Genetic Determinants of Antagonistic Interactions and the Response of New Endophytic Strain Serratia quinivorans KP32 to Fungal Phytopathogens
Abstract
:1. Introduction
2. Results
2.1. In Vitro Inhibition of Phytopathogens by the S. quinivornas KP32 Strain
2.2. The Properties of Genome and Phylogenetic Analyses
2.3. Genes Essential for Biocontrol Activity in the KP32 Strain Genome
2.4. Determination of the Effect of Fungal Phytopathogens on the Expression of Genes Responsible for Antifungal Activity
2.5. Evaluation of Biocontrol Features of the KP32 Strain in a Biochemical Assay
3. Discussion
4. Materials and Methods
4.1. Bacterial Strains and Growth Conditions
4.2. Pathogenic Fungi
4.3. In Vitro Screening of Antagonistic Behavior of the KP32 Strain against Fungal Phytopathogens
4.3.1. Dual-Culture Assay
4.3.2. Detection of Diffusible Metabolite Production
4.3.3. Detection of Volatile Metabolites Production
4.3.4. Evaluation of the Effect of KP32 Cell-Free Culture Filtrate
4.4. Genome Sequencing and Sequence Analysis
4.5. Phylogenetic Analysis
4.6. Evaluation of the Effect of Fungal Pathogens on the Expression Level of Genes Engaged in Antifungal Activity
4.6.1. Preparation of Fungal Filtrates
4.6.2. Influence of Fungal Filtrates on Bacterial Genes Expression
4.7. Evaluation of the Effect of Fungal Pathogens on Lytic and Antioxidant Enzymes Activity
4.7.1. Lytic Enzyme Activity
4.7.2. Antioxidant Enzyme Activity
4.8. Plant Growth Promotion Features of the KP32 Strain
4.9. Colonization Features of the KP32 Strain
Utilization of Selected Organic Compounds as the Sole Source of Carbon and Energy
4.10. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
BCA | Biological Control Agents |
ISR | Induced Systemic Resistance |
N-AHLs | N-acyl-homoserine lactones |
PCR | Polymerase Chain Reaction |
VOCs | Volatile Organic Compounds |
CDS | Protein-encoding sequences |
KEGG | Kyoto Encyclopedia of Genes and Genomes |
COG | Cluster of Orthologous Genes |
NRPS | Nonribosomal Peptide-Synthetase |
DHBA | Dihydroxybenzoic Acid |
MFS | Major Facilitator Superfamily |
IAA | Indole-3-acetic acid |
TRP | Tryptophane |
CBS | Cystathionine β synthase |
CTH | Cystathionine-γ-lyase |
GTS | Glutathione S-transferases |
QS | Quorum sensing |
CAZy | Carbohydrate-Active Enzymes |
T2SS | Type II Secretion Systems |
T6SS | Type VI Secretion Systems |
T4PS | Type IV Pilus System |
GI | Genomic Islands |
RT-qPCR | quantitative reverse transcription PCR |
SA | Salicylic Acid |
ACC | 1-aminocyclopropane-1-carboxylate |
DF | Dworkin and Foster |
HCN | Hydrogen Cyanide |
SOD | Superoxide Dismutase |
CAT | Catalase |
EPS | Exopolysaccharide |
CRA | Congo Red Agar |
SEM | Scanning Electron Microscopy |
PGI | Percent Growth Inhibition |
LB | Luria-Bertani broth |
CV | Crystal Violet |
PSI | Phosphate Solubilizing Index |
CAS | Chrome azurol S |
PGPB | Plant Growth Promoting Bacteria |
PGP | Plant Growth Promotion |
PDA | Potato Dextrose Agar |
CWDEs | Cell Wall-Degrading Enzymes |
DNS | 3,5-dinitro salicylic acid |
LSD | Lowest Significant Difference |
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Attribute | Value |
---|---|
Genome size (bp) | 5,456,872 |
Contigs | 107 |
G + C content (%) | 64 |
Genes (total) | 5194 |
CDSs (total) | 5098 |
Genes (coding) | 5024 |
Protein genes | 5024 |
RNA genes | 126 |
rRNAs | 35 |
tRNAs | 72 |
ncRNAs | 12 |
Pseudogenes | 44 |
Genes assigned to COGs | 5018 |
Genes assigned to KEGG pathways | 3342 |
BioProject ID | PRJNA743191 |
BioSample ID | SAMN20003760 |
GenBank accession number | JAHTKS000000000.1 |
Enzyme’s Activity | KP32 | KP32 + RS | KP32 + FA | KP32 + CD | KP32 + SS |
---|---|---|---|---|---|
