Abstract
Cyanobacterial blooms have become a serious problem in Lake Taihu during the last 20 years, and Microcystis aeruginosa and Synechococcus sp. are the two dominant species in cyanobacterial blooms of Lake Taihu. A freshwater bacterial strain, Shewanella sp. Lzh-2, with strong algicidal properties against harmful cyanobacteria was isolated from Lake Taihu. Two substances with algicidal activity secreted extracellularly by Shewanella sp. Lzh-2, S-2A and S-2B, were purified from the bacterial culture of strain Lzh-2 using ethyl acetate extraction, column chromatography, and high performance liquid chromatography (HPLC) in turn. The substances S-2A and S-2B were identified as hexahydropyrrolo[1,2-a]pyrazine-1,4-dione and 2, 3-indolinedione (isatin), respectively, based on liquid chromatography-mass spectrometry (LC-MS), gas chromatography-mass spectrometry (GC-MS), and hydrogen-nuclear magnetic resonance (H-NMR) analyses, making this the first report of their algicidal activity toward cyanobacteria. S-2A (hexahydropyrrolo[1,2-a]pyrazine-1,4-dione) had no algicidal effects against Synechococcus sp. BN60, but had a high level of algicidal activity against M. aeruginosa 9110. The LD50 value of S-2A against M. aeruginosa 9110 was 5.7 μg/ml. S-2B (2, 3-indolinedione) showed a potent algicidal effect against both M. aeruginosa 9110 and Synechococcus sp. BN60, and the LD50 value of S-2B against M. aeruginosa 9110 and Synechococcus sp. BN60 was 12.5 and 34.2 μg/ml, respectively. Obvious morphological changes in M. aeruginosa 9110 and Synechococcus sp. BN60 were observed after they were exposed to S-2A (or S-2B) for 24 h. Approximately, the algicidal activity, the concentration of S-2A and S-2B, and the cell density of Lzh-2 were positively related to each other during the cocultivation process. Overall, these findings increase our knowledge about algicidal substances secreted by algicidal bacteria and indicate that strain Lzh-2 and its two algicidal substances have the potential for use as a bio-agent in controlling cyanobacterial blooms in Lake Taihu.
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References
Armando JW, Boghigian BA, Pfeifer BA (2012) LC-MS/MS quantification of short-chain acyl-CoA's in Escherichia coli demonstrates versatile propionyl-CoA synthetase substrate specificity. Lett Appl Microbiol 54(2):140–148. doi:10.1111/j.1472-765X.2011.03184.x
Bach MK, Magee WE (1962) Biochemical effects of isatin beta-thiosemicarbazone on development of vaccinia virus. Proc Soc Exp Biol Med Soc Exp Biol Med 110:565–567
Cai W, Wang H, Tian Y, Chen F, Zheng T (2011) Influence of a bacteriophage on the population dynamics of toxic dinoflagellates by lysis of algicidal bacteria. Appl Environ Microbiol 77(21):7837–7840. doi:10.1128/AEM.05783-11
Chen WM, Sheu FS, Sheu SY (2011) Novel L-amino acid oxidase with algicidal activity against toxic cyanobacterium Microcystis aeruginosa synthesized by a bacterium Aquimarina sp. Enzym Microb Technol 49(4):372–379. doi:10.1016/j.enzmictec.2011.06.016
Grant G, Smith G, Sudhakar R (1988) Gas Chromatographic-Mass Spectrometric Analysis of the Curie-point Pyrolysis Products of Some Dipeptides and their Diketopiperazine. J Chem Soc Perkin Trans 2:203–211
Hare CE, Demir E, Coyne KJ, Cary SC, Kirchman DL, Hutchins DA (2005) A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful Algae 4(2):221–234. doi:10.1016/j.hal.2004.03.001
Haughey MA, Anderson MA, Whitney RD, Taylor WD, Losee RF (2000) Forms and fate of Cu in a source drinking water reservoir following CuSO4 treatment. Water Res 34(13):3440–3452. doi:10.1016/s0043-1354(00)00054-3
Houston DR, Synstad B, Eijsink VG, Stark MJ, Eggleston IM, van Aalten DM (2004) Structure-based exploration of cyclic dipeptide chitinase inhibitors. J Med Chem 47(23):5713–5720. doi:10.1021/jm049940a
Imamura N, Motoike I, Noda M, Adachi K, Konno A, Fukami H (2000) Argimicin A, a novel anti-cyanobacterial compound produced by an algae-lysing bacterium. J Antibiot 53(11):1317–1319
Imamura N, Motoike I, Shimada N, Nishikori M, Morisaki H, Fukami H (2001) An efficient screening approach for anti-Microcystis compounds based on knowledge of aquatic microbial ecosystem. J Antibiot 54(7):582–587
