The Response Regulator FlmD Regulates Biofilm Formation in Comamonas testosteroni through the Transcriptional Activator SoxR
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains and Plasmids
2.2. Transcriptome Analysis by RNA-Seq
2.3. Reverse Transcription PCR (RT-PCR) and Quantitative Reverse Transcription PCR (RT-qPCR)
2.4. Biofilm Formation Assays and Growth Measurement
2.5. Genetic Cloning, Overexpression, and Protein Purification
2.6. Gel Shift Assay (EMSA)
2.7. Protein Co-Purification
2.8. Bacterial Two-Hybrid Assay
2.9. Sequence Alignment and Analysis
2.10. Statistical Analysis
3. Results
3.1. Certain Transporter Genes Regulated by FlmD
3.2. The Effect of TolC on Biofilm Formation
3.3. The Transcriptional Regulation of SoxR on the acrAB-tolC Operon
3.4. FlmD Variants Involved in Phosphorylation
3.5. The Interaction between FlmD and SoxR
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Strain/Plasmid | Relevant Genotype or Description | Sources |
---|---|---|
Strains | ||
Comamonas testosteroni | ||
CNB-1 | [25] | |
CNB-1ΔflmD | FlmD (CtCNB1_3988) disrupted in CNB-1 | [7] |
CNB-1ΔdhlC | DhlC (CtCNB1_0516) disrupted in CNB-1 | This study |
CNB-1ΔansP | AnsP (CtCNB1_0951) disrupted in CNB-1 | This study |
CNB-1ΔCtCNB1_0381 | CtCNB1_0381 disrupted in CNB-1 | This study |
CNB-1ΔacrA | AcrA (CtCNB1_0177) disrupted in CNB-1 | This study |
CNB-1ΔacrB | AcrB (CtCNB1_0178) disrupted in CNB-1 | This study |
CNB-1ΔtolC | TolC (CtCNB1_0179) disrupted in CNB-1 | This study |
CNB-1ΔsoxR | SoxR (CtCNB1_0176) disrupted in CNB-1 | This study |
Escherichia coli | ||
DH5α | F-φ80d lacZΔM15 Δ(lacZYA-argF) U169 recA1 endA1 hsdR17(rK- mK+) supE44 λ- thi-1 gyrA96 relA1 phoA; host for DNA manipulations | TransGen |
BL21(DE3) | F- ompT hsdS (rB- mB-) gal dcm (DE3) | Novagen |
XL1-Blue | MRF’ Kan, glycerol stockb (host strain for propagating pBT and pTRG recombinants) | Stratagene |
Plasmids | ||
pBBR1MCS-2 | Kmr, lacPOZ’ broad host vector with R type conjugative origin | [26] |
pBBR1MCS2-flmD | Carries flmD to generate complementation | [7] |
pBBR1MCS2-flmDD55A | A mutation from an aspartate to an alanine in 55th residue | [7] |
pBBR1MCS2-flmDD12K | A mutation from an aspartate to a lysine in 12th residue | This study |
pBBR1MCS2-soxR | Carries soxR to generate complementation | This study |
pBBR1MCS2-acrA | Carries acrA to generate complementation | This study |
pBBR1MCS2-acrB | Carries acrB to generate complementation | This study |
pBBR1MCS2-tolC | Carries tolC to generate complementation | This study |
pBBR1MCS2-soxR-his | pBBR1MCS2 derivative for expression of SoxR | This study |
pBBR1MCS2-flmDD12K-sterp + soxR-his | pBBR1MCS2 derivative for co-purification of SoxR and FlmDD12K | This study |
pBBR1MCS2-flmDD55A-sterp + soxR-his | pBBR1MCS2 derivative for co-purification of SoxR and FlmDD55A | This study |
pBBR1MCS2pfer | adds a strong constitutive promoter in pBBR1MCS-2 | [7] |
pBBR1MCS2pfer-flmD | Carries flmD to overexpression | [7] |
pET28a | Kmr, bacterial expression vector with a His-tag | Youbio |
pET28a-flmD | pET28a derivative for expression of FlmD | [7] |
pET28a-flmDD55A | pET28a derivative for expression of FlmD with D55A mutation | This study |
pET28a-flmDD12K | pET28a derivative for expression of FlmD with D12K mutation | This study |
