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Experimental removal of Alexandrium tamarense cells using sulfobetaines and their modified clays

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Abstract

To find new chemical modifiers and new modified clays with excellent algae removal efficiency, the removal effects of betaine and five sulfobetaines including octyl sulfobetaine, caprylyl sulfobetaine, lauryl sulfobetaine, myristyl sulfobetaine, and palmityl sulfobetaine (SB3-16) against the harmful alga Alexandrium tamarense were observed. Betaine and the five sulfobetaines exhibited certain removal effects against A. tamarense with the highest removal efficiency by SB3-16. Hence, a series of modified clay, montmorillonite (MMT) intercalated by SB3-16 were prepared, and their removal efficiencies were evaluated. The organo-clay with 11 wt% of SB3-16 exhibited the highest removal efficiency against A. tamarense cells. Combining the environmentally benign nature of SB3-16 and the high efficiency of SB3-16 modified clay against A. tamarense, SB3-16 modified clay could be a favorable choice to control harmful algal blooms (HABs) of this species.

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References

  • Aldred N, Li G, Gao Y, Clare AS, Jiang S (2010) Modulation of barnacle (Balanus amphitrite Darwin) cyprid settlement behavior by sulfobetaine and carboxybetaine methacrylate polymer coatings. Biofouling 26:673–683

    Article  CAS  PubMed  Google Scholar 

  • Anderson DM (1997) Turning back the harmful red tide. Nature 388:513–514

  • Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52:342–347

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann Rev Mar Sci 4:143–176

    Article  PubMed  Google Scholar 

  • Archambault MC, Bricelj VM, Grant J, Anderson DM (2004) Effects of suspended and sedimented clays on juvenile hard clams, Mercenaria mercenaria, within the context of harmful algal bloom mitigation. Mar Biol 144:553–565

    Article  Google Scholar 

  • Awad WH, Gilman JW, Nyden M, Harris RH, Sutto TE, Callahan J, Trulove PC, DeLong HC, Fox DM (2004) Thermal degradation studies of alkyl-imidazolium salts and their application in nanocomposites. Thermochim Acta 409:3–11

    Article  CAS  Google Scholar 

  • Baek S, Shin K, Son M, Bae S, Cho H, Na D, Kim Y, Kim S (2014) Algicidal effects of yellow clay and the thiazolidinedione derivative TD49 on the fish-killing dinoflagellate Cochlodinium polykrikoides in mesocosm experiments. J Appl Phycol 26:2367–2378

    Article  CAS  Google Scholar 

  • Cao XH, Yu ZM (2003) Extinguishment of harmful algae by organo-clay. Chin J Appl Ecol 14:1169–1172 (in Chinese, with English abstract)

    CAS  Google Scholar 

  • Cervantes-Uc JM, Cauich-Rodriguez JV, Vazquez-Torres H, Garfias-Mesias LF, Paul DR (2007) Thermal degradation of commercially available organoclays studied by TGA-FTIR. Thermochim Acta 457:92–102

    Article  CAS  Google Scholar 

  • Chen J, Pan G (2012) Harmful algal blooms mitigation using clay/soil/sand modified with xanthan and calcium hydroxide. J Appl Phycol 24:1183–1189

    Article  CAS  Google Scholar 

  • Chen SG, Chen SJ, Jiang S, Mo YM, Luo JX, Tang JN, Ge ZC (2011) Study of zwitterionic sulfopropylbetaine containing reactive siloxanes for application in antibacterial materials. Colloids Surf B 85:323–329

    Article  CAS  Google Scholar 

  • Cosmetic Ingredient Review. Safety assessment of alkyl betaines as used in cosmetics (2014) http://www.cir-safety.org/sites/default/files/alkbet032014final_0.pdf.

  • Cosquer A, Ficamos M, Jebbar M, Corbel JC, Choquet G, Fontenelle C, Uriac P, Bernard T (2004) Antibacterial activity of glycine betaine analogues: involvement of osmoporters. Bioorgan Med Chem Let 14:2061–2065

    Article  CAS  Google Scholar 

  • Craig SAS (2004) Betaine in human nutrition. Am J Clin Nutr 80:539–549

    CAS  PubMed  Google Scholar 

  • Davies J, Ward RS, Hodges G, Roberts DW (2004) Quantitative structure-activity relationship modeling of acute toxicity of quaternary alkylammonium sulfobetaines to Daphnia magna. Environ Toxicol Chem 23:2111–2115

    Article  CAS  PubMed  Google Scholar 

  • Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642

    Article  CAS  PubMed  Google Scholar 

  • Dong SJ, Li YL, Song YB, Zhi LF (2013) Synthesis, characterization and performance of unsaturated long-chain carboxybetaine and hydroxy sulfobetaine. J Surfact Deterg 16:523–529

