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Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa

  • Environmental biotechnology
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Abstract

A freshwater algicidal bacterial strain, Lzh-5, isolated from Lake Taihu, with strong algicidal activity against Microcystis aeruginosa, was identified as Bacillus sp. based on its phenotypic characteristics and 16S ribosomal RNA (rRNA) gene sequence. The algicidal mode of Bacillus sp. Lzh-5 was indirect, attacking M. aeruginosa cells by releasing algicidal compounds. Two algicidal compounds (S-5A and S-5B) produced by Bacillus sp. Lzh-5 were purified with ethyl acetate extraction, column chromatography, and high-performance liquid chromatography and identified as hexahydropyrrolo[1,2-a]pyrazine-1,4-dione and 3-isopropyl-hexahydropyrrolo[1,2-a]pyrazine-1,4-dione based on liquid chromatography–mass spectrometry, gas chromatography–mass spectrometry, and nuclear magnetic resonance analyses. The active algicidal compounds S-5A (hexahydropyrrolo[1,2-a]pyrazine-1,4-dione) and S-5B (3-isopropyl-hexahydropyrrolo[1,2-a]pyrazine-1,4-dione) displayed high levels of algicidal activity against M. aeruginosa 9110, with LD50 values of 5.7 and 19.4 μg/ml, respectively. This is the first report of 3-isopropyl-hexahydropyrrolo[1,2-a]pyrazine-1,4-dione as an algicidal compound. Compounds S-5A and S-5B also induced obvious morphological changes in M. aeruginosa 9110. In cocultures of M. aeruginosa 9110 and Bacillus sp. Lzh-5, the cell density of Bacillus sp. Lzh-5 and the concentrations of S-5A and S-5B correlated positively with the algicidal activity. Our results indicate that strain Lzh-5 and its two algicidal compounds are potentially useful for 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 

  • Belin P, Moutiez M, Lautru S, Seguin J, Pernodet JL, Gondry M (2012) The nonribosomal synthesis of diketopiperazines in tRNA-dependent cyclodipeptide synthase pathways. Nat Prod Rep 29(9):961–979. doi:10.1039/c2np20010d

    Article  CAS  PubMed  Google Scholar 

  • Borthwick AD (2012) 2,5-Diketopiperazines: synthesis, reactions, medicinal chemistry, and bioactive natural products. Chem Rev 112(7):3641–3716. doi:10.1021/cr200398y

    Article  CAS  PubMed  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  PubMed Central  Google Scholar 

  • Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum Ecol Risk Assess 7:1393–1407

    Article  Google Scholar 

  • CLSI (2006) Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. CLSI documents M27-S3. 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087–1898 USA

  • Fdhila F, Vazquez V, Sanchez JL, Riguera R (2003) dd-diketopiperazines: antibiotics active against Vibrio anguillarum isolated from marine bacteria associated with cultures of Pecten maximus. J Nat Prod 66(10):1299–1301. doi:10.1021/np030233e

    Article  CAS  PubMed  Google Scholar 

  • Grant GS, 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 

  • 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 

  • 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 

  • 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  PubMed Central  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 

  • 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  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 

  • Li Y, Hongyi W, Komatsu M, Ishibashi K, Jinsan L, Ito T, Yoshikawa T, Maeda H (2012) Isolation and characterization of bacterial isolates algicidal against a harmful bloom-forming cyanobacterium Microcystis aeruginosa. Biocontrol Sci 17(3):107–114

    Article  PubMed  Google Scholar 

  • Li Z, Lin S, Liu X, Tan J, Pan J, Yang H (2014) 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 doi:10.1007/s00253-014-5602-1

  • 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  PubMed Central  Google Scholar 

  • Luo J, Wang Y, Tang S, Liang J, Lin W, Luo L (2013) Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8(10):e76444. doi:10.1371/journal.pone.0076444

    Article  CAS  PubMed  PubMed Central  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 

  • 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 

  • Nishanth Kumar S, Dileep C, Mohandas C, Nambisan B, Ca J (2014) Cyclo(D-Tyr-D-Phe): a new antibacterial, anticancer, and antioxidant cyclic dipeptide from Bacillus sp. N strain associated with a rhabditid entomopathogenic nematode. J Pept Sci Off Publ Eur Pept Soc 20(3):173–185. doi:10.1002/psc.2594

