Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells
Abstract
:1. Introduction
2. Results
2.1. Enzyme Inhibition
2.2. Effects on F-actin
2.2.1. Morphological Alterations
2.2.2. F-actin Fluorescence Intensity Measurements
2.3. Effects on Microtubules and Chromatin
2.4. Induction of Oxidative Stress
3. Discussion
4. Materials and Methods
4.1. Culture of Cyanobacteria, Biomass Collection, and Preparation of Extracts
Taxonomic Order | Strain | Habitat | Lifestyle | Detection of MCs | References |
---|---|---|---|---|---|
Chroococcales | Microcystis flos-aquae TAU-MAC 1410 | Freshwater | Planktic | + | [29,59] |
Microcystis viridis TAU-MAC 1810 | Freshwater | Planktic | − | [29,59] | |
Microcystis sp. TAU-MAC 2410 | Freshwater | Planktic | + | [29,59] | |
Synechococcales | Synechococcus sp. TAU-MAC 0499 | Freshwater | Planktic | − | [29,59] |
Jaaginema sp. TAU-MAC 0110 | Freshwater | Planktic | − | [29,59] | |
Jaaginema sp. TAU-MAC 0210 | Freshwater | Planktic | − | [29,59] | |
Nostocales | Calothrix epiphytica TAU-MAC 0399 | Freshwater | Epiphytic | − | [29,59] |
Chlorogloeopsis fritschii TAU-MAC 0599 | Freshwater | Epiphytic | − | [29,59] | |
Raphidiopsis raciborskii TAU-MAC 1414 | Freshwater | Planktic | + 1 | [59,60] | |
Trichormus variabilis TAU-MAC 1614 | Freshwater | Planktic | + | Unpublished data | |
Nostoc oryzae TAU-MAC 0315 | Freshwater | Epiphytic | − | Unpublished data | |
Nodularia sp. TAU-MAC 0717 | Brackish | Planktic | − | Unpublished data | |
Scytonema sp. TAU-MAC 1218 | Terrestrial cave | Epilithic | − | Unpublished data | |
Oscillatoriales | Planktothrix agardhii TAU-MAC 0514 | Freshwater | Planktic | − | [29,59] |
Phormidium sp. TAU-MAC 0517 | Terrestrial cave | Epilithic | − | Unpublished data | |
Lyngbya sp. TAU-MAC 4418 | Intertidal zone | Epilithic | − | Unpublished data |
4.2. Enzyme Inhibition Assays
4.2.1. Protein Phosphatase Inhibition Assay
4.2.2. Trypsin Inhibition Assay
4.2.3. Elastase Inhibition Assay
4.3. Plant Material and Treatments
4.4. Cytoskeletal Studies
4.4.1. Tubulin Immunolabeling
4.4.2. F-actin Labeling
4.4.3. Confocal Fluorescence Microscopy
4.4.4. Fluorescence Intensity Measurements
4.5. Detection of Hydrogen Peroxide Production
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
CLSM | Confocal laser scanning microscope |
CTCF | Corrected total cell fluorescence |
DAPI | 4′,6-diamidino-2-phenylindole |
DCF-DA | 2,7-dichlorofluorescein diacetate |
DMSO | Dimethyl sulfoxide |
LC–MS/MS | Liquid chromatography with tandem mass spectrometry |
MC | Microcystin |
MC+ | Microcystin-rich |
MC− | Microcystin-devoid |
PBS | Phosphate buffer saline |
PEM | PIPES EGTA MgSO4 |
PFA | Paraformaldehyde |
PPB | Preprophase band |
PP1 | Protein phosphatase 1 |
PP2A | Protein phosphatase 2A |
ROS | Reactive oxygen species |
Appendix A
Taxonomic Order | Strain | Culture Medium | References |
---|---|---|---|
Chroococcales | Microcystis flos-aquae TAU-MAC 1410 | BG-11 | [61,69] |
Microcystis viridis TAU-MAC 1810 | BG-11 | ||
