) The number of specific genes for each strain of <span class="html-italic">B. velezensis</span>. The inner circle displays the core genomes shared between all strains. The unique genes for each strain are displayed in each of the outer circles. The number below the strain name represents the CDS of each strain. (<b>B</b>) The curves for <span class="html-italic">B. velezensis</span> pan-genomes and core genomes. The blue plots represent the pan-genome size of <span class="html-italic">B. velezensis</span> for each genome comparison, while the green plots represent the core genome size of <span class="html-italic">B. velezensis</span> for each genome comparison. The median values are linked to display the relationship between the number of genomes. (<b>C</b>) COG distribution of core, specific, and accessory genes present in all 30 analyzed <span class="html-italic">B. velezensis</span> strains.</p> "> Figure 3 Cont.
<p>Pan-genomes of <span class="html-italic">B. velezensis</span> strains. (<b>A</b>) The number of specific genes for each strain of <span class="html-italic">B. velezensis</span>. The inner circle displays the core genomes shared between all strains. The unique genes for each strain are displayed in each of the outer circles. The number below the strain name represents the CDS of each strain. (<b>B</b>) The curves for <span class="html-italic">B. velezensis</span> pan-genomes and core genomes. The blue plots represent the pan-genome size of <span class="html-italic">B. velezensis</span> for each genome comparison, while the green plots represent the core genome size of <span class="html-italic">B. velezensis</span> for each genome comparison. The median values are linked to display the relationship between the number of genomes. (<b>C</b>) COG distribution of core, specific, and accessory genes present in all 30 analyzed <span class="html-italic">B. velezensis</span> strains.</p> "> Figure 4
<p>The domain analysis of seven potential c-di-GMP-related proteins in <span class="html-italic">B. velezensis</span> LQ-3. (<b>A</b>) Distribution of DgcK, DgcP, YdaK, YybT, PdeH, YkuI, and DgrA in <span class="html-italic">B. velezensis</span> group. The yellow box represents the presence of a gene within a genome, and the green box indicates the absence of a gene within a genome. (<b>B</b>) Domain composition and organization of seven c-di-GMP-related proteins in <span class="html-italic">B. velezensis</span> LQ-3. The orange box indicates the conserved domain of diguanylate cyclases (DGCs), the GGDEF domain. The blue box indicates the conserved domain of phosphodiesterases (PDEs), the EAL domain.</p> "> Figure 5
<p>Analysis of conserved amino acid residues in the GGDEF, EAL, and PilZ domains. (<b>A</b>) Conservation analysis of amino acid residues in the GGDEF domain. The I site and catalytic site are highlighted with blue boxes. (<b>B</b>) Conservation analysis of amino acid residues in the EAL domain. The c-di-GMP binding site and metal binding site are marked with red boxes. (<b>C</b>) Conservation analysis of amino acid residues in the PilZ domain. The c-di-GMP binding site is identified by an orange box. The letters in the figure represent the abbreviations of amino acids.</p> "> Figure 6
<p>Structural features of the GGDEF, EAL, and PilZ domains in LQ-3 and their comparison with the corresponding templates. (<b>A</b>) The α helices, β strands, and loop regions of each domain are marked in red, yellow, and green, respectively. In the structural comparison, each domain is marked in pink, while the template domains are marked in white. Structural features of the GGDEF domain, using WspR (PDB id: 3I5C) from <span class="html-italic">P. aeruginosa</span> as the template. (<b>B</b>) The structural comparison between the GGDEF domains of LQ-3 and WspR. The SSSD and GGDEF motifs are marked in blue, corresponding to the colored boxes marking