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The Inhibitory Effects of Garlic (Allium Sativum) and Diallyl Trisulfide on Alexandrium Tamarense and Other Harmful Algal Species

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The Inhibitory Effects of Garlic (Allium Sativum) and Diallyl Trisulfide on Alexandrium Tamarense and Other Harmful Algal Species J Appl Phycol (2008) 20:349–358 DOI 10.1007/s10811-007-9262-8 The Inhibitory Effects of Garlic (Allium sativum) and Diallyl Trisulfide on Alexandrium tamarense and other Harmful Algal Species L. H. Zhou & T. L. Zheng & X. H. Chen & X. Wang & S. B. Chen & Y. Tian & H. S. Hong Received: 30 March 2007 /Revised and Accepted: 21 September 2007 /Published online: 10 January 2008 # Springer Science + Business Media B.V. 2007 Abstract Using cell suspension ability as an indicator, we effective was a concentration of 0.04% on A. tamarense and studied the inhibitory effect of garlic (Allium sativum) and S. trochoidea. Moreover, the higher the concentration, the diallyl trisulfide on six species of red tide causing algae. stronger was the inhibition, and a high inhibitory rate (IR) This included: the inhibition by 0.08% garlic solution of could be maintained for at least three days when the garlic five algal species — Alexandrium tamarense, Scrippsiella concentration was above 0.04%. For A. tamarense, it was trochoidea, Alexandrium catenella, Alexandrium minutum also found that the longer the inhibitory time and the higher and Alexandrium satoanum; the effects of garlic concen- the concentration, the lower was the rate of resumed cell tration on the inhibition of A. tamarense, S. trochoidea and activity. On the contrary, garlic solution could not inhibit A. Chaetoceros sp.; the effects of inhibitory time on the minutum or Chaetoceros sp.; 2) The IR to A. tamarense was rejuvenation of algal cells; and the effects of heating and reduced slightly as the heating time of the garlic solution preservation time on algal inhibition by garlic solution. In was lengthened, but the average IR was still above 80%. addition, whether or not the ingredients of garlic solution There was no significant difference between the IR of the had a possible algicidal effect was studied by comparing supernatant and sediment of the garlic solution. Further- inhibition of A. tamarense by garlic solution and man-made more, no change of algal inhibition was found when the diallyl trisulfide. The results showed that 1) inhibition by garlic solution was preserved at 20°C for several days; 3) garlic solution was significant on A. tamarense, A. As with garlic solution, diallyl trisulfide inhibited A. satoanum, A. catenella and S. trochoidea, and the least tamarense strongly; the IR was above 93% and was maintained for at least three days, as long as the concentration was 3.2–10.0 mg L−1. Thus, diallyl trisulfide : : : L. H. Zhou T. L. Zheng (*) X. Wang Y. Tian may have been the major ingredient in garlic solution School of Life Sciences, which inhibited the algae but, in addition, more than one MOE Key Lab. for Cell Biology and Tumor Cell Engineering, ingredient may have been inhibiting the algae. In conclu- Xiamen University, Xiamen 361005, China sion, garlic was a good algal inhibitor with many e-mail: [email protected] advantages, such as being common, cheap, non toxic and : : with high efficiency, and diallyl trisulfide, one of the L. H. Zhou T. L. Zheng H. S. Hong components of garlic, was similarly effective in algal State Key Lab. of Marine Environmental Science, Xiamen University, inhibition. It would be useful, therefore, to further study Xiamen 361005, China garlic as an environmentally friendly algal inhibitor. : : L. H. Zhou X. H. Chen S. B. Chen Keywords Red tide causing algae . Inhibitory time . Fisheries College, Institute of aquaculture biotechnology, Jimei University, Inhibitory rate . Allium sativum . Diallyl trisulfide . Xiamen 361021, China Environmentally friendly algal inhibitor DO09262; No of Pages 9 350 J Appl Phycol (2008) 20:349–358 Introduction Materials and methods The control of harmful algae is one of the most important Algal culture parts of red tide research since, if algal blooms can be effectively mitigated as they arise, the damage by red tide The experimental algae, except Chaetoceros sp., were can be reduced. One method involves the use of algal provided by the Third Institute of Oceanography, State inhibitors, and many researchers have been trying to find Oceanic Administration, China. They were A. tamarense effective algicides. For example, bluestone (a mineral form strain DH01 (ATDH01), S. trochoidea strain XM01 of blue hydrated copper sulphate) has been proved to kill (STXM01), A. catenella strain DH01 (ACDH01), A. algae quickly and has been applied to deal with algal blooms minutum strain TW01 (AMTW01), and A. satoanum strain for a long time (Elder and Horne 1978; Murray-Gulde et al. DH01 (ASDH01). Chaetoceros sp. was provided by the 2002; Melville et al. 2002). In recent years, more and more Fisheries College of Jimei University. Algal cultures were chemicals having algicidal