Loading Effects of Aminoclays in Co-Culture of Two Cyanobacterial Microcystis and Anabaena Species as an Algicidal Role
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Synthesis of Aminoclays (ACs)
2.3. Mono-Culture Experiments on Cyanobacterial Strains in Presence of Aminoclay (AC)
2.4. Co-Culture Experiments on Cyanobacterial Strains in Presence of Aminoclay (AC)
2.5. Effect of Microcystis Cell (M.S.)-Free Medium Containing Aminoclay (AC) on Anabaena sp. KVSF7 (A.S.)
2.6. Data Collection
2.7. Statistical Tests
3. Results
3.1. Cell Growth of Mono-Culture of Cyanobacterial Strains in Presence of Aminoclay (AC)
3.2. Cell Growth of Co-Culture of Two Cyanobacterial Strains in the Presence of Aminoclay (AC)
3.3. Reactive Oxygen Species (ROS) Formation in Cyanobacterial Co-Culture in Presence of Aminoclay (AC)
3.4. Zeta Potentials of Aminoclays for Two Microalgal Species
3.5. Effects of Microcystis sp. KW Cell-Free Medium and CaAC on Anabaena sp. KVSF7
3.6. Microalgal Cell Disruptions in Aminoclay (AC)-Treated Cultures
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Anderson, D.M. Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast. Manag. 2009, 52, 342–347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kirkpatrick, B.; Fleming, L.E.; Squicciarini, D.; Backer, L.C.; Clark, R.; Abraham, W.; Benson, J.; Cheng, Y.S.; Johnson, D.; Pierce, R. Literature review of Florida red tide: Implications for human health effects. Harmful Algae 2004, 3, 99–115. [Google Scholar] [CrossRef] [Green Version]
- Kim, C.S.; Lee, S.G.; Lee, C.K.; Kim, H.G.; Jung, J. Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J. Plankton Res. 1999, 21, 2105–2115. [Google Scholar] [CrossRef]
- Han, P.; Lu, Q.; Fan, L.; Zhou, W. A review on the use of microalgae for sustainable aquaculture. Appl. Sci. 2019, 9, 2377. [Google Scholar] [CrossRef] [Green Version]
- Inaba, N.; Kodama, I.; Nagai, S.; Shiraishi, T.; Matsuno, K.; Yamaguchi, A.; Imai, I. Distribution of Harmful Algal Growth-Limiting Bacteria on Artificially Introduced Ulva and Natural Macroalgal Beds. Appl. Sci. 2020, 10, 5658. [Google Scholar] [CrossRef]
- Kim, H. Mitigation and controls of HABs. In Ecology of Harmful Algae; Springer: Berlin/Heidelberg, Germany, 2006; pp. 327–338. [Google Scholar]
- Hallegraeff, G.M. A review of harmful algal blooms and their apparent global increase. Phycologia 1993, 32, 79–99. [Google Scholar] [CrossRef] [Green Version]
- Anderson, D.M. Turning back the harmful red tide. Nature 1997, 388, 513–514. [Google Scholar] [CrossRef]
- Diaz, R.J.; Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 2008, 321, 926–929. [Google Scholar] [CrossRef] [PubMed]
- Yang, K.; Chen, Q.; Zhang, D.; Zhang, H.; Lei, X.; Chen, Z.; Li, Y.; Hong, Y.; Ma, X.; Zheng, W. The algicidal mechanism of prodigiosin from Hahella sp. KA22 against Microcystis aeruginosa. Sci. Rep. 2017, 7, 7750. [Google Scholar] [CrossRef] [Green Version]
- Kang, Y.-H.; Kang, S.-K.; Park, C.-S.; Joo, J.-H.; Lee, J.-W.; Han, M.-S. Use of lactic acid bacteria as a biological agent against the cyanobacterium Anabaena flos-aquae. J. Appl. Phycol. 2016, 28, 1747–1757. [Google Scholar] [CrossRef]
