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Algicidal Effect of Serratia Sp. PDGS120915 Against Harmful Dinophyceae Algae Keunho Ji and Young Tae Kim*

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Algicidal Effect of Serratia Sp. PDGS120915 Against Harmful Dinophyceae Algae Keunho Ji and Young Tae Kim* 10(2): 089-095 (2016) Journal of FisheriesSciences.com E-ISSN 1307-234X © 2016 www.fisheriessciences.com ORIGINAL ARTICLE Research Article Algicidal Effect of Serratia sp. PDGS120915 against Harmful Dinophyceae Algae Keunho Ji and Young Tae Kim* Department of Microbiology, Pukyong National University, Busan 608-737, South Korea Received: 28.02.2016 / Accepted: 19.04.2016 / Published online: 30.04.2016 Abstract: Harmful algal blooms (HABs) can cause massive economic losses. In this study, the bacterial strain PDGS120915 produced a red pigment (prodigiosin). It was isolated from lightly contaminated stream water taken from Busan, Korea. The isolated strain was identified as Serratia sp. by 16S rDNA sequence analysis and morphological characteristics. Prodigiosin from Serratia sp. PDGS120915 was extracted and purified by high-performance liquid chromatography (HPLC). This pigment showed algicidal activity against dinophyceae, Alexandrium catenella, Gymnodinium impudicum, and Cochlodinium polykrikoides. The algicidal activity of this prodigiosin against dominant bloom-forming dinophyceae on the Korean coast was examined, and it exhibited high algicidal activity against A. catenella (83.4%), G. impudicum (92.1%), and C. polykrikoides (92.3%). Furthermore, prodigiosin from Serratia sp. PDGS120915 showed a broad range of algicidal activity against raphidophyceae (Chattonella marina, Heterosigma akashiwo), coscinodiscophyceae (Skeletonema costatum), and bacillariophyceae (Nitzschia pungens). The optimum concentration of this activity was observed at 5 ppb. Additionally, algicidal activity increased rapidly after 9-h and showed more than 80% algicidal activity at 12-h. Our research suggested that the algicidal bacterium Serratia sp. PDGS120915 and its algicidal compound, prodigiosin, could be a potential bio-agent for the prevention and control of harmful algal blooms. Keywords: Algicide; Dinophyceae; HABs; Prodigiosin; Serratia *Correspondence to: Young Tae Kim, Department of Microbiology, Pukyong National University, Busan 608-737, South Korea, Tel: 8210-3569-63668 E-mail: [email protected] 89 Journal of FisheriesSciences.com Yumi et al., 10(2): 089-095 (2016) Journal abbreviation: J FisheriesSciences.com Introduction Bacterial Strain The bacteria sample was collected from lightly polluted Harmful algal blooms (HABs) have been accompanied by stream water in Busan, Korea. To screen the algicidal bacteria, huge economic losses through massive fish deaths and a threat the isolated strain was inoculated into logarithmic-phase algal with shellfish poisoning in marine and freshwater ecosystems cultures. The algicidal substance-producing bacterium designated (Hallegraeff, 1993; Landsberg, 2002; Sellner et al., 2003). PDGS120915 was obtained on Luria Bertani (LB) medium at 25°C. Moreover, approximately 2,000 cases of human poisoning Identification of Algicidal Bacteria resulting from algal toxins are reported each year (Zingone and Enevoldsen, 2000). A number of methods of bloom control have An isolated strain was grown at 25°C for 1 day on LB medium. been investigated. Many chemical (e.g. copper sulphate, ozone) Standard physiological and biochemical characteristics were and physical (e.g. clay/algal flocculation, ultrasonic irradiation) examined using API kits (API 20E and APIZYM; BioMerieux, methods have been proposed to mitigate or control HABs France). For the sequence analysis, bacterial genomic DNA was (Anderson, 1997; Kim, 2006). However, most of these methods extracted and purified using a DNA extraction kit according are inapplicable because of high costs and secondary pollution. to the manufacturer’s instructions (Promega Co., Madison, Therefore, research on economic and feasible approaches for USA). 16S rDNA was amplified by PCR using the universal algae removal has important theoretical and practical significance primers 8F (5’- AGAGTTTGATCCATGGC-3’) and 1492R (Pei et al., 2005). Recently, some studies have demonstrated (5’-GTTACCTTGTTACGACTT-3’). The obtained nucleotide that the bacteria could lyse alga cells by producing extracellular sequences were analyzed by the BLASTN database (http:// substances, such as protease (Lee et al., 2000b), hydroxylamine www.ncbi.nlm.nih.gov/BLAST) at the National Center for (Berger et al., 1979), antibiotics (Dakhama et al., 1993), and Biotechnology Information (NCBI). A neighbor-joining aminophenol (Yoshikawa et al., 2000; Yamanoto et al., 1998). phylogenetic tree was constructed using MEGA 5.0. Bacteria that can control algal blooms are called algicidal Purification of algicidal compound bacteria. Many bacteria with strong algicidal activity against The bacterial cells were harvested, and pigment extraction was HAB species have been isolated and investigated (Kodani et al., performed using acidified ethanol (5% HCl and 95% ethanol). 