Skip to main content
SpringerLink
Log in

Photosynthetic inhibition and oxidative stress to the toxic Phaeocystis globosa caused by a diketopiperazine isolated from products of algicidal bacterium metabolism

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Algicidal bacteria have been turned out to be available for inhibiting Phaeocystis globosa which frequently caused harmful algal blooms and threatened to economic development and ecological balance. A marine bacterium Bacillus sp. Ts-12 exhibited significant algicidal activity against P. globosa by indirect attack. In present study, an algicidal compound was isolated by silica gel column, Sephadex G-15 column and HPLC, further identified as hexahydropyrrolo[1,2-a]pyrazine-1,4-dione, cyclo-(Pro-Gly), by GC-MS and 1H-NMR. Cyclo-(Pro-Gly) significantly increased the level of reactive oxygen species (ROS) within P. globosa cells, further activating the enzymatic and non-enzymatic antioxidant systems, including superoxide dismutase (SOD), catalase (CAT), glutathione (GSH) and ascorbic acid (AsA). The increase in methane dicarboxylic aldehyde (MDA) content showed that the surplus ROS induced lipid peroxidation on membrane system. Transmission electron microscope (TEM) and flow cytometry (FCM) analysis revealed that cyclo-(Pro-Gly) caused reduction of Chl-a content, destruction of cell membrane integrity, chloroplasts and nuclear structure. Real-time PCR assay showed that the transcriptions of photosynthesis related genes (psbA, psbD, rbcL) were significantly inhibited. This study indicated that cyclo-(Pro-Gly) from marine Bacillus sp. Ts-12 exerted photosynthetic inhibition and oxidative stress to P. globosa and eventually led to the algal cells lysis. This algicidal compound might be potential bio-agent for controlling P. globosa red tide.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad, P., Jaleel, C.A., Salem, M.A., Nabi, G., and Sha rma, S. 2010. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit. Rev. Biotechnol. 30, 161–175.

    Article  CAS  PubMed  Google Scholar 

  • Allahverdiyeva, Y., Mamedov, F., Maenpaa, P., Vass, I., and Aro, E.M. 2005. Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: Characterization of the rbcl deletion mutant of tobacco. BBA-Bioenergetics 1709, 69–83.

    Article  CAS  PubMed  Google Scholar 

  • Amaro, A.M., Fuentes, M.S., Ogalde, S.R., Venegas, J.A., and Suarez-Isla, B.A. 2005. Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J. Eukaryot. Microbiol. 52, 191–200.

    Article  PubMed  Google Scholar 

  • Anderson, D.M., Cembella, A.D., and Hallegraeff, G.M. 2012. Progress in understanding harmful algal blooms: Paradigm shifts and new technologies for research, monitoring, and management, pp. 143–176. In C. A. Carlson and S. J. Giovannoni (eds.), Annual review of marine science, vol 4.

    Google Scholar 

  • Apel, K. and Hirt, H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399.

    Article  CAS  PubMed  Google Scholar 

  • Asada, K. 2006. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391–396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avery, S.V. 2011. Molecular targets of oxidative stress. Biochem. J. 434, 201–210.

    Article  CAS  PubMed  Google Scholar 

  • Chagas, R.M., Silveira, J.A.G., Ribeiro, R.V., Vitorello, V.A., and Carrer, H. 2008. Photochemical damage and comparative performance of superoxide dismutase and ascorbate peroxidase in sugarcane leaves exposed to paraquat-induced oxidative stress. Pestic. Biochem. Physiol. 90, 181–188.

    Article  CAS  Google Scholar 

  • Chang, D.W., Hsieh, M.L., Chen, Y.M., Lin, T.F., and Chang, J.S. 2011. Kinetics of cell lysis for Microcystis aeruginosa and Nitzschia palea in the exposure to beta-cyclocitral. J. Hazard. Mater. 185, 1214–1220.

    Article  CAS  PubMed  Google Scholar 

  • Duan, J.L., Li, X.J., Gao, J.M., Wang, D.S., Yan, Y., and Xue, Q.H. 2013. Isolation and identification of endophytic bacteria from root tissues of Salvia miltiorrhiza Bge. and determination of their bioactivities. Ann. Microbiol. 63, 1501–1512.

    Article  CAS  Google Scholar 

  • Erickson, J.M., Rahire, M., Malnoe, P., Girard-Bascou, J., Pierre, Y., Bennoun, P., and Rochaix, J.D. 1986. Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem ii stability and d1 expression. EMBO J. 5, 1745–1754.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer, C.H., Lelandais, M., and Kunert, K.J. 1994. Photooxidative stress in plants. Physiol. Plant. 92, 696–717.

    Article  CAS  Google Scholar 

  • Guan, C., Guo, X., Cai, G., Zhang, H., Li, Y., Zheng, W., and Zheng, T. 2014. Novel algicidal evidence of a bacterium Bacillus sp. Lp-10 killing Phaeocystis globosa, a harmful algal bloom causing species. Biol. Control 76, 79–86.