Protease (U mL−1) | 10.32 ± 0.45 a | 24.03 ± 0.21 b | 9.05 ± 0.09 c | 10.89 ± 0.10 d | 4.98 ± 0.24 e |
Amylase (U mL−1) | 0.61 ± 0.25 a | 0.64 ± 0.03 a | 0.64 ± 0.01 a | 0.21 ± 0.11 b | 0.11 ± 0.14 c |
Cellulase (U mL−1) | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a | 0.00 ± 0.00 a |
Chitinase (U mL−1) | 0.84 ± 0.12 a | 0.85 ± 0.04 b | 0.89 ± 0.21 a | 2.12 ± 0.10 c | 1.32 ± 05 d |
Catalase (U mg−1 of protein) | 2.84 ± 0.25 a | 8.49 ± 0.07 b | 4.05 ± 0.51 c | 4.89 ± 0.10 c | 2.47 ± 0.14 d |
Superoxide dismutase (U mg−1 of protein) | 0.43 ± 0.06 a | 0.32 ± 0.09 a | 0.60 ± 0.08 b | 0.32 ± 0.11 c | 0.24 ± 0.02 d |
Features | Strain KP32 |
---|---|
Plant growth promotion | |
Acetoin and 2,3-butanediol production | + |
IAA production (μg/mL) | 14.32 ± 0.12 |
SA production (μg/mL) | 5.43 ± 0.89 |
ACC deaminase production | + |
Ammonia production | + |
HCN production | + |
Siderophore production | + |
Phosphate solubilization (PSI) | 2.75 ± 11 |
Colonization properties | |
Autoaggregation (%) | |
2 h | 4.08 ± 0.21 |
24 h | 34.2 ± 0.09 |
Biofilm formation (OD590 of crystal violet) | |
24 h | 0.297 ± 0.02 |
48 h | 0.40 ± 0.12 |
72 h | 0.52 ± 0.05 |
Motility (mm) | |
Swimming (0.3%) | 3.20 ± 0.3 |
Swarming (0.5%) | 2.10 ± 0.07 |
Twitching (1%) | 0.78 ± 0.15 |
Exopolysacharydes production | + |
N-AHLs production | + |
Gene | Protein | Forward (5′-3’) | Reverse (5′-3’) | Tm (°C) | PCR Efficiency (%) | Slope | Product Size (bp) |
---|---|---|---|---|---|---|---|
gyrA | DNA gyrase subunit A | TGCGCTATATGCTGGTGGAC | GCAATTTTGGACATGCGCAC | 53.8 51.8 | 97.24 | −3.396 | 100 |
gyrB | DNA gyrase subunit B | CGGCGGCAAATTTGATGACA | AACCAGTTCCAGCTTCTCGG | 51.8 53.8 | 99.00 | −3.351 | 100 |
chiA | Chitinase | TGGAATGGCGATACCGGTAC | CCTTAAAGTTTGCCGTGCCC | 53.8 53.8 | 101.35 | −3.297 | 100 |
budA | Alpha-acetolactate decarboxylase | CGGTGTTTACGAAGGGGAGG | GAAGGCGATCAGTTCACCGT | 55.9 53.8 | 90.94 | −3.567 | 100 |
hcnC | Hydrogen cyanide synthase | ACAGCACTATCGACATGCCG | CCAGTCCAGCAGCGGATAAT | 53.8 53.8 | 106.76 | −3.178 | 100 |
iucA | Aerobactic synthase | GTATGCCCCGGAATACCAGG | CTGGGTCAGCGGATATGCTT | 55.9 53.8 | 109.00 | −3.116 | 100 |
entB | Enterobactin synthase | GATCAAGCAGGTGGTGGAGA | ATCGCTCTGCTGATTTGGCT | 53.8 51.8 | 108.20 | −3.147 | 100 |
pchB | Isochorismate pyruvate lyase | TCATTAAGCTGATCGCCCGG | ATGGCCTCAAAGCGCTCTTT | 53.8 51.8 | 105.15 | −3.202 | 100 |
katG | Catalase | GTTCACATTCCCAACTGCGC | ATCACCTTATTCCAGGCGGC | 53.8 53.8 | 105.35 | −3.201 | 100 |
sodB | Superoxide dismutase | CGGCGGCATCTTCAACAATG | GGCCAGTTTACCTTCAGGCT | 53.8 53.8 | 104.53 | −3.219 | 100 |
mtlR | Mannitol dehydrogenase | TCCCTTAAGTGAACGCCTCG | ATCGTGGCCAAACACCGTAT | 51.8 53.8 | 110.28 | −3.098 | 100 |
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Chlebek, D.; Grebtsova, V.; Piński, A.; Żur-Pińska, J.; Hupert-Kocurek, K. Genetic Determinants of Antagonistic Interactions and the Response of New Endophytic Strain Serratia quinivorans KP32 to Fungal Phytopathogens. Int. J. Mol. Sci. 2022, 23, 15561. https://doi.org/10.3390/ijms232415561
Chlebek D, Grebtsova V, Piński A, Żur-Pińska J, Hupert-Kocurek K. Genetic Determinants of Antagonistic Interactions and the Response of New Endophytic Strain Serratia quinivorans KP32 to Fungal Phytopathogens. International Journal of Molecular Sciences. 2022; 23(24):15561. https://doi.org/10.3390/ijms232415561
Chicago/Turabian StyleChlebek, Daria, Valeriia Grebtsova, Artur Piński, Joanna Żur-Pińska, and Katarzyna Hupert-Kocurek. 2022. "Genetic Determinants of Antagonistic Interactions and the Response of New Endophytic Strain Serratia quinivorans KP32 to Fungal Phytopathogens" International Journal of Molecular Sciences 23, no. 24: 15561. https://doi.org/10.3390/ijms232415561