- Haughey, M.; Anderson, M.; Whitney, R.; Taylor, W.; Losee, R. Forms and fate of Cu in a source drinking water reservoir following CuSO4 treatment. Water Res. 2000, 34, 3440–3452. [Google Scholar] [CrossRef]
- Chambouvet, A.; Morin, P.; Marie, D.; Guillou, L. Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 2008, 322, 1254–1257. [Google Scholar] [CrossRef] [Green Version]
- Jeong, H.J.; Kim, J.S.; YOO, Y.D.; Kim, S.T.; Kim, T.H.; Park, M.G.; Lee, C.H.; Seong, K.A.; Rang, N.S.; Shim, J.H. Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: A potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol. 2003, 50, 274–282. [Google Scholar] [CrossRef] [PubMed]
- Yu, Z.; Song, X.; Cao, X.; Liu, Y. Mitigation of harmful algal blooms using modified clays: Theory, mechanisms, and applications. Harmful Algae 2017, 69, 48–64. [Google Scholar] [CrossRef]
- Choi, M.-H.; Lee, S.C.; Oh, Y.-K.; Lee, H.U.; Lee, Y.-C. Clay-based Management for Removal of Harmful Red Tides in Korea: A Multi-perspective Approach. J. Mar. Biosci. Biotechnol. 2014, 6, 17–25. [Google Scholar] [CrossRef] [Green Version]
- Sengco, M.R.; Anderson, D.M. Controlling harmful algal blooms through clay flocculation 1. J. Eukaryot. Microbiol. 2004, 51, 169–172. [Google Scholar] [CrossRef]
- Sengco, M.R.; Li, A.; Tugend, K.; Kulis, D.; Anderson, D.M. Removal of red-and brown-tide cells using clay flocculation. I. Laboratory culture experiments with Gymnodinium breve and Aureococcus anophagefferens. Mar. Ecol. Prog. Ser. 2001, 210, 41–53. [Google Scholar] [CrossRef]
- Lee, Y.-C.; Jin, E.; Jung, S.W.; Kim, Y.-M.; Chang, K.S.; Yang, J.-W.; Kim, S.-W.; Kim, Y.-O.; Shin, H.-J. Utilizing the algicidal activity of aminoclay as a practical treatment for toxic red tides. Sci. Rep. 2013, 3, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Archambault, M.-C.; Bricelj, V.M.; Grant, J.; Anderson, D.M. Effects of suspended and sedimented clays on juvenile hard clams, Mercenaria mercenaria, within the context of harmful algal bloom mitigation. Mar. Biol. 2004, 144, 553–565. [Google Scholar]
- Datta, K.; Achari, A.; Eswaramoorthy, M. Aminoclay: A functional layered material with multifaceted applications. J. Mater. Chem. A 2013, 1, 6707–6718. [Google Scholar] [CrossRef]
- Bui, V.K.H.; Park, D.; Lee, Y.-C. Aminoclays for biological and environmental applications: An updated review. Chem. Eng. J. 2018, 336, 757–772. [Google Scholar] [CrossRef]
- Lee, Y.-C.; Park, W.-K.; Yang, J.-W. Removal of anionic metals by amino-organoclay for water treatment. J. Hazard. Mater. 2011, 190, 652–658. [Google Scholar] [CrossRef]
- Patil, A.J.; Mann, S. Self-assembly of bio-inorganic nanohybrids using organoclay building blocks. J. Mater. Chem. 2008, 18, 4605–4615. [Google Scholar] [CrossRef]
- Patil, A.J.; Li, M.; Dujardin, E.; Mann, S. Novel bioinorganic nanostructures based on mesolamellar intercalation or single-molecule wrapping of DNA using organoclay building blocks. Nano Lett. 2007, 7, 2660–2665. [Google Scholar] [CrossRef]
