Characterization of the Pyrroloquinoline Quinone Producing Rhodopseudomonas palustris as a Plant Growth-Promoting Bacterium under Photoautotrophic and Photoheterotrophic Culture Conditions
Abstract
:1. Introduction
2. Results
2.1. PQQ Synthesis Genes in Rhodopseudomonas Palustris CGA009 Genome
2.2. Transcriptional Levels of PQQ Relative Genes
2.3. Confirmation of PQQ Production in R. palustris CGA009 under Different Culturing Conditions
2.4. Phosphorus-Solubilizing Activity Assay
2.5. Estimated Siderophore Activity
2.6. R. palustris CGA009 Effect on Arabidopsis thaliana’s Growth Parameters
2.7. Identification of Diverse Endophytes in Arabidopsis following R. palustris CGA009 Inoculation
Conditions | Pellets or Supernatant | Endophyte Colony | Phosphorus-Solubilizing Activity | The Best Match with 16S rRNA Gene in BLAST Results (Identity %) | Relative Researches |
---|---|---|---|---|---|
HCO3 medium, microaerobic, light, 30 °C, 17 days | R. palustris Pellets | HP1 | No | Stenotrophomonas maltophilia (99.51%) | Plant-growth-promoting rhizobacterium against stress conditions [34] |
HP2 | Yes | Microbacterium proteolyticum (99.21%) | Endophytic bacterium isolated from roots of Halimione portulacoides [37] | ||
HP3 | Yes | Paraburkholderia pallidirosea (97.70%) 1 | Belong to plant-beneficial environmental groups of bacterium [38] | ||
Supernatant | HS1 | No | Rhodanobacter lindaniclasticus (99.17%) | A lindane-degrading bacterium [39] | |
HS2 | Yes | Rhodanobacter fulvus (99.15%) | Biological control activity towards the root-rot plant pathogen Cylindrocladium spathiphylli [40] | ||
HS3 | Yes | Rhodanobacter soli (93%) 1 | A soil bacterium from a ginseng field [41] | ||
Acetate medium, microaerobic, light, 30 °C, 8 days | R. palustris Pellets | AP1 | Yes | Burkholderia anthina (99.79%) | Plant-growth-promoting bacteria of sugarcane [35] |
Supernatant | AS1 | Yes | Pseudomonas citronellolis (95.17%) 1 | Multi-metal resistant [42] | |
FsMSG medium, microaerobic, light, 30 °C, 8 days | R. palustris Pellets | FP1 | Yes | Achromobacter insuavis (94.45%) 1 | Could be isolated from cystic fibrosis patients [43] |
FP2 | Yes | Achromobacter insuavis (99.56%) | |||
FP3 | Yes | Achromobacter insuavis (99.86%) | |||
Supernatant | FS1 | No | Paraburkholderia kururiensis (99.58) | A trichloroethylene-degrading bacterium [44] | |
FS2 | No | Ferrovibrio xuzhouensis (99.49%) | A cyhalothrin-degrading bacterium [45] | ||
FS3 | Yes | Amycolatopsis rhabdoformis (98.81%) | A soil bacterium from a tropical forest [46] |
3. Discussion
4. Materials and Methods
4.1. Culture Conditions
4.2. Transcriptome Analysis
4.3. Phosphorus-Solubilizing Activity Assay
4.4. Siderophore Estimation Assay
4.5. PQQ Extraction for LC-MS Analysis
4.6. LC-MS Method
4.7. Enzymatic PQQ Determination
4.7.1. Preparation of E. coli Membrane Fractions
4.7.2. PQQ Bioassays
4.8. Plant’s Growth Condition
4.9. Chlorophyll Content Measurements
4.10. Isolation and Identification of Endophytes
4.11. Statistic
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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PQQ Synthesis Related Genes | Conserved Protein Domain Family | References for PQQ Synthesis | Locus Tag in CGA009 (NCBI Reference Sequence: NC_005296.1) 1 |
---|---|---|---|
pqqA | PQQ_syn_pqqA (TIGR02107) | [17,22,23] | TX73_RS09945 |
pqqB | PRK05184 | [17,24,25] | TX73_RS09950 |
