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A Polysaccharide-Degrading Marine Bacterium Flammeovirga Sp. MY04 and Its Extracellular Agarase System

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A Polysaccharide-Degrading Marine Bacterium Flammeovirga Sp. MY04 and Its Extracellular Agarase System 中国科技论文在线 http://www.paper.edu.cn J. Ocean Univ. China (Oceanic and Coastal Sea Research) DOI 10.1007/s11802-012-1929-3 ISSN 1672-5182, 2012 11 (3): 375-382 http://www.ouc.edu.cn/xbywb/ E-mail:[email protected] A Polysaccharide-Degrading Marine Bacterium Flammeovirga sp. MY04 and Its Extracellular Agarase System HAN Wenjun1), 2), 3), GU Jingyan1), 3), YAN Qiujie2), LI Jungang2), WU Zhihong3), *, GU Qianqun1), *, and LI Yuezhong3) 1) Key Laboratory of Marine Drugs, Chinese Ministry of Education, School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, P. R . C hi n a 2) School of Life Science and Biotechnology, Mianyang Normal University, Mianyang 621000, P. R. China 3) State Key Laboratory of Microbial Technology, School of Life Science, Shandong University, Jinan 250100, P. R. China (Received February 2, 2012; revised April 8, 2012; accepted May 29, 2012) © Ocean University of China, Science Press and Springer-Verlag Berlin Heidelberg 2012 Abstract Bacteria of the genus Flammeovirga can digest complex polysaccharides (CPs), but no details have been reported re- garding the CP depolymerases of these bacteria. MY04, an agarolytic marine bacterium isolated from coastal sediments, has been identified as a new member of the genus Flammeovirga. The MY04 strain is able to utilize multiple CPs as a sole carbon source and -1 -1 grows well on agarose, mannan, or xylan. This strain produces high concentrations of extracellular proteins (490 mg L ± 18.2 mg L liquid culture) that exhibit efficient and extensive degradation activities on various polysaccharides, especially agarose. These pro- -1 -1 teins have an activity of 310 U mg ± 9.6 U mg proteins. The extracellular agarase system (EAS) in the crude extracellular enzymes contains at least four agarose depolymerases, which are with molecular masses of approximately 30–70 kDa. The EAS is stable at a -1 wide range of pH values (6.0–11.0), temperatures (0–50℃), and sodium chloride (NaCl) concentrations (0– 0.9 mol L ). Two major degradation products generated from agarose by the EAS are identified to be neoagarotetraose and neoagarohexaose, suggesting that β-agarases are the major constituents of the MY04 EAS. These results suggest that the Flammeovirga strain MY04 and its polysac- charide-degradation system hold great promise in industrial applications. Key words Flammeovirga; polysaccharide degradation; extracellular agarase system; neoagaro-oligosaccharide while only two α-agarases have been reported, one from 1 Introduction Thalassomonas sp. JAMB-A33 and one from Alteromo- nas agarlyticus GJ1B (Ohta et al., 2005b; Potin et al., Complex polysaccharides (CPs), which are composed 1993). of repeated units of complex sugars, are widely present in Agarases are useful in the preparation of algal proto- plants, animals, and microorganisms, in which they serve plasts (Gupta et al., 2010; Yeong et al., 2008) and the as essential structural and functional components. Agar, recovery of DNA from agarose gels (Cole and Åkerman, composed of agarose and agaropectin, is the main com- 2000) , and have potential in the production of functional ponent of the cell wall of red algae (Rhodophyta) (Rochas oligosaccharides (Hatada et al., 2006; Hu et al., 2006; et al., 1986). Agarose is a polymer composed of 3,6-an- Wang et al., 2004; Wu et al., 2005). Although the agarose hydro-L-galactopyranose-α-1,3-D-galactopyranose units degradation abilities of many microorganisms isolated that are joined by β1-4 bonds (Rees, 1969). Agarose can from marine environment, fresh water, or soil have been be cleaved by either α-agarase (E.C. 3.2.1.158) at the investigated and the corresponding enzymes have been α1-3 linkage (Rochas et al., 1994) or β-agarase (E.C. characterised, only β-agarase I from Pseudoalteromonas 3.2.1.81) at the β1-4 linkage (Morrice et al., 1983a and atlantica has been industrially applied for the gel recov- 1983b), producing a series of oligosaccharides that have ery of DNA (Fu and Kim, 2010). There are many limita- reducing ends. The oligomers yielded from the degrada- tions in the applications of agarases. For example, the tion of agarose by α-agarase and β-agarase are termed heterologous expression levels of agarases are usually agaro- and neoagaro-oligosaccharides, respectively. There low and the use of these enzymes for some purposes, such have been many studies of agarases and their degradation as the enzymatic preparation of functional oligosaccha- of agarose. Most of the reported agarases are β-agarases, rides, is expensive. The use of native agarase-producers or their extracellular agarase systems (EASs) may provide * Corresponding authors. Tel: 0086-532-82032065 an alternative. E-mail: [email protected]; [email