the conserved amino acid residues in the GGDEF domain. (<b>C</b>) The structural features of the EAL domain, using RmcA (PDB id: 5M3C) from <span class="html-italic">P. aeruginosa</span> as the template. (<b>D</b>) The structural comparison between the EAL domains of LQ-3 and RmcA. (<b>E</b>) Structural features of the PilZ domain, using MotI (PDB id: 5VX6) from <span class="html-italic">B. subtilis</span> as the template. (<b>F</b>) Structural comparison between the PilZ domains of LQ-3 and MotI. The RxxxR and (D/N)x(S/A)xxG motifs are marked in orange, corresponding to the colored boxes marking the conserved amino acid residues in the PilZ domain.</p> "> Figure 7
<p>Assay of biocontrol-related phenotypes of c-di-GMP-metabolism-related proteins in LQ-3. (<b>A</b>,<b>B</b>) The swarming motility test of LQ-3 (pUBXC) and its mutant strains. (<b>C</b>) The pellicle biofilm detection of LQ-3 and corresponding mutant strains. (<b>D</b>) The colony biofilm detection of LQ-3 and corresponding mutant strains. (<b>E</b>) Colonization ability detection of LQ-3 and its mutant strains in wheat roots. The statistical analysis was performed using GraphPad Prism 8 software by one-way ANOVA with the Turkey test (<span class="html-italic">p</span> < 0.05). LQ-3(pUBXC): wild-type strains containing the pUBXC plasmid; <span class="html-italic">dgcK</span>, <span class="html-italic">dgcP</span>: c-di-GMP diguanylate cyclases (DGCs); <span class="html-italic">pdeH</span>: c-di-GMP phosphodiesterases (PDEs); <span class="html-italic">ydaK</span>, <span class="html-italic">ykuI</span>: c-di-GMP receptor.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Strains and Growth Conditions
2.2. Antifungal Assay
2.3. Genome Sequencing, Assembly, and Annotation
2.4. Phylogenomic Analysis
2.5. Pan-Genome Analysis
2.6. Involvement of Proteins with Conserved Structural Domains and Quantitative Analysis in the c-di-GMP Metabolism and Regulation
2.7. Structural Analysis of Proteins Involved in c-di-GMP Metabolism and Regulation
2.8. Construction of Knockout Mutants in B. velezensis LQ-3
2.9. Bacterial Growth Rate Analysis
2.10. Swarming Motility Assay
2.11. Biofilm Formation Assay
2.12. Root Colonization Capability Assay
3. Results
3.1. Biocontrol Efficacy of B. velezensis LQ-3
3.2. Genome Features of Strain LQ-3
3.3. Phylogenetic Analysis of Strain LQ-3
3.4. Pan-genome Analysis of B. velezensis
3.5. Potential Proteins Involved in c-di-GMP Metabolism and Regulation in B. velezensis
3.6. Structural Features of the GGDEF, EAL, and PilZ Domains of B. velezensis LQ-3
3.7. C-di-GMP Regulates the Biocontrol-Related Phenotypes of B. velezensis LQ-3
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Attribute | LQ-3 |
---|---|
Genome size (bp) | 3,929,792 |
G + C (%) | 46.50 |
Protein-coding genes | 3747 |
rRNA | 27 |
tRNA | 86 |
Gene total length (bp) | 3,523,857 |
Average length of protein-coding genes (bp) | 913 |
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Li, R.; Yang, P.; Zhang, H.; Wang, C.; Zhao, F.; Liu, J.; Wang, Y.; Liang, Y.; Sun, T.; Xie, X. Comparative Genomic and Functional Analysis of c-di-GMP Metabolism and Regulatory Proteins in Bacillus velezensis LQ-3. Microorganisms 2024, 12, 1724. https://doi.org/10.3390/microorganisms12081724
Li R, Yang P, Zhang H, Wang C, Zhao F, Liu J, Wang Y, Liang Y, Sun T, Xie X. Comparative Genomic and Functional Analysis of c-di-GMP Metabolism and Regulatory Proteins in Bacillus velezensis LQ-3. Microorganisms. 2024; 12(8):1724. https://doi.org/10.3390/microorganisms12081724
Chicago/Turabian StyleLi, Rong, Panlei Yang, Hongjuan Zhang, Chunjing Wang, Fang Zhao, Jiehui Liu, Yanbin Wang, Yan Liang, Ting Sun, and Xiansheng Xie. 2024. "Comparative Genomic and Functional Analysis of c-di-GMP Metabolism and Regulatory Proteins in Bacillus velezensis LQ-3" Microorganisms 12, no. 8: 1724. https://doi.org/10.3390/microorganisms12081724