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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

  • Environmental biotechnology
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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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol. doi:10.1021/es103316q

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • XiuZhu D, Cai M (2001) Systematic identification manual of common bacteria. Science press, Beijing

    Google Scholar 

  • Yamamoto Y, Suzuki K (1990) Distribution and algal-lysing activity of fruiting myxobacteria in Lake Suwa. J Phycol 26:457–462

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

Download references

Acknowledgments

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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Correspondence to Hong Yang.

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253_2014_5602_MOESM1_ESM.pdf

Electronic supplementary material contains phenotypic characteristics of strain Lzh-2, some details for purification (Fig. S1–Fig. S6) and identification (Fig. S7–Fig. S12) of the algicidal substances. (PDF 489 kb)

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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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