activity have been found, such cultivated at 20±0.5°C and day / night cycle (12 h:12 h, as amino acid (Hehmann et al. 2002), biquaternary with a light intensity of 52 μmol photons m−2 s−1 as used ammonium salt (Liu et al. 2004), and chlorine dioxide during the experiments), in F/2 media prepared with sterile- (Zhang et al. 2003). However, the obvious shortcoming of filtered seawater. Cells in the exponential growth phase using chemicals as effective algicides is that they them- were used in the experiments. selves may become pollutants in the marine environment (Lam et al. 1995; Peterson et al. 1997; Pierce et al. 2004), Preparation of garlic solution and diallyl trisulfide and serious consideration should be given before applying them to control red tide. For this reason, natural allelo- Garlic (peeled) was mixed with distilled water, in a ratio of chemicals from different organisms have been considered 100 grams garlic per 100 mL water; mashed completely as the source for potential algicides (Wu et al. 1998; using an MSL-218 blender; filtered through a screen in a Lovejoy et al. 1998; Ridge et al. 1999; Xu et al. 2002; press; the volume readjusted; and a 100% garlic concen- Brownlee et al. 2003; Etchegaray et al. 2004). Furusawa tration (100% w/v, garlic weight / garlic solution volume) et al. (2003) found that a marine bacterium, Saprospira was kept at 20°C as the experimental garlic solution. The sp. SS98-5, which was isolated from Kagoshima Bay, Japan, content of allicin (organosulfur components) in the solu- was able to kill and lyse the cells of the diatom Chaetoceros tion, measured using the fixed sulfur method (Chen et al. ceratosporum. Yang et al. (2005) reported that wood meals 2004a), was 2.43‰. The diallyl trisulfide, with a molecular from china fir can inhibit and sink the cells of Alexandrium formula of C6H10S3, was obtained in the form of an allitride tamarense in cultures. Alamsjah et al. (2005) and Wang et al. injection (product number 5E38003), at a concentration of (2006) found that the green algae Ulva fasciata and Ulva 15 mg mL−1, produced by Hefeng Medicine Corporation of pertusa showed strong algicidal activity. In the last few Shanghai. years, we found that red tide inhibitors made with Chinese herbs, such as golden thread (Rhizoma coptidis Huang Lian) Inhibitory effects of garlic solution on different algae and areca seed (Semen arecae Bing Lang), had the merits of low concentration, fast reaction (Zhou et al. 2007). Although Experiments were conducted in 125 mL clean and ster- some algicides have been applied in the control of red tide, ilized flasks. To determine the algicidal activities of garlic most of them are still undergoing laboratory research. In solution against the five red tide phytoplankton ATDH01, addition, most research has focused on fresh water, and not ACDH01, AMTW01, ASDH01 and STXM01, the garlic enough has concentrated on marine water. Thus, it is still a solution (100%, kept at 20°C for 15 days) was added into long-term task to research and develop effective algicides 100 mL algal cultures at a concentration of 0.08% (w/v), with less toxicity for use against marine algae. Garlic and a 100 mL algal culture without garlic was used as the (Allium sativum L), being a common plant, is applied control. Four duplicate treatments were cultivated under extensively in medicine, aquaculture, stock raising as well the same conditions as described above. Samples (1 mL) as human food because of its antibacterial, antiviral and were taken 0.5, 1 and 2 hours after the addition of the nutritional functions. However, no attempt has been made to garlic, and the numbers of algal cells counted using a use garlic as an algicide. Since garlic can be used as both a 0.1 mL counting chamber under an anatomical microscope medicine and food, it should be safer than other chemicals (×40). Samples were taken 1 cm below the water surface, for use as an algal inhibitor. The algicidal effects of garlic with movement, to reduce erroneous results. However, and diallyl trisulfide (one of its components) are reported measures were taken to avoid the re-suspension of sunken here, and the purpose of this study is to discover environ- algae cells. Thus, immobility / sinking of cells to the mentally friendly algicides. bottom was assessed. Each sampling was replicated 3 J Appl Phycol (2008) 20:349–358 351 times, averaged, and the decrease of algae in suspension volumes of supernatant and sediment readjusted. This was used as a cell mobility indicator, namely inhibitory provided a supernatant of garlic solution heated for rate (IR): 20 min (abbrev. 20'S), a sediment of garlic solution heated for 20 min (abbrev. 20′D), similarly, supernatant heated for N0 À NS IR ¼ Â 100% 40 min (40′S), sediment heated for 40 min (40′D), N 0 supernatant heated for 60 min (60′S), sediment heated for Where IR = algal inhibitory rate of garlic; N0 = control algal 60 min (60′D), respectively; and, again, 10 mL fresh garlic −1 −1 density (cell mL ); Ns = treatment algal density (cell mL ).
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