    Article  Google Scholar 

  • Ham, M.H., Choi, J.H., Boghossian, A.A., Jeng, E.S., Graff, R.A., Heller, D.A., Chang, A.C., Mattis, A., Bayburt, T.H., Grinkova, Y.V., et al. 2010. Photoelectrochemical complexes for solar energy conversion that chemically and autonomously regenerate. Nat. Chem. 2, 929–936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton, C.E., Gundel, P.E., Helander, M., and Saikkonen, K. 2012. Endophytic mediation of reactive oxygen species and antioxidant activity in plants: A review. Fungal Divers. 54, 1–10.

    Article  Google Scholar 

  • Hong, Y., Hu, H.Y., Xie, X., Sakoda, A., Sagehashi, M., and Li, F.M. 2009. Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. Aquat. Toxicol. 91, 262–269.

    Article  CAS  PubMed  Google Scholar 

  • Jeong, S.Y., Ishida, K., Ito, Y., Okada, S., and Murakami, M. 2003. Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. sy-1, against the harmful dinoflagellate, cochlodinium polykrikoides. Tetrahedron Lett. 44, 8005–8007.

    Article  CAS  Google Scholar 

  • Kim, M.J., Jeong, S.Y., and Lee, S.J. 2008. Isolation, identification, and algicidal activity of marine bacteria against Cochlodinium polykrikoides. J. Appl. Phycol. 20, 1069–1078.

    Article  Google Scholar 

  • Kim, Y.S., Son, H.J., and Jeong, S.Y. 2015. Isolation of an algicide from a marine bacterium and its effects against the toxic dinoflagellate Alexandrium catenella and other harmful algal bloom species. J. Microbiol. 53, 511–517.

    Article  PubMed  Google Scholar 

  • Kobayashi, Y., Imamura, S., Hanaoka, M., and Tanaka, K. 2011. A tetrapyrrole-regulated ubiquitin ligase controls algal nuclear DNA replication. Nat. Cell Biol. 13, 483–487.

    Article  CAS  PubMed  Google Scholar 

  • Kodani, S., Imoto, A., Mitsutani, A., and Murakami, M. 2002. Isolation and identification of the antialgal compound, harmane (1-methyl-β-carboline), produced by the algicidal bacterium, Pseudomonas sp. k44-1. J. Appl. Phycol. 14, 109–114.

    Article  CAS  Google Scholar 

  • Kwok, C.T., van de Merwe, J.P., Chiu, J.M.Y., and Wu, R.S.S. 2012. Antioxidant responses and lipid peroxidation in gills and hepatopancreas of the mussel Perna viridis upon exposure to the red-tide organism Chattonella marina and hydrogen peroxide. Harmful Algae 13, 40–46.

    Article  CAS  Google Scholar 

  • Larson, R.A. 1988. The antioxidants of higher plants. Phytochemistry 27, 969–978.

    Article  CAS  Google Scholar 

  • Lei, X., Li, D., Li, Y., Chen, Z., Chen, Y., Cai, G., Yang, X., Zheng, W., and Zheng, T. 2015. Comprehensive insights into the response of Alexandrium tamarense to algicidal component secreted by a marine bacterium. Front. Microbiol. 6.

    Google Scholar 

  • Li, Z., Geng, M., and Yang, H. 2014a. Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa. Appl. Microbiol. Biotechnol. 99, 981–990.

    Article  PubMed  Google Scholar 

  • Li, Z., Lin, S., Liu, X., Tan, J., Pan, J., and Yang, H. 2014b. 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.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Zhu, H., Guan, C., Zhang, H., Guo, J., Chen, Z., Cai, G., Lei, X., Zheng, W., Tian, Y., et al. 2014c. Towards molecular, physiological, and biochemical understanding of photosynthetic inhibition and oxidative stress in the toxic Alexandrium tamarense induced by a marine bacterium. Appl. Microbiol. Biotechnol. 98, 4637–4652.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Zhu, H., Lei, X., Zhang, H., Cai, G., Chen, Z., Fu, L., Xu, H., and Zheng, T. 2015. The death mechanism of the harmful algal bloom species alexandrium tamarense induced by algicidal bacterium deinococcus sp. Y35. Front. Microbiol. 6, 992.

    PubMed  PubMed Central  Google Scholar 

  • Livak, K.J. and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative pcr and the 2−ΔΔCT method. Methods 25, 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Luo, J., Wang, Y., Tang, S., Liang, J., Lin, W., and Luo, L. 2013. Isolation and identification of algicidal compound from streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8, e76444.

    Article  Google Scholar 

  • Maughan, S.C., Pasternak, M., Cairns, N., Kiddle, G., Brach, T., Jarvis, R., Haas, F., Nieuwland, J., Lim, B., Mueller, C., et al. 2010. Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc. Natl. Acad. Sci. USA. 107, 2331–2336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mihara, M. and Uchiyama, M. 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem. 86, 271–278.

