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Cell death in a harmful algal bloom causing species Alexandrium tamarense upon an algicidal bacterium induction

  • Applied microbial and cell physiology
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Abstract

Harmful algal blooms occur throughout the world, destroying aquatic ecosystems and threatening human health. The culture supernatant of the marine algicidal bacteria DHQ25 was able to lysis dinoflagellate Alexandrium tamarense. Loss of photosynthetic pigments, accompanied by a decline in Photosystem II (PSII) photochemical efficiency (Fv/Fm), in A. tamarense was detected under bacterial supernatant stress. Transmission electron microscope analysis showed obvious morphological modifications of chloroplast dismantling as a part of the algicidal process. The PSII electron transport chain was seriously blocked, with its reaction center damaged. This damage was detected in a relative transcriptional level of psbA and psbD genes, which encode the D1 and D2 proteins in the PSII reaction center. And the block in the electron transport chain of PSII might generate excessive reactive oxygen species (ROS) which could destroy the membrane system and pigment synthesis and activated enzymic antioxidant systems including superoxide dismutase (SOD) and catalase (CAT). This study indicated that marine bacteria with indirect algicidal activity played an important role in the changes of photosynthetic process in a harmful algal bloom species.

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References

  • Alboresi A, Dall’Osto L, Aprile A, Carillo P, Roncaglia E, Cattivelli L, Bassi R (2011) Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC plant biol 11(1):62

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Amaro AM, Fuentes MS, Ogalde SR, Venegas JA, Suarez-Isla BA (2005) Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J Eukaryot Microbiol 52(3):191–200

    Article  PubMed  Google Scholar 

  • Anderson DM (1997) Turning back the harmful red tide. Nature 388(6642):513–514

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bai SJ, Huang LP, Su JQ, Tian Y, Zheng TL (2011) Algicidal effects of a novel marine actinomycete on the toxic dinoflagellate Alexandrium tamarense. Curr Microbiol 62(6):1774–81

    Article  CAS  PubMed  Google Scholar 

  • Baker KH, Herson DS (1978) Interactions between the diatom Thallasiosira pseudonanna and an associated pseudomonad in a mariculture system. Appl Environ Microbiol 35(4):791–796

    CAS  PubMed Central  PubMed  Google Scholar 

  • Banin E, Khare SK, Naider F, Rosenberg E (2001) Proline-rich peptide from the coral pathogen Vibrio shiloi that inhibits photosynthesis of zooxanthellae. Appl Environ Microbiol 67(4):1536–1541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Behrenfeld MJ, O’Malley RT, Siegel DA, McClain CR, Sarmiento JL, Feldman GC, Milligan AJ, Falkowski PG, Letelier RM, Boss ES (2006) Climate-driven trends in contemporary ocean productivity. Nature 444(7120):752–755

    Article  CAS  PubMed  Google Scholar 

  • Bird DF, Kalff J (1986) Bacterial grazing by planktonic lake algae. Science 231(4737):493–495

    Article  CAS  PubMed  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438(7064):90–93

    Article  CAS  PubMed  Google Scholar 

  • Doucette GJ (2006) Interactions between bacteria and harmful algae: a review. Nat Toxins 3(2):65–74

    Article  Google Scholar 

  • He YY, Häder DP (2002) Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp. J Photochem Photobiol B 66(1):73–80

    Article  CAS  PubMed  Google Scholar 

  • Izawa S (1980) Acceptors and donors and chloroplast electron transport. Method Enzymol 69:413–434

    Article  CAS  Google Scholar 

  • Kwok CT, van de Merwe JP, Chiu JM, Wu RS (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 

  • Lee YJ, Choi JK, Kim EK, Youn SH, Yang EJ (2008) Field experiments on mitigation of harmful algal blooms using a Sophorolipid—yellow clay mixture and effects on marine plankton. Harmful Algae 7(2):154–162

    Article  Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41(2):271–283

    Article  CAS  Google Scholar 

  • Li HS, Sun Q, Zhao SJ (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education, Beijing, pp 186–191

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔct method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Vonshak A (1999) Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New phytol 141(2):231–239

    Article  CAS  Google Scholar 

  • Mayali X, Azam F (2005) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51(2):139–144

    Article  Google Scholar 

  • Mitsutani A, Takesue K, Kirita M, Ishida Y (1992) Lysis of Skeletonema costatum by Cytophaga sp. isolated from the coastal water of the Ariake Sea. Nippon Suisan Gakkaishi 58(11):2159–2169

    Article  Google Scholar 

  • Nakashima T, Miyazaki Y, Matsuyama Y, Muraoka W, Yamaguchi K, Oda T (2006) Producing mechanism of an algicidal compound against red tide phytoplankton in a marine bacterium γ-proteobacterium. Appl Microbiol Biotech 73(3):684–690

    Article  CAS  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20(20):5587–5594

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry-us 43(35):11321–11330

    Article  CAS  Google Scholar 

  • Okamoto O, Pinto E, Latorre L, Bechara E, Colepicolo P (2001) Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Con Tox 40(1):18–24

    Article  CAS  Google Scholar 

  • Perez-Perez ME, Lemaire SD, Crespo JL (2012) Reactive oxygen species and autophagy in plants and algae. Plant Physiol 160(1):156–164