pqqC | PRK05157 | [17] | TX73_RS09955 |
pqqD | PqqD Superfamily (cl05126) | [17] | TX73_RS09960 |
pqqE | PRK05301 | [17,25] | TX73_RS09965 |
Peptidases | |||
pqqF | PQQ_syn_pqqF (TIGR02110) | [17] | None |
pqqL | PqqL (COG0612) | [18] | TX73_RS04330, TX73_RS22305, TX73_RS22310 |
pqqG | PqqL (COG0612) | [20] | TX73_RS04330, TX73_RS22305, TX73_RS22310 |
pqqH | DAP2 (COG1506) 2 | [26] | none |
pqqM | DAP2 (COG1506) 2 | [10] | none |
TldD | PmbA_TldD Superfamily (cl19356) | [19] | TX73_RS04255, TX73_RS05895 |
Gene Name 1 | Gene Description 2 | HCO3 (TPM) | Acetate (TPM) | log2 Ratio | p Value |
---|---|---|---|---|---|
PQQ-dependent enzyme genes | |||||
TX73_RS03805 | PQQ_dependent_sugar_dehydrogenase | 136.1 | 3.3 | 5.33 | 0.007 |
TX73_RS16265 | PQQ_dependent_dehydrogenase__methanol_ethanol_family | 298.7 | 2.5 | 6.81 | 0.006 |
TX73_RS22090 | PQQ_dependent_sugar_dehydrogenase | 18.0 | 8.5 | 1.06 | 0.429 |
PQQ synthesis genes | |||||
pqqA | pyrroloquinoline_quinone_precursor_peptide_PqqA | 2523.6 | 160.9 | 3.97 | 0.039 |
pqqB | pyrroloquinoline_quinone_biosynthesis_protein_PqqB | 159.7 | 6.9 | 4.51 | 0.016 |
pqqC | pyrroloquinoline_quinone_synthase_PqqC | 69.3 | 5.0 | 3.78 | 0.016 |
pqqD | pyrroloquinoline_quinone_biosynthesis_peptide_chaperone_PqqD | 30.5 | 1.7 | 4.12 | 0.004 |
pqqE | pyrroloquinoline_quinone_biosynthesis_protein_PqqE | 20.9 | 1.6 | 3.65 | 0.013 |
TX73_RS20405 | PqqD_family_protein | 38.3 | 7.3 | 2.39 | 0.066 |
Peptidase genes 3 | |||||
TX73_RS04330 | Predicted Zn-dependent peptidase (PqqL) | 20.7 | 35.2 | −0.76 | 0.608 |
TX73_RS22305 | Predicted Zn-dependent peptidase (PqqL) | 12.1 | 18.2 | −0.59 | 0.669 |
TX73_RS22310 | Predicted Zn-dependent peptidase (PqqL) | 13.3 | 21.6 | −0.69 | 0.620 |
tldD | PmbA_TldD Superfamily | 116.8 | 149.9 | −0.35 | 0.847 |
TX73_RS05895 | PmbA_TldD Superfamily | 15.0 | 39.7 | −1.39 | 0.357 |
Medium | Culture Condition | Culture Period (Day) | Final OD650 | Percent Siderophore Unit |
---|---|---|---|---|
HCO3 | Photoautotrophic | 17 | 0.745 | 28.9 ± 4 |
Acetate | Photoheterotrophic | 8 | 1.84 | 0 |
FsMSG | photoheterotrophic | 8 | 4.19 | 0 |
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Lo, S.-C.; Tsai, S.-Y.; Chang, W.-H.; Wu, I.-C.; Sou, N.-L.; Hung, S.-H.W.; Chiang, E.-P.I.; Huang, C.-C. Characterization of the Pyrroloquinoline Quinone Producing Rhodopseudomonas palustris as a Plant Growth-Promoting Bacterium under Photoautotrophic and Photoheterotrophic Culture Conditions. Int. J. Mol. Sci. 2023, 24, 14080. https://doi.org/10.3390/ijms241814080
Lo S-C, Tsai S-Y, Chang W-H, Wu I-C, Sou N-L, Hung S-HW, Chiang E-PI, Huang C-C. Characterization of the Pyrroloquinoline Quinone Producing Rhodopseudomonas palustris as a Plant Growth-Promoting Bacterium under Photoautotrophic and Photoheterotrophic Culture Conditions. International Journal of Molecular Sciences. 2023; 24(18):14080. https://doi.org/10.3390/ijms241814080
Chicago/Turabian StyleLo, Shou-Chen, Shang-Yieng Tsai, Wei-Hsiang Chang, I-Chen Wu, Nga-Lai Sou, Shih-Hsun Walter Hung, En-Pei Isabel Chiang, and Chieh-Chen Huang. 2023. "Characterization of the Pyrroloquinoline Quinone Producing Rhodopseudomonas palustris as a Plant Growth-Promoting Bacterium under Photoautotrophic and Photoheterotrophic Culture Conditions" International Journal of Molecular Sciences 24, no. 18: 14080. https://doi.org/10.3390/ijms241814080