2002; Su et al., 2007; Ma et al., 2011). Algicidal bacteria have a Subsequently, the extracted pigments were chromatographed on broad range of potential industrial and environmental applications an XTerra MS C18 reverse-phase column (125Å, 2.5 µm, 2.1 mm from the point view of diversity, biodegradability, low toxicity, × 20 mm, Waters). HPLC was carried out with the Bio-Rad HPLC and biocompatibility (Fiechter, 1992). The greatest advantage system (Bio-Rad, USA) at a 0.3 ml/min flow rate. of biosurfactants when compared with synthetic surfactants is that they are easily biodegraded, making them environmentally Characterization of Algicidal Effect acceptable in contrast to some synthetic algicides (Mulligan, Activities of different treatments: Bacterial cells, bacterial 2005). Additionally, several studies have stated that algicidal cultures, cell-free filtrates, and purified compounds were bacteria may only be effective on a specific genus or species of inoculated into each algal culture. Afterward, the inoculates were algae (Fukami et al., 1992; Doucette et al., 1999), while others cultivated in adjusted algae conditions. target a broader range of algal classes (Imai et al., 1995; Lovejoy et al., 1998; Kang et al., 2008; Roth et al., 2008a). Several Effects of growth phase of bacteria: To investigate the strains of algicidal bacteria have been isolated, but few algicides algicidal activities related to bacterial growth phase, the bacterial have been purified. Great difficulties exist in the isolation and growth and algicidal activity of each time were examined. purification of algicidal compounds because of the apparent Effects of concentration: The purified compound was variation in characteristics across different species of algicidal inoculated into each algal culture at concentrations of 1, 3, 5, 7, bacteria (Skerratt et al., 2002). and 10 ppb, and f/2 medium was used as a control. All experiments In this study, the algicidal bacterium PDGS120915 was were performed in triplicate. The cultivation used the same isolated from lightly contaminated stream water. Furthermore, conditions as those used for the algal culture. characterization of the lytic effect was examined against several Mode of activity: Isolated bacterium PDGS120915 was HAB species. These results were investigated to determine the cultured in LB medium at 25°C for 24-h. Cells were harvested potential source of algicidal bacteria or controlling HABs. by centrifugation at 12,000 × g for 20 min, and supernatants were passed through 0.22-µm filters to obtain cell-free filtrates. Materials and Methods Bacterial cultures, cell-free filtrates, and purified compounds were Algal Cultures inoculated into each algal cell culture, respectively. Then, they were cultivated at 20°C, pH 8, and 120 µE/m2/sec in a 12-h light Alexandrium catenella, Gymnodinium impudicum, and and 12-h dark cycle. Cochlodinium polykrikoides were supplied by the Korea Marine Microalgae Culture Center (KMCC). All algal cultures were Analysis of algicidal activity: To measure the algicidal grown in f/2 medium (Guillard and Ryther, 1962) at 20°C, pH 8, activities of the isolated bacterial strain, the algal cells were and 120 µE/m2/sec in a 12-h light and 12-h dark cycle. quantified using a hemocytometer under a light microscope. 90 Journal of FisheriesSciences.com Yumi et al., 10(2): 089-095 (2016) Journal abbreviation: J FisheriesSciences.com Lugol’s iodine reagent fixed algal cell counting. The following time the concentration increased, stronger algicidal activity was formula was used to calculate the algicidal effect: observed (Figure 4). Even though increase ratio was under 1% by stages between 5 and 10 ppb, this seems to be a concentration- (Number of initial cells - Number of survived cells) Algicidal activity( %) = × 100 dependent reaction. Number of initial cells Results The algicidal range of Serratia sp. PDGS120915 120915 Physiological identification The algicidal range of Serratia sp. PDGS was examined against other HAB classes. The 5 ppb purified prodigiosin was 120915 The bacterium PDGS was determined to be a gram-negative added to each algal culture reached at the mid-exponential phase. rod shape and reddish colony obtained on an LB agar plate. The results The cultivation was adequate for the growth of each algal cell. of its biochemical and enzymatic characteristics are shown in Table 1. The Algicidal activity was estimated using the aforementioned strain utilized citrate, fructose, galactose, glucose, maltose, mannitol, equation. The algicidal activities against raphidophyceae, mannose, sorbitol, sucrose, and trehalose, as well as the hydrolysis coscinodiscophyceae, and bacillariophyceae were as follows of gelatin
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