protected] Flammeovirga is a newly defined bacterial genus be- 转载 中国科技论文在线 http://www.paper.edu.cn 376 HAN et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2012 11 (3): 375-382 longing to the family Flammeovirgaceae of the class glucose. After incubation at 30℃ for 16 h with agitation, α-Proteobacteria. Five species have been reported in this the turbidity of the broth was measured at 600 nm to genus: F. aprica (Nakagawa et al., 1997), F. arenaria, F. evaluate the cellular growth. The initial pH of the medium yaeyamensis (Takahashi et al., 2006), F. kamogawensis was adjusted to 5.0–11.0 before autoclaving. Culture tem- (Hosoya and Yokota, 2007), and F. pacifica (Xu et al., peratures were between 4℃ and 45℃. The cellular toler- 2011). All of the type strains have a potent ability to de- ance to sodium chloride was assayed over a concentration grade marine CPs, including agarose. Yang et al. have range of 0–5.0%. The requirement of metal ions for growth described the gene cloning and biochemical characteristic was analysed by growing a series of cultures in which a of an agarase, AgaYT, from the F. yaeyamensis strain YT single metal salt had been removed from the medium. (Yang et al., 2011). Although the heterologously ex- pressed enzyme exhibited a high degradation activity on 2.3 Polysaccharide-Utilizing Abilities of the MY04 agarose, when the protein was expressed in E. coli, it was Strain mostly present in the form of inclusion bodies. To date, To evaluate the ability of the bacterial isolate to utilize we know few of the CP-degradation characteristics of different polysaccharides, the sole carbon source in the Flammeovirga strains or their extracellular agarase sys- BM broth was supplemented with various CPs, including tems, although these strains/systems have been suggested algae-derived polysaccharides (alginate, agar, agarose, to be relevant for biotechnological applications. carrageenan, and ι-carrageenan), plant-derived polysac- Herein, we report the polysaccharide-degradation char- charides (cellulose, carboxymethylcellulose (CMC), crude acteristics of a marine isolate, Flammeovirga sp. MY04, mannan, superfine mannan, microcrystalline cellulose and its extracellular agarase system. (MC), pectate, starch, and xylan), and crustacean poly- saccharides (chitin and chitosan). Polysaccharides were 2 Materials and Methods added to the media at a final concentration of 0.10%. Af- ter the initial culture in the BM broth supplemented with 2.1 Isolation of Agarose-Degrading Bacteria 0.2% glucose, the MY04 bacteria were collected by cen- Coastal sediments were collected from a laver farm trifugation when the culture reached an OD600 of 0.8 and near Ganyu City in Jiangsu Province, China. A basal me- were washed twice using sterilised seawater. The washed dium (BM) composed of 3.0% NaCl, 0.75% KCl, 0.11% bacterial sludge was resuspended in BM broth, and an CaCl2, 0.72% Mg2SO4, 0.15% NH4Cl, and 1.5% agar (pH aliquot was transferred into each restricted broth at a 7.0) was used to isolate agarolytic bacteria. After incuba- starting OD600 of 0.08. The cellular growth of MY04 was tion at 30℃ for 72 h, the colonies that formed deep cra- evaluated as described above. ters in the agar were transferred to a fresh BM plate for further purification. To evaluate the agar-digestion ability 2.4 Preparation of the Crude Extracellular of the isolates, the BM plates were stained with an iodine Enzymes solution (Hodgson and Chater, 1981) following a 16-h To prepare the crude extracellular enzymes, the MY04 ℃ incubation at 30 . strain was cultured at 30℃ for 72 h in 1 L of BM broth supplemented with 0.4% tryptone and 0.25% yeast extract. 2.2 Identification of the MY04 Isolate The following preparation was performed at 4℃. The Genomic DNA was prepared using a genomic DNA cultures were centrifuged at 12 000\× g for 15 min, and extraction kit (TianGen Inc., Beijing, China). For PCR ammonium sulphate was added into the supernatant to amplification of the 16S ribosomal RNA (rRNA) gene reach 80% saturation. After a 4-h incubation to precipitate sequence, the bacterial universal primer pair 27f the proteins, the mixture was centrifuged at 15 000 × g for -1 (5’-GAGTTTGATCCTGGCTCAG-3’) and 1492r (5’-AA- 30 min. The pellet was dissolved in 50 mL of 50 mmol L -1 GGAGGTGATCCAGC C-3’) (Weisburg et al., 1991) were HEPES buffer (pH 7.5) containing 0.5 mmol L EDTA used. The PCR products were gel-purified with a DNA and 5% glycerol, which was dialysed three times against extraction kit (TAKARA Inc., Dalian, China) according to the same buffer for 6 h. The dialysed enzyme solution was the manufacturer’s instructions and cloned into the stored in aliquots at −20℃ before use. pMD18-T vector (TAKARA Inc., Dalian, China) for se- quencing. The sequence was analysed against the GenBank 2.5 Polysaccharide-Degradation Activities of the database using the on-line BLAST program (Altschul Crude Extracellular Enzymes et al., 1990) to search for the most similar sequences.
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