Jarrahpour A, Khalili D, De Clercq E, Salmi C, Brunel JM (2007) Synthesis, antibacterial, antifungal and antiviral activity evaluation of some new bis-Schiff bases of isatin and their derivatives. Molecules 12(8):1720–1730
Jeong H, Yim JH, Lee C, Choi SH, Park YK, Yoon SH, Hur CG, Kang HY, Kim D, Lee HH, Park KH, Park SH, Park HS, Lee HK, Oh TK, Kim JF (2005) Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res 33(22):7066–7073. doi:10.1093/nar/gki1016
Jeong JH, Jin HJ, Sohn CH, Suh KH, Hong YK (2000) Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. J Appl Phycol 12(1):37–43. doi:10.1023/a:1008139129057
Jeong SY, Ishida K, Ito Y, Okada S, Murakami M (2003) Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. SY-1, against the harmful dinoflagellate, Cochlodinium polykrikoides. Tetrahedron Lett 44(43):8005–8007. doi:10.1016/j.tetlet.2003.08.115
Jung SW, Kim BH, Katano T, Kong DS, Han MS (2008) Pseudomonas fluorescens HYK0210-SK09 offers species-specific biological control of winter algal blooms caused by freshwater diatom Stephanodiscus hantzschii. J Appl Microbiol 105(1):186–195. doi:10.1111/j.1365-2672.2008.03733.x
Kang YH, Kim JD, Kim BH, Kong DS, Han MS (2005) Isolation and characterization of a bio-agent antagonistic to diatom, Stephanodiscus hantzschii. J Appl Microbiol 98(5):1030–1038. doi:10.1111/j.1365-2672.2005.02533.x
Kim YS, Lee DS, Jeong SY, Lee WJ, Lee MS (2009) Isolation and characterization of a marine algicidal bacterium against the harmful raphidophyceae Chattonella marina. J Microbiol 47(1):9–18. doi:10.1007/s12275-008-0141-z
Kupinic M, Medic-Saric M, Movrin M, Maysinger D (1979) Antibacterial and antifungal activities of isatin N-Mannich bases. J Pharm Sci 68(4):459–462
Kwon SK, Park YK, Kim JF (2010) Genome-wide screening and identification of factors affecting the biosynthesis of prodigiosin by Hahella chejuensis, using Escherichia coli as a surrogate host. Appl Environ Microbiol 76(5):1661–1668. doi:10.1128/AEM.01468-09
Lee YS, Kim JD, Lim WA, Lee SG (2009) Survival and growth of Cochlodinium polykrikoides red tide after addition of yellow loess. J Environ Biol / Acad Environ Biol India 30(6):929–932
Liu ZY, Zhou XN, Zhang HH, Wan L, Sun ZL (2011) An integrated method for degradation products detection and characterization using hybrid ion trap/time-of-flight mass spectrometry and data processing techniques: application to study of the degradation products of danofloxacin under stressed conditions. Anal Bioanal Chem 399(7):2475–2486. doi:10.1007/s00216-010-4629-0
Lovejoy C, Bowman JP, Hallegraeff GM (1998) Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl Environ Microbiol 64(8):2806–2813
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51(2):139–144. doi:10.1111/j.1550-7408.2004.tb00538.x
Mayali X, Franks PJ, Azam F (2008) Cultivation and ecosystem role of a marine roseobacter clade-affiliated cluster bacterium. Appl Environ Microbiol 74(9):2595–2603. doi:10.1128/AEM.02191-07
Nakashima T, Kim D, Miyazaki Y, Yamaguchi K, Takeshita S, Oda T (2006a) Mode of action of an antialgal agent produced by a marine gammaproteobacterium against Chattonella marina. Aquat Microb Ecol 45(3):255–262. doi:10.3354/ame045255
Nakashima T, Miyazaki Y, Matsuyama Y, Muraoka W, Yamaguchi K, Oda T (2006b) Producing mechanism of an algicidal compound against red tide phytoplankton in a marine bacterium gamma-proteobacterium. Appl Microbiol Biotechnol 73(3):684–690. doi:10.1007/s00253-006-0507-2
Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol. doi:10.1021/es103316q
Ogata A, Hamaue N, Terado M, Minami M, Nagashima K, Tashiro K (2003) Isatin, an endogenous MAO inhibitor, improves bradykinesia and dopamine levels in a rat model of Parkinson’s disease induced by Japanese encephalitis virus. J Neurol Sci 206(1):79–83
Paerl HW, Xu H, McCarthy MJ, Zhu GW, Qin BQ, Li YP, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45(5):1973–1983. doi:10.1016/j.watres.2010.09.018
Pandeya SN, Sriram D, Nath G, De Clercq E (1999) Synthesis, antibacterial, antifungal and anti-HIV evaluation of Schiff and Mannich bases of isatin derivatives with 3-amino-2-methylmercapto quinazolin-4(3H)-one. Pharm Acta Helv 74(1):11–17