    CAS  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 

  • 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 

  • Park SC, Lee JK, Kim SW, Park Y (2011) Selective algicidal action of peptides against harmful algal bloom species. PLoS One 6(10):e26733. doi:10.1371/journal.pone.0026733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul C, Pohnert G (2011) Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS One 6(6):e21032. doi:10.1371/journal.pone.0021032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul C, Pohnert G (2013) Induction of protease release of the resistant diatom Chaetoceros didymus in response to lytic enzymes from an algicidal bacterium. PLoS One 8(3):e57577. doi:10.1371/journal.pone.0057577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perzborn M, Syldatk C, Rudat J (2013) Enzymatical and microbial degradation of cyclic dipeptides (diketopiperazines). AMB Express 3(1):51. doi:10.1186/2191-0855-3-51

    Article  PubMed  PubMed Central  Google Scholar 

  • Prasad C (1995) Bioactive cyclic dipeptides. Peptides 16(1):151–164

    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 Manag 45(1):105–112. doi:10.1007/s00267-009-9393-6

    Article  Google Scholar 

  • Ran R, Zhang W, Cui B, Yi X, Han Z, Aibo W, 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 

  • Ross C, Santiago-Vazquez L, Paul V (2006) Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 78(1):66–73. doi:10.1016/j.aquatox.2006.02.007

    Article  CAS  PubMed  Google Scholar 

  • Shunyu S, Yongding L, Yinwu S, Genbao L, Li D (2006) Lysis of Aphanizomenon flos-aquae (Cyanobacterium) by a bacterium Bacillus cereus. Biol Control 39:345–351

    Article  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 

  • Stark T, Hofmann T (2005) Structures, sensory activity, and dose/response functions of 2,5-diketopiperazines in roasted cocoa nibs (Theobroma cacao). J Agric Food Chem 53(18):7222–7231. doi:10.1021/jf051313m

    Article  CAS  PubMed  Google Scholar 

  • Stierle AC, Cardellina JH 2nd, Singleton FL (1988a) A marine Micrococcus produces metabolites ascribed to the sponge Tedania ignis. Experientia 44(11–12):1021

    Article  CAS  PubMed  Google Scholar 

  • Stierle AC, Cardellina JH, Strobel GA (1988b) Maculosin, a host-specific phytotoxin for spotted knapweed from Alternaria alternata. Proc Natl Acad Sci U S A 85(21):8008–8011

    Article  CAS  PubMed  PubMed Central  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 

  • 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 

  • 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 

  • 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 

  • 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 H, An X, Zhou Y, Zhang B, Zhang S, Li D, Chen Z, Li Y, Bai S, Lv J, Zheng W, Tian Y, Zheng T (2013) Effect of oxidative stress induced by Brevibacterium sp. BS01 on a HAB causing species—Alexandrium tamarense. PLoS One 8(5):e63018

    Article  CAS  PubMed  PubMed Central  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 

  • Zurawell RW, Chen H, Burke JM, Prepas EE (2005) Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J Toxicol Environ Health B Crit Rev 8(1):1–37. doi:10.1080/10937400590889412

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 21277089), the National Basic Research Program of China (973 Program) (No. 2012CB720802), the National High Technology Research and Development Program of China (863 Program) (No. 2011AA100901), and the National Natural Science Foundation of China (No. J1210047).

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  1. State Key Laboratory of Microbial Metabolism and School of Life Science and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan Rd., Shanghai, 200240, China

    Zhenghua Li, Mengxin Geng & Hong Yang

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  1. Zhenghua Li
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  2. Mengxin Geng
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  3. Hong Yang
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Correspondence to Hong Yang.

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Electronic supplementary material contains phenotypic characteristics of strain Lzh-5, some details for purification (Fig. S4–Fig. S9) and identification (Fig. S10–Fig. S15) of the algicidal compounds.

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Li, Z., Geng, M. & Yang, H. Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa . Appl Microbiol Biotechnol 99, 981–990 (2015). https://doi.org/10.1007/s00253-014-6043-6

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