    Article  CAS  Google Scholar 

  • Ernst R, Arditti J (1984) Biological effects of surfactants VII. Growth and development of Brassocatleya (Orchidaceae) seedlings. New Phytol 96: 197–205

  • Felix N, Sudharsan M (2004) Effect of glycine betaine, a feed attractant affecting growth and feed conversion of juvenile freshwater prawn Macrobrachium rosenbergii. Aquacult Nutrit 10:193–197

    Article  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hagström JA, Sengco MR, Villareal TA (2010) Potential methods for managing Prymnesium parvum blooms and toxicity, with emphasis on clay and barley straw: a review. J Am Wat Res Assoc 46:187–198

    Article  Google Scholar 

  • Han MY, Kim W (2001) A theoretical consideration of algae removal with clays. Microchem J 68:157–161

    Article  CAS  Google Scholar 

  • Hayes KC, Pronczuk A, Cook MW, Robbins MC (2003) Betaine in sub-acute and sub-chronic rat studies. Food Chem Toxicol 41:1685–700

    Article  CAS  PubMed  Google Scholar 

  • Kamaya Y, Kurogi Y, Suzuki K (2003) Acute toxicity of fatty acids to the freshwater green alga Selenastrum capricornutum. Environ Toxicol 18:289–294

    Article  CAS  PubMed  Google Scholar 

  • Lagaly G (1986) Interaction of alkylamines with different types of layered compounds. Solid State Ionics 22:43–51

    Article  CAS  Google Scholar 

  • Lee YJ, Choi JK, Kim EK, Youn SH, Yang EJ (2008) Field experiments on mitigation of harmful algal blooms using a sophorolipid-yellow clay mixture and effects on marine plankton. Harmful Algae 7:154–162

    Article  Google Scholar 

  • Lewis MA, Dantin DD, Walker CC, Kurtz JC, Greene RM (2003) Toxicity of clay flocculation of the toxic dinoflagellate, Karenia brevis, to estuarine invertebrates and fish. Harmful Algae 2:235–246

    Article  Google Scholar 

  • Li YH, Wu T, Yang WD, Li HY, Liu JS (2014) The effectiveness of five natural products against the three harmful algae. Water Environ J 28:270–276

    Article  CAS  Google Scholar 

  • Lindstedt M, Allenmark S, Thompson RA, Edebo L (1990) Antimicrobial activity of betaine esters, quaternary ammonium amphiphiles which spontaneously hydrolyze into nontoxic components. Antimicrob Agents Chemother 34:1949–1954

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu G, Fan C, Zhong J, Zhang L, Ding S, Yan S, Han S (2010) Using hexadecyl trimethyl ammonium bromide (CTAB) modified clays to clean the Microcystis aeruginosa blooms in Lake Taihu, China. Harmful Algae 9:413–418

    Article  CAS  Google Scholar 

  • Padilla LV, San Diego-McGlone ML, Azanza RV (2010) Exploring the potential of clay in mitigating Pyrodinium bahamense var. compressum and other harmful algal species in the Philippines. J Appl Phycol: 761–768

  • Pan G, Zhang MM, Chen H, Zou H, Yan H (2006) Removal of cyanobacterial blooms in Taihu Lake using local soils. I. Equilibrium and kinetic screening on the flocculation of Microcystis aeruginosa using commercially available clays and minerals. Environ Pollut 141:195–200

    Article  CAS  PubMed  Google Scholar 

  • Pavlić Ž, Vidaković-Cifrek Ž, Puntarić D (2005) Toxicity of surfactants to green microalgae Pseudokirchneriella subcapitata and Scenedesmus subspicatus and to marine diatoms Phaeodactylum tricornutum and Skeletonema costatum. Chemosphere 61:1061–1068

    Article  PubMed  Google Scholar 

  • Pierce RH, Henry MS, Higham CJ, Blum P, Sengco MR, Anderson DM (2004) Removal of harmful algal cells (Karenia brevis) and toxins from seawater culture by clay flocculation. Harmful Algae 3:141–148

    Article  Google Scholar 

  • Quintana R, Jańczewski D, Vasantha VA, Jana S, Lee SS, Parra-Velandia FJ, Guo S, Parthiban A, Teo SL, Vancso GJ (2014) Sulfobetaine-based polymer brushes in marine environment: is there an effect of the polymerizable group on the antifouling performance? Colloids Surf B: Biointerfaces 120:118–24

    Article  CAS  PubMed  Google Scholar 

  • Röderer G (1987) Toxic effects of tetraethyl lead and its derivatives on the chrysophyte Poterioochromonas malhamensis. VIII. Comparative studies with surfactants. Arch Environ Contam Toxicol 16:291–301