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qian H, Yu S, Sun Z, Xie X, Liu W, Fu Z (2010) Effects of copper sulfate, hydrogen peroxide and N-phenyl-2-naphthylamine on oxidative stress and the expression of genes involved photosynthesis and microcystin disposition in Microcystis aeruginosa. Aquat Toxicol 99(3):405–12

    Article  CAS  PubMed  Google Scholar 

  • Shukla B, Rai LC (2006) Potassium-induced inhibition of photosynthesis and associated electron transport chain of Microcystis: implication for controlling cyanobacterial blooms. Harmful algae 5(2):184–191

    Article  CAS  Google Scholar 

  • Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom “Thalassiosira pseudonana”: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr:494–505

  • Steele JH (1962) Environmental control of photosynthesis in the sea. Limnol Oceanogr:137–150

  • Su J, Yang X, Zheng T, Hong H (2007a) An efficient method to obtain axenic cultures of Alexandrium tamarense—a PSP-producing dinoflagellate. J Microbiol Methods 69(3):425–430

    Article  CAS  PubMed  Google Scholar 

  • Su JQ, Yang XR, Zheng TL, Tian Y, Jiao NZ, Cai LZ, Hong HS (2007b) Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 6(6):799–810

    Article  CAS  Google Scholar 

  • Su J, Yang X, Zhou Y, Zheng T (2011) Marine bacteria antagonistic to the harmful algal bloom species Alexandrium tamarense (Dinophyceae). Biol Control 56(2):132–138

    Article  Google Scholar 

  • Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45(2):251–255

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Zhou Y, Bai S, Su J, Tian Y, Zheng T, Yang X (2010a) A novel marine bacterium algicidal to the toxic dinoflagellate Alexandrium tamarense. Lett Appl Microbiol 51(5):552–557

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Li Z, Su J, Tian Y, Ning X, Hong H, Zheng T (2010b) Lysis of a red-tide causing alga, Alexandrium tamarense, caused by bacteria from its phycosphere. Biol Control 52(2):123–130

    Article  Google Scholar 

  • Wang B, Yang X, Zhou Y, Lv J, Su J, Tian Y, Zhang J, Lin G, Zheng T (2012) An algicidal protein produced by bacterium isolated from the Donghai Sea, China. Harmful Algae 13:83–88

    Article  CAS  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96(14):8007–8012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang CY, Liu SJ, Zhou SW, Wu HF, Yu JB, Xia CH (2011) Allelochemical ethyl 2-methyl acetoacetate (EMA) induces oxidative damage and antioxidant responses in Phaeodactylum tricornutum. Pestic Biochem Phys 100(1):93–103

    Article  CAS  Google Scholar 

  • Yin L, Huang J, Huang W, Li D, Wang G, Liu Y (2005) Microcystin-RR-induced accumulation of reactive oxygen species and alteration of antioxidant systems in tobacco BY-2 cells. Toxicon 46(5):507–512

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Zhang B, Dai W, Zhang X (2011) Oxidative damage and antioxidant responses in Microcystis aeruginosa exposed to the allelochemical berberine isolated from golden thread. J plant physiol 168(7):639–643

    Article  CAS  PubMed  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 Central  PubMed  Google Scholar 

  • Zheng TL, Lv JL, Zhou YY, Su JQ, Yang XR, Tian Y (2011) Discovery and research on the marine bacteria capable of controlling HABs. J Xiamen Univ 50(3):445–454

    Google Scholar 

  • Zheng X, Zhang B, Zhang J, Huang L, Lin J, Li X, Zhou Y, Wang H, Yang X, Su J (2012) A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Appl microbiol biotech 97(20):9207–9215

    Article  Google Scholar 

  • Zhou W, Juneau P, Qiu B (2006) Growth and photosynthetic responses of the bloom-forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere 65:1738–1746

    Article  CAS  PubMed  Google Scholar 

  • Zhou LH, Zheng TL, Wang X, Ye JL, Tian Y, Hong HS (2007) Effect of five Chinese traditional medicines on the biological activity of a red-tide causing alga—Alexandrium tamarense. Harmful Algae 6:354–360

    Article  CAS  Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation (40930847, 41376119), Special Fund for PhD Program in the university-priority development area (20120121130001), and the Public Science and Technology Research Funds for Ocean Projects (201305016, 201305022). We would like to thank Professor John Hodgkiss of The University of Hong Kong for help with English.

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Authors and Affiliations

  1. State Key Laboratory of Marine Environmental Science and Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, School of Life Sciences, Xiamen University, 422, Siming Nan Road, Xiamen, 361005, China

    Huajun Zhang, Jinglin Lv, Yun Peng, Su Zhang, Xinli An, Hong Xu, Jun Zhang, Yun Tian, Wei Zheng & Tianling Zheng

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  1. Huajun Zhang
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  2. Jinglin Lv
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  3. Yun Peng
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  4. Su Zhang
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  6. Hong Xu
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  7. Jun Zhang
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  8. Yun Tian
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  9. Wei Zheng
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  10. Tianling Zheng
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Correspondence to Wei Zheng or Tianling Zheng.

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Huajun Zhang and Jinglin Lv contributed equally to this work and should be regarded as co-first authors.

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Zhang, H., Lv, J., Peng, Y. et al. Cell death in a harmful algal bloom causing species Alexandrium tamarense upon an algicidal bacterium induction. Appl Microbiol Biotechnol 98, 7949–7958 (2014). https://doi.org/10.1007/s00253-014-5886-1

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  • DOI: https://doi.org/10.1007/s00253-014-5886-1

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