    Article  CAS  PubMed  Google Scholar 

  • Pokrzywinski, K.L., Place, A.R., Warner, M.E., and Coyne, K.J. 2012. Investigation of the algicidal exudate produced by Shewanella sp. iri-160 and its effect on dinoflagellates. Harmful Algae 19, 23–29.

    Article  CAS  Google Scholar 

  • Qi, Y.Z., Chen, J.F., Wang, Z.H., Xu, N., Wang, Y., Shen, P.P., Lu, S.H., and Hodgkiss, I.J. 2004. Some observations on harmful algal bloom (hab) events along the coast of guangdong, southern china in 1998. Hydrobiologia 512, 209–214.

    Article  Google Scholar 

  • Qian, H., Sheng, G.D., Liu, W., Lu, Y., Liu, Z., and Fu, Z. 2008. Inhibitory effects of atrazine on Chlorella vulgaris as assessed by real-time polymerase chain reaction. Environ. Toxicol. Chem. 27, 182–187.

    Article  CAS  PubMed  Google Scholar 

  • Qian, H., Xu, X., Chen, W., Jiang, H., Jin, Y., Liu, W., and Fu, Z. 2009. Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75, 368–375.

    Article  CAS  PubMed  Google Scholar 

  • Styring, S., Virgin, I., Ehrenberg, A., and Andersson, B. 1990. Strong light photoinhibition of electrontransport in photosystem ii. Impairment of the function of the first quinone acceptor, QA. Biochim. Biophys. Acta 1015, 269–278.

    Article  CAS  Google Scholar 

  • Tommonaro, G., Abbamondi, G.R., Iodice, C., Tait, K., and De Rosa, S. 2012. Diketopiperazines produced by the halophilic archaeon, Haloterrigena hispanica, activate AHL bioreporters. Microb. Ecol. 63, 490–495.

    Article  CAS  PubMed  Google Scholar 

  • Yang, C.Y., Liu, S.J., Zhou, S.W., Wu, H.F., Yu, J.B., and Xia, C.H. 2011. Allelochemical ethyl 2-methyl acetoacetate (eMA) induces oxidative damage and antioxidant responses in Phaeodactylum tricornutum. Pestic. Biochem. Physiol. 100, 93–103.

    Article  CAS  Google Scholar 

  • Yang, X., Li, X., Zhou, Y., Zheng, W., Yu, C., and Zheng, T. 2014. Novel insights into the algicidal bacterium dh77-1 killing the toxic dinoflagellate Alexandrium tamarense. Sci. Total Environ. 482–483, 116–124.

    Article  PubMed  Google Scholar 

  • Yang, C., Zhou, J., Liu, S., Fan, P., Wang, W., and Xia, C. 2013. Allelochemical induces growth and photosynthesis inhibition, oxidative damage in marine diatom Phaeodactylum tricomutum. J. Exp. Mar. Biol. Ecol. 444, 16–23.

    Article  CAS  Google Scholar 

  • Zhang, B., Cai, G., Wang, H., Li, D., Yang, X., An, X., Zheng, X., Tian, Y., Zheng, W., and Zheng, T. 2014a. Streptomyces alboflavus rps and its novel and high algicidal activity against harmful algal bloom species phaeocystis globosa. PLoS One 9.

    Google Scholar 

  • Zhang, H., Lv, J., Peng, Y., Zhang, S., An, X., Xu, H., Zhang, J., Tian, Y., Zheng, W., and Zheng, T. 2014b. Cell death in a harmful algal bloom causing species Alexandrium tamarense upon an algicidal bacterium induction. Appl. Microbiol. Biotechnol. 98, 7949–7958.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, L., Chen, L., and Yin, P. 2014. Algicidal metabolites produced by Bacillus sp. strain b1 against Phaeocystis globosa. J. Ind. Microbiol. Biotechnol. 41, 593–599.

    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., et al. 2013. A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Appl. Microbiol. Biotechnol. 97, 9207–9215.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, School of Life Science and technology, Jinan University, Guangzhou, 510632, P. R. China

    Shuo Tan, Xiaoli Hu & Pinghe Yin

  2. Key Laboratory of Water/Soil Toxic Pollutants Control and Bioremediation of Guangdong Higher Education Institutes, School of Environment, Jinan University, Guangzhou, 510632, P. R. China

    Ling Zhao

Authors
  1. Shuo Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoli Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pinghe Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ling Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pinghe Yin or Ling Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tan, S., Hu, X., Yin, P. et al. Photosynthetic inhibition and oxidative stress to the toxic Phaeocystis globosa caused by a diketopiperazine isolated from products of algicidal bacterium metabolism. J Microbiol. 54, 364–375 (2016). https://doi.org/10.1007/s12275-016-6012-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-016-6012-0

Keywords

Search

Navigation