pBT | Bacterial two-hybrid bait plasmid with λ repressor protein (λcI) | Stratagene |
pBT-cheA | pBT derivative with λcI linked to CheA | [7] |
pBT-flmDD12K | pBT derivative with λcI linked to FlmDD12K | This study |
pBT-flmDD55A | pBT derivative with λcI linked to FlmDD55A | This study |
pTRG | Bacterial two-hybrid bait plasmid with α-subunit of RNA polymerase (RNAp) | Stratagene |
pTRG-cheW | pTRG derivative with RNAp linked to CheW | [7] |
pTRG-soxR | pTRG derivative with RNAp linked to SoxR | This study |
Gene | Locus_Tag | Annotations | Padj | log2FoldChange |
---|---|---|---|---|
hmp | CtCNB1_0015 | ferredoxin | 2.39 × 102 | 1.1233 |
boxA | CtCNB1_0065 | benzoyl-CoA oxygenase | 3.01 × 103 | 1.5735 |
boxB | CtCNB1_0066 | benzoyl-CoA oxygenase | 3.81 × 1013 | 1.6828 |
boxC | CtCNB1_0067 | benzoyl-CoA-dihydrodiol lyase | 3.08 × 106 | 1.2693 |
livK1 | CtCNB1_0096 | ABC transporter permease | 6.45 × 107 | 1.249 |
bCL | CtCNB1_0097 | 4-hydroxybenzoate--CoA ligase | 2.09 × 106 | 1.1543 |
tauA | CtCNB1_0160 | ABC transporter permease | 1.48 × 109 | 1.2986 |
tauC | CtCNB1_0161 | ABC transporter permease | 8.38 × 104 | 1.1119 |
acrA | CtCNB1_0177 | RND family efflux transporter MFP subunit | 9.97 × 108 | 1.0644 |
tolC | CtCNB1_0179 | RND transporter | 1.74 × 106 | 1.2098 |
CtCNB1_0381 | CtCNB1_0381 | hypothetical protein | 4.06 × 103 | 1.108 |
caiD | CtCNB1_0392 | enoyl-CoA hydratase | 1.77 × 107 | 1.0308 |
gpmB | CtCNB1_0417 | phosphoglycerate mutase | 2.67 × 102 | 1.0422 |
dhlC | CtCNB1_0516 | SSS sodium solute transporter superfamily protein | 2.94 × 104 | 1.1811 |
araJ | CtCNB1_0518 | major facilitator transporter | 3.17 × 104 | 1.4008 |
ansP | CtCNB1_0951 | proline-specific permease | 5.09 × 105 | 1.6276 |
dadA | CtCNB1_0952 | amino acid dehydrogenase | 4.35 × 104 | 1.0916 |
livK2 | CtCNB1_1147 | twin-arginine translocation pathway signal protein | 1.94 × 103 | 1.2937 |
eutG | CtCNB1_1590 | 4-hydroxybutyrate dehydrogenase | 2.33 × 103 | 1.1806 |
CtCNB1_2363 | CtCNB1_2363 | hypothetical protein | 1.15 × 102 | 1.0003 |
soxX | CtCNB1_2868 | SoxX protein | 3.36 × 102 | 1.0829 |
soxA | CtCNB1_2869 | SoxA protein | 4.58 × 103 | 1.0581 |
soxY | CtCNB1_2871 | twin-arginine translocation pathway signal | 2.94 × 104 | 1.1995 |
soxD | CtCNB1_2872 | cytochrome C | 2.07 × 105 | 1.3067 |
CtCNB1_3408 | CtCNB1_3408 | hypothetical protein | 2.02 × 102 | 1.1134 |
dctP | CtCNB1_3427 | TRAP dicarboxylate transporter, DctP subunit | 2.54 × 1018 | 1.1641 |
ilvD | CtCNB1_3428 | phosphogluconate dehydratase | 3.83 × 1011 | 1.1086 |
eda | CtCNB1_3429 | keto-deoxy-phosphogluconate aldolase | 2.26 × 107 | 1.4534 |
livK3 | CtCNB1_3479 | ABC transporter permease | 2.97 × 103 | 1.097 |
sapF | CtCNB1_3509 | ABC-type antimicrobial peptide | 1.39 × 103 | 1.2249 |
coxL | CtCNB1_3514 | carbon monoxide dehydrogenase | 9.86 × 103 | 1.1075 |
coxS | CtCNB1_3515 | carbon monoxide dehydrogenase | 3.64 × 102 | 1.079 |
ilvB | CtCNB1_4060 | thiamine pyrophosphate-requiring enzymes | 3.64 × 103 | 1.0155 |
apbA | CtCNB1_4061 | 2-dehydropantoate 2-reductase | 1.80 × 102 | 1.4053 |
tctC | CtCNB1_4499 | ABC transporter substrate-binding protein | 9.44 × 1012 | 1.3628 |
CtCNB1_4500 | CtCNB1_4500 | hypothetical protein | 1.07 × 105 | 1.6667 |
ubiH | CtCNB1_4501 | FAD-dependent oxidoreductase | 5.75 × 104 | 1.214 |