Qin BQ, Zhu GW, Gao G, Zhang YL, Li W, Paerl HW, Carmichael WW (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environ Manage 45(1):105–112. doi:10.1007/s00267-009-9393-6
Ran R, Zhang W, Cui B, Xu Y, Han Z, Wu A, Li D, Zhang D, Wang C, Shi J (2013) A simple and rapid method for the determination of deoxynivalenol in human cells by UPLC-TOF-MS. Anal Methods 5:5637–5643
Ren HQ, Zhang P, Liu CH, Xue YR, Lian B (2010) The potential use of bacterium strain R219 for controlling of the bloom-forming cyanobacteria in freshwater lake. World J Microbiol Biotechnol 26:465–472
Rinta-Kanto JM, Ouellette AJA, Boyer GL, Twiss MR, Bridgeman TB, Wilhelm SW (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ Sci Technol 39(11):4198–4205. doi:10.1021/es048249u
Sakai H, Oguma K, Katayama H, Ohgaki S (2007) Effects of low or medium-pressure UV irradiation on the release of intracellular microcystin. Water Res 41(15):3458–3464. doi:10.1016/j.watres.2007.04.031
Sigee DC, Glenn R, Andrews MJ, Bellinger EG, Butler RD, Epton HAS, Hendry RD (1999) Biological control of cyanobacteria: principles and possibilities. Hydrobiologia 395:161–172. doi:10.1023/a:1017097502124
Su RQ, Yang XR, Zheng TL, Tian Y, Jiao NZ, Cai LZ, Hong HS (2007) Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 6(6):799–810. doi:10.1016/j.hal.2007.04.004
Taizo S, akeshi T, Satomi N (2011) Algicidal activity and identification of an algicidal substance produced by marine Pseudomonas sp. C55a-2. Fish Sci : FS 77:397–402
Tian C, Liu XL, Tan J, Lin SQ, Li DT, Yang H (2012) Isolation, identification and characterization of an algicidal bacterium from Lake Taihu and preliminary studies on its algicidal compounds. J Environ Sci 24(10):1823–1831
Tian C, Tan J, Wu X, Ye WJ, Liu XL, Li DT, Yang H (2009) Spatiotemporal transition of bacterioplankton diversity in a large shallow hypertrophic freshwater lake, as determined by denaturing gradient gel electrophoresis. J Plankton Res 31(8):885–897. doi:10.1093/plankt/fbp028
Wang XL, Gong LY, Liang SK, Han XR, Zhu CJ, Li YB (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4(2):433–443. doi:10.1016/j.hal.2004.06.001
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992
Wu X, Xi WY, Ye WJ, Yang H (2007) Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol Ecol 61(1):85–96. doi:10.1111/j.1574-6941.2007.00326.x
XiuZhu D, Cai M (2001) Systematic identification manual of common bacteria. Science press, Beijing
Yamamoto Y, Suzuki K (1990) Distribution and algal-lysing activity of fruiting myxobacteria in Lake Suwa. J Phycol 26:457–462
Yang F, Li X, Li Y, Wei H, Yu G, Yin L, Liang G, Pu Y (2013) Lysing activity of an indigenous algicidal bacterium Aeromonas sp. against Microcystis spp. isolated from Lake Taihu. Environ Technol 34(9–12):1421–1427
Ye WJ, Tan J, Liu XL, Lin SQ, Pan JL, Li DT, Yang H (2011) Temporal variability of cyanobacterial populations in the water and sediment samples of Lake Taihu as determined by DGGE and real-time PCR. Harmful Algae 10(5):472–479. doi:10.1016/j.hal.2011.03.002
Zhang X, Liu Y, Yan K, Wu H (2007) Decolorization of anthraquinone-type dye by bilirubin oxidase-producing nonligninolytic fungus Myrothecium sp. IMER1. J Biosci Bioeng 104(2):104–110. doi:10.1263/jbb.104.104
Zheng X, Zhang B, Zhang J, Huang L, Lin J, Li X, Zhou Y, Wang H, Yang X, Su J, Tian Y, Zheng T (2012) A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-4617-8
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This work was supported by the National Natural Science Foundation of China (No. 21277089), the National Basic Research Program (973) of China (No. 2012CB720802), and the National High Technology Research and Development Program (863) of China (No. 2011AA100901).
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Li, Z., Lin, S., Liu, X. et al. A freshwater bacterial strain, Shewanella sp. Lzh-2, isolated from Lake Taihu and its two algicidal active substances, hexahydropyrrolo[1,2-a]pyrazine-1,4-dione and 2, 3-indolinedione. Appl Microbiol Biotechnol 98, 4737–4748 (2014). https://doi.org/10.1007/s00253-014-5602-1
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DOI: https://doi.org/10.1007/s00253-014-5602-1