Microcystis sp. TAU-MAC 2410 | BG-11 | ||
Synechococcales | Synechococcus sp. TAU-MAC 0499 | BG-11 | |
Jaaginema sp. TAU-MAC 0110 | BG-11 | ||
Jaaginema sp. TAU-MAC 0210 | BG-11 | ||
Nostocales | Calothrix epiphytica TAU-MAC 0399 | BG-110 | |
Chlorogloeopsis fritschii TAU-MAC 0599 | BG-110 | ||
Raphidiopsis raciborskii TAU-MAC 1414 | BG-110 | ||
Trichormus variabilis TAU-MAC 1614 | BG-110 | ||
Nostoc oryzae TAU-MAC 0315 | BG-110 | ||
Nodularia sp. TAU-MAC 0717 | MN0 | ||
Scytonema sp. TAU-MAC 1218 | BG-110 | ||
Oscillatoriales | Planktothrix agardhii TAU-MAC 0514 | BG-11 | |
Phormidium sp. TAU-MAC 0517 | BG-11 | ||
Lyngbya sp. TAU-MAC 4418 | MN |
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MCs Production Status | TAU-MAC Strain | PP1 1 | Trypsin 1 | Elastase 2 |
---|---|---|---|---|
MC-producing | Microcystis flos-aquae 1410 | + | − | + |
Microcystis sp. 2410 | + | − | + | |
Trichormus variabilis 1614 | + | + | + | |
Raphidiopsis raciborskii 1414 3 | − | − | + | |
Non-MC-producing | Jaaginema sp. 0110 | − | − | + |
Jaaginema sp. 0210 | − | − | + | |
Microcystis viridis 1810 | − | − | + | |
Synechococcus sp. 0499 | − | − | + | |
Chlorogloeopsis fritschii 0599 | − | − | + | |
Calothrix epiphytica 0399 | − | − | + | |
Planktothrix agardhii 0514 | − | − | + | |
Phormidium sp. 0517 | − | − | + | |
Scytonema sp. 1218 | − | − | + | |
Nostoc oryzae 0315 | − | − | + | |
Lyngbya sp. 4418 | − | − | + | |
Nodularia sp. 0717 | − | − | − |
MCs Production Status | TAU-MAC Strain | F-actin | Microtubules | H2O2 Levels |
---|---|---|---|---|
MC-producing | Microcystis flos-aquae 1410 | ✓ | ✓ | ✓ |
Microcystis sp. 2410 | ✓ | ✓ | ✓ | |
Trichormus variabilis 1614 | ✓ | ✓ | ✓ | |
Raphidiopsis raciborskii 1414 1 | ✓ | ✓ 3 | ✘ | |
Non-MC-producing | Jaaginema sp. 0110 | ✓ | ✓ | ✓ |
Jaaginema sp. 0210 | ✓ | ✓ | ✓ | |
Microcystis viridis 1810 | ✓ | ✓ | ✓ | |
Synechococcus sp. 0499 | ✓ | ✓ 3 | ✘ | |
Chlorogloeopsis fritschii 0599 | ✓ | ✓ 3 | ✘ | |
Planktothrix agardhii 0514 | ✓ | ✓ 3,4 | ✘ | |
Calothrix epiphytica 0399 | ✓ | ✘ | ✘ | |
Phormidium sp. 0517 | ✓ | ✘ | ✘ | |
Scytonema sp. 1218 | ✓ | ✘ | ✘ | |
Nostoc oryzae 0315 | ✓ 2 | ✘ | ✘ | |
Lyngbya sp. 4418 | ✓ 2 | ✘ | ✘ | |
Nodularia sp. 0717 | ✘ | ✘ | ✘ |
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Pappas, D.; Panou, M.; Adamakis, I.-D.S.; Gkelis, S.; Panteris, E. Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells. Int. J. Mol. Sci. 2020, 21, 9649. https://doi.org/10.3390/ijms21249649
Pappas D, Panou M, Adamakis I-DS, Gkelis S, Panteris E. Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells. International Journal of Molecular Sciences. 2020; 21(24):9649. https://doi.org/10.3390/ijms21249649
Chicago/Turabian StylePappas, Dimitris, Manthos Panou, Ioannis-Dimosthenis S. Adamakis, Spyros Gkelis, and Emmanuel Panteris. 2020. "Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells" International Journal of Molecular Sciences 21, no. 24: 9649. https://doi.org/10.3390/ijms21249649