    Article  PubMed  Google Scholar 

  • Sengco MR (2009) Prevention and control of Karenia brevis blooms. Harmful Algae 8:623–628

    Article  CAS  Google Scholar 

  • Sengco MR, Anderson DM (2004) Controlling harmful algal blooms through clay flocculation. J Eukaryor Microbiol 51:169–172

    Article  CAS  Google Scholar 

  • Shankar R, Murthy HS, Pavadi P, Thanuja K (2008) Effect of betaine as a feed attractant on growth, survival, and feed utilization in fingerlings of the Indian major carp, Labeo rohita. Bamidgeh 60:95–99

    Google Scholar 

  • Sun XX, Choi JK, Kim EK (2004) A preliminary study on the mechanism of harmful algal bloom mitigation by use of sophorolipid treatment. J Exp Mar Biol Ecol 304:35–49

    Article  CAS  Google Scholar 

  • Sun YY, Wang CH, Chen J (2008) Growth inhibition of the eight species of microalgae by growth inhibitor from the culture of Isochrysis galbana and its isolation and identification. J Appl Phycol 20:315–321

    Article  Google Scholar 

  • Tian F, Zhou JY, Sun ZW, Cai ZP, Xu N, An M, Duan SS (2014) Inhibitory effects of Chinese traditional herbs and herb-modified clays on the growth of harmful algae, Phaeocystis globosa and Prorocentrum donghaiense. Harmful Algae 37:153–159

    Article  Google Scholar 

  • Wang HL, Yu ZM, Cao XH, Song XX (2011) Fractal dimensions of flocs between clay particles and HAB organisms. Chin J Oceanol Limnol 29:656–663

    Article  Google Scholar 

  • Wu P, Yu ZM (2007) Extinguishment of harmful algae by organo-clay modified by gemini surfactant. Environ Sci 28(1):80–86 (in Chinese, with English abstract)

    CAS  Google Scholar 

  • Wu P, Yu ZM, Song XX (2006) Extinguishment of harmful algae by organo-clay modified by alkyl glucoside quaternary ammonium compound. Environ Sci 27:2164–2169

    Google Scholar 

  • Wu T, Yan XY, Cai X, Tan SZ, Li HY, Liu JS, Yang WD (2010) Removal of Chattonella marina by Gemini ammonium salts intercalated clays. Appl Clay Sci 50:604–607

    Article  CAS  Google Scholar 

  • Yang WD, Liu JS, Li HY, Zhang XL, Qi YZ (2009) Inhibition of the growth of Alexandrium tamarense by algicidal substances in Chinese fir, Cunninghamia lanceolata. Bull Environ Contamin Toxicol 83:537–541

    Article  CAS  Google Scholar 

  • Yu ZM, Zou JZ, Ma XN (1994) Application of clays to removal of red tide organisms II. Coagulation of different species of red tide organisms with montmorillonite and effect of clay pretreatment. Chin J Oceanol Limnol 12(4):316–324 (in Chinese, with English abstract)

    Article  CAS  Google Scholar 

  • Zhang Z, Finlay JA, Wang L, Gao Y, Callow JA, Callow ME, Jiang S (2009) Polysulfobetaine-grafted surfaces as environmentally benign ultra-low fouling marine coatings. Langmuir 25:13516–13521

    Article  CAS  PubMed  Google Scholar 

  • Zhou LH, Zheng TL, Wang X, Ye JL, Tian Y, Hong HS (2007) Effect of five Chinese traditional medicines on the biological activity of a red-tide causing alga-Alexandrium tamarense. Harmful Algae 6:354–360

    Article  CAS  Google Scholar 

  • Zou H, Pan G, Chen H, Yuan XZ (2006) Removal of cyanobacterial blooms in Taihu Lake using local soils. II. Effective removal of Microcystis aeruginosa using local soils and sediments modified by chitosan. Environ Pollut 141:201–205

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Basic Research Program of China (973 Program) (2010CB428702), the Technical Extension Special Project of Guangdong Marine Fisheries Service (A201201K01), the Science and Technology Projects of Guangdong Province (2009B030803042), and Guangzhou Environmental Protection Project (2008–07).

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Correspondence to Jie-Sheng Liu or Wei-Dong Yang.

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Liang, JJ., Li, YH., Liu, F. et al. Experimental removal of Alexandrium tamarense cells using sulfobetaines and their modified clays. J Appl Phycol 27, 2313–2319 (2015). https://doi.org/10.1007/s10811-014-0482-4

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  • DOI: https://doi.org/10.1007/s10811-014-0482-4

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