thiJ | CtCNB1_4569 | putative intracellular protease/amidase | 2.03 × 1014 | 1.0617 |
modA | CtCNB1_4661 | extracellular solute-binding protein | 5.80 × 105 | 1.1208 |
Gene | Locus_Tag | Annotations | Padj | log2FoldChange |
---|---|---|---|---|
tolC | CtCNB1_0179 | RND transporter | 5.23 × 103 | −1.2708 |
CtCNB1_0378 | CtCNB1_0378 | hypothetical protein | 2.67 × 103 | −1.6453 |
CtCNB1_0381 | CtCNB1_0381 | hypothetical protein | 1.12 × 104 | −1.6966 |
CtCNB1_0383 | CtCNB1_0383 | hypothetical protein | 4.46 × 103 | −1.3307 |
dhlC | CtCNB1_0516 | SSS sodium solute transporter superfamily | 4.24 × 102 | −1.4034 |
ansP | CtCNB1_0951 | proline-specific permease | 1.10 × 103 | −1.3189 |
cirA | CtCNB1_1178 | TonB-dependent receptor | 6.02 × 1010 | −1.132 |
nrdA | CtCNB1_1179 | ribonucleotide reductase | 2.33 × 102 | −2.1049 |
hemS | CtCNB1_1180 | ribonucleotide reductase | 3.54 × 1020 | −1.5981 |
chuT | CtCNB1_1181 | ABC transporter substrate-binding protein | 2.26 × 1013 | −1.5584 |
fepD | CtCNB1_1182 | hemin transport system permease protein | 2.71 × 102 | −1.3963 |
fepC | CtCNB1_1183 | ABC transporter | 4.39 × 104 | −1.2717 |
fhuE | CtCNB1_1601 | ligand-gated channel protein | 1.73 × 103 | −1.2529 |
cbiK | CtCNB1_1602 | TonB-dependent receptor | 2.04 × 102 | −1.2527 |
CtCNB1_1891 | CtCNB1_1891 | hypothetical protein | 1.77 × 1019 | 1.7244 |
CtCNB1_1892 | CtCNB1_1892 | hypothetical protein | 4.26 × 105 | 1.2684 |
CtCNB1_2304 | CtCNB1_2304 | hypothetical protein | 6.55 × 103 | 1.1858 |
oafA | CtCNB1_3421 | acyltransferase | 3.30 × 104 | −1.3331 |
coxG | CtCNB1_3510 | carbon monoxide dehydrogenase subunit G | 4.97 × 102 | −1.2019 |
hppD | CtCNB1_3836 | 4-hydroxyphenylpyruvate dioxygenase | 3.02 × 1013 | −1.2022 |
CtCNB1_3837 | CtCNB1_3837 | hypothetical protein | 6.02 × 1010 | −1.0953 |
lraI | CtCNB1_3842 | ABC-type metal ion transport system | 4.71 × 102 | −1.462 |
CtCNB1_3869 | CtCNB1_3869 | hypothetical protein | 6.64 × 104 | −1.3152 |
fepA | CtCNB1_4259 | TonB-dependent receptor | 6.55 × 103 | −1.0318 |
livK1 | CtCNB1_4328 | ABC transporter permease | 5.94 × 1017 | −1.2227 |
livK2 | CtCNB1_4497 | ABC transporter permease | 2.55 × 106 | −1.2985 |
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Wang, Y.; Huang, Z.; Zhou, N.; Liu, C.; Jiang, C.; Li, D.; Liu, S. The Response Regulator FlmD Regulates Biofilm Formation in Comamonas testosteroni through the Transcriptional Activator SoxR. Microorganisms 2022, 10, 356. https://doi.org/10.3390/microorganisms10020356
Wang Y, Huang Z, Zhou N, Liu C, Jiang C, Li D, Liu S. The Response Regulator FlmD Regulates Biofilm Formation in Comamonas testosteroni through the Transcriptional Activator SoxR. Microorganisms. 2022; 10(2):356. https://doi.org/10.3390/microorganisms10020356
Chicago/Turabian StyleWang, Yunhao, Zhou Huang, Nan Zhou, Chang Liu, Chengying Jiang, Defeng Li, and Shuangjiang Liu. 2022. "The Response Regulator FlmD Regulates Biofilm Formation in Comamonas testosteroni through the Transcriptional Activator SoxR" Microorganisms 10, no. 2: 356. https://doi.org/10.3390/microorganisms10020356
APA StyleWang, Y., Huang, Z., Zhou, N., Liu, C., Jiang, C., Li, D., & Liu, S. (2022). The Response Regulator FlmD Regulates Biofilm Formation in Comamonas testosteroni through the Transcriptional Activator SoxR. Microorganisms, 10(2), 356. https://doi.org/10.3390/microorganisms10020356