- Farooq, W.; Lee, H.U.; Huh, Y.S.; Lee, Y.-C. Chlorella vulgaris cultivation with an additive of magnesium-aminoclay. Algal Res. 2016, 17, 211–216. [Google Scholar] [CrossRef]
- Kim, Y.-E.; Matter, I.A.; Lee, N.; Jung, M.; Lee, Y.-C.; Choi, S.-A.; Lee, S.Y.; Kim, J.R.; Oh, Y.-K. Enhancement of astaxanthin production by Haematococcus pluvialis using magnesium aminoclay nanoparticles. Bioresour. Technol. 2020, 307, 123270. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.-C.; Kim, E.J.; Ko, D.A.; Yang, J.-W. Water-soluble organo-building blocks of aminoclay as a soil-flushing agent for heavy metal contaminated soil. J. Hazard. Mater. 2011, 196, 101–108. [Google Scholar] [CrossRef]
- Yang, L.; Lee, Y.-C.; Kim, M.I.; Park, H.G.; Huh, Y.S.; Shao, Y.; Han, H.-K. Biodistribution and clearance of aminoclay nanoparticles: Implication for in vivo applicability as a tailor-made drug delivery carrier. J. Mater. Chem. B 2014, 2, 7567–7574. [Google Scholar] [CrossRef]
- Ma, Z.; Fang, T.; Thring, R.W.; Li, Y.; Yu, H.; Zhou, Q.; Zhao, M. Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris. Harmful Algae 2015, 48, 21–29. [Google Scholar] [CrossRef]
- Li, Y.; Li, D. Competition between toxic Microcystis aeruginosa and nontoxic Microcystis wesenbergii with Anabaena PCC7120. J. Appl. Phycol. 2012, 24, 69–78. [Google Scholar] [CrossRef] [Green Version]
- Chia, M.A.; Jankowiak, J.G.; Kramer, B.J.; Goleski, J.A.; Huang, I.-S.; Zimba, P.V.; do Carmo Bittencourt-Oliveira, M.; Gobler, C.J. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions. Harmful Algae 2018, 74, 67–77. [Google Scholar] [CrossRef] [PubMed]
- Choi, M.-H.; Hwang, Y.; Lee, H.U.; Kim, B.; Lee, G.-W.; Oh, Y.-K.; Andersen, H.R.; Lee, Y.-C.; Huh, Y.S. Aquatic ecotoxicity effect of engineered aminoclay nanoparticles. Ecotoxicol. Environ. Saf. 2014, 102, 34–41. [Google Scholar] [CrossRef] [PubMed]
- Sukenik, A.; Eshkol, R.; Livne, A.; Hadas, O.; Rom, M.; Tchernov, D.; Vardi, A.; Kaplan, A. Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): A novel allelopathic mechanism. Limnol. Oceanogr. 2002, 47, 1656–1663. [Google Scholar] [CrossRef]
- Dunker, S.; Jakob, T.; Wilhelm, C. Contrasting effects of the cyanobacterium M icrocystis aeruginosa on the growth and physiology of two green algae, O ocystis marsonii and S cenedesmus obliquus, revealed by flow cytometry. Freshw. Biol. 2013, 58, 1573–1587. [Google Scholar] [CrossRef]
- Do Carmo Bittencourt-Oliveira, M.; Chia, M.A.; de Oliveira, H.S.B.; Araújo, M.K.C.; Molica, R.J.R.; Dias, C.T.S. Allelopathic interactions between microcystin-producing and non-microcystin-producing cyanobacteria and green microalgae: Implications for microcystins production. J. Appl. Phycol. 2015, 27, 275–284. [Google Scholar] [CrossRef]
- Zhang, X.-W.; Fu, J.; Song, S.; Zhang, P.; Yang, X.-H.; Zhang, L.-R.; Luo, Y.; Liu, C.-H.; Zhu, H.-L. Interspecific competition between Microcystis aeruginosa and Anabaena flos-aquae from Taihu Lake, China. Z. Naturforsch. C 2014, 69, 53–60. [Google Scholar] [CrossRef]
- Barreiro, A.; Hairston, N.G., Jr. The influence of resource limitation on the allelopathic effect of Chlamydomonas reinhardtii on other unicellular freshwater planktonic organisms. J. Plankton Res. 2013, 35, 1339–1344. [Google Scholar] [CrossRef] [Green Version]
- Hiltunen, T.; Barreiro, A.; Hairston, N.G., Jr. Mixotrophy and the toxicity of Ochromonas in pelagic food webs. Freshw. Biol. 2012, 57, 2262–2271. [Google Scholar] [CrossRef]
- Berman-Frank, I.; Lundgren, P.; Falkowski, P. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 2003, 154, 157–164. [Google Scholar] [CrossRef]
- Yu, B.P. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 1994, 74, 139–162. [Google Scholar] [CrossRef]
- Pan, G.; Chen, J.; Anderson, D.M. Modified local sands for the mitigation of harmful algal blooms. Harmful Algae 2011, 10, 381–387. [Google Scholar] [CrossRef] [Green Version]
- Lee, Y.-C.; Huh, Y.S.; Farooq, W.; Chung, J.; Han, J.-I.; Shin, H.-J.; Jeong, S.H.; Lee, J.-S.; Oh, Y.-K.; Park, J.-Y. Lipid extractions from docosahexaenoic acid (DHA)-rich and oleaginous Chlorella sp. biomasses by organic-nanoclays. Bioresour. Technol. 2013, 137, 74–81. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, M.K.; Moon, J.-Y.; Bui, V.K.H.; Oh, Y.-K.; Lee, Y.-C. Recent advanced applications of nanomaterials in microalgae biorefinery. Algal Res. 2019, 41, 101522. [Google Scholar] [CrossRef]
- Jung, S.W.; Yun, S.M.; Yoo, J.W.; Zhun, L.; Jang, P.-G.; Lim, D.-I.; Lee, Y.-C.; Lee, H.U.; Lee, T.-K.; Heo, J. Can the algicidal material Ca-aminoclay be harmful when applied to a natural ecosystem? An assessment using microcosms. J. Hazard. Mater. 2015, 298, 178–187. [Google Scholar] [CrossRef]
- Batterton, J.; Winters, K.; Van Baalen, C. Anilines: Selective toxicity to blue-green algae. Science 1978, 199, 1068–1070. [Google Scholar] [CrossRef]
- Elimelech, M.; Phillip, W.A. The future of seawater desalination: Energy, technology, and the environment. Science 2011, 333, 712–717. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nguyen, M.K.; Bui, V.K.H.; Ahn, C.-Y.; Oh, H.-M.; Koh, J.-S.; Moon, J.-Y.; Lee, Y.-C. Loading Effects of Aminoclays in Co-Culture of Two Cyanobacterial Microcystis and Anabaena Species as an Algicidal Role. Appl. Sci. 2021, 11, 5607. https://doi.org/10.3390/app11125607
Nguyen MK, Bui VKH, Ahn C-Y, Oh H-M, Koh J-S, Moon J-Y, Lee Y-C. Loading Effects of Aminoclays in Co-Culture of Two Cyanobacterial Microcystis and Anabaena Species as an Algicidal Role. Applied Sciences. 2021; 11(12):5607. https://doi.org/10.3390/app11125607
Chicago/Turabian StyleNguyen, Minh Kim, Vu Khac Hoang Bui, Chi-Yong Ahn, Hee-Mock Oh, Jin-Soo Koh, Ju-Young Moon, and Young-Chul Lee. 2021. "Loading Effects of Aminoclays in Co-Culture of Two Cyanobacterial Microcystis and Anabaena Species as an Algicidal Role" Applied Sciences 11, no. 12: 5607. https://doi.org/10.3390/app11125607
APA StyleNguyen, M. K., Bui, V. K. H., Ahn, C. -Y., Oh, H. -M., Koh, J. -S., Moon, J. -Y., & Lee, Y. -C. (2021). Loading Effects of Aminoclays in Co-Culture of Two Cyanobacterial Microcystis and Anabaena Species as an Algicidal Role. Applied Sciences, 11(12), 5607. https://doi.org/10.3390/app11125607