Skip to main content
Log in

Growth, death, and photobiology of dinoflagellates (Dinophyceae) under bacterial-algicide control

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Naturally occurring allelopathic compounds, specific to some phytoplankton, may be a good source of bio-control agents against microalgae responsible for harmful algal blooms (HABs). Global expansion of HABs has invigorated research into different approaches to control these algae, including the search for naturally derived algicidal compounds. Here, we investigated the effects of a filtrate from the algicidal marine bacterium Shewanella sp. IRI-160 on photochemical function of four cultured dinoflagellates, Karlodinium veneficum, Gyrodinium instriatum, Prorocentrum minimum, and Alexandrium tamarense. The filtrate (designated IRI-160AA) contains bioactive compound(s), which were recently shown to inhibit growth of several dinoflagellate species. Results of this study show that all dinoflagellates but P. minimum exhibited photosystem II (PSII) inhibition, loss of photosynthetic electron transport, and varying degrees of cellular mortality. Exposure assays over 24 h showed that PSII inhibition and loss of cell membrane integrity occurred simultaneously in G. instriatum, but not in K. veneficum, where PSII activity declined prior to losing outer-membrane integrity. In addition, PSII inhibition and population growth inhibition were dose-dependent in K. veneficum, with an average EC-50 of 7.9 % (v/v) IRI-160AA. Application of IRI-160AA induced significantly higher PSII inhibition and cell mortality in K. veneficum subjected to continuous darkness as compared to cells maintained with 12:12 h light/dark cycles, while no such dark effect was noted for G. instriatum. The marked differences in the rate and impact of this algicide suggest that multiple cellular targets and different cascades of cellular dysfunction occur across these dinoflagellates.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:562–584

    Article  Google Scholar 

  • Anderson DM, Burkholder JM, Cochlan W, Glibert PM, Gobler CJ, Heil CA, Kudela RM, Parsons ML, Rensel JEJ, Townsend DW, Trainer VL, Vargo GA (2008) Harmful algal blooms and eutrophication: examining linkages from selected coastal regions of the United States. Harmful Algae 8:39–53

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bachmann RW, Hoyer MV, Fernandez C, Canfield DE Jr (2003) An alternative to proposed phosphorus TMDLs for the management of Lake Okeechobee. Lake Reserv Manage 19:251–264

    Article  CAS  Google Scholar 

  • Bergo E, Segalla A, Giacometti GM, Tarantino D, Soave C, Andreucci F, Barbato R (2003) Role of visible light in the recovery of photosystem II structure and function from ultraviolet-B stress in higher plants. J Exp Bot 54:1665–1673

    Article  PubMed  CAS  Google Scholar 

  • Bolch CJS, de Salas MF (2007) A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandriumtamarensis complex” to Australasia. Harmful Algae 6:465–485

    Article  CAS  Google Scholar 

  • Boylan JD, Morris JE (2003) Limited effects of barley straw on algae and zooplankton in a midwestern pond. Lake Reserv Manage 19:265–271

    Article  Google Scholar 

  • Cosgrove J, Borowitzka MA (2010) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prasil OJ, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–18

    Chapter  Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302–317

    Article  Google Scholar 

  • Einhellig FA (1999) An integrated view of allelochemcials amid multiple stresses. In: Inderjit, Dakshini KMM, Foy CL (eds) Principles and practices in plant ecology: allelochemical interactions. CRC, Boca Raton, pp 479–494

    Google Scholar 

  • Faust MA, Larsen J, Moestrup Ø (1999) Potentially toxic phytoplankton. 3. Genus Prorocentrum (Dinophyceae). In: Lindley JA (ed) ICES identification leaflets for plankton. Leaflet no. 184. Copenhagen, pp 1–24

  • Fukuyo Y (1985) Morphology of Protogonyaulax tamarensis (Lebour) Taylor and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters. Bull Mar Sci 37:529–537

    Google Scholar 

  • Furusato E, Asaeda T, Manatunge J (2004) Tolerance for prolonged darkness of three phytoplankton species, Microcystis aeruginosa (Cyanophyceae), Scenedesmus quadricauda (Chlorophyceae), and Melosira ambigua (Bacillariophyceae). Hydrobiologia 527:153–162

    Article  Google Scholar 

  • Gleason FK, Case DE (1986) Activity of the natural algicide, cyanobacterin, on angiosperms. Plant Physiol 80:834–837

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson S, Hultberg M, Figueroa RI, Rengefors K (2009) On the control of HAB species using low biosurfactant concentrations. Harmful Algae 8:857–863

    Article  CAS  Google Scholar 

  • HAB RDDTT (2008) In: Dortch Q, Anderson DM, Ayres DL, Glibert PM (eds) Harmful algal bloom research, development, demonstration, and technology transfer national workshop report. Woods Hole, Massachusetts, USA

    Google Scholar 

  • Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99

    Article  Google Scholar 

  • Hallegraeff GM (2010) Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J Phycol 46:220–235

    Article  CAS  Google Scholar 

  • Hare CE, Demir ED, Coyne KJ, Cary SC, Kirchman DL, Hutchins D (2005) A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful Algae 4:221–234

    Article  Google Scholar 

  • Heisler J, Glibert P, Burkholder J, Anderson D, Cochlan W, Dennison W, Dortch Q, Gobler C, Heil C, Humphries E, Lewitus A, Magnien R, Marshall HG, Sellner K, Stockwell D, Stoecker DK, Suddleson M (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3–13

    Article  CAS  Google Scholar 

  • Hoagland P, Scatasta S (2006) The economic effects of harmful algal blooms. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin, pp 391–402

    Chapter  Google Scholar 

  • Jauzein C, Collos Y, Laabir M, Vaquer A (2011) Dark metabolism and carbon-nitrogen uncoupling in the toxic dinoflagellate Alexandrium catenella (Dinophyceae). Harmful Algae 11:73–80

    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 33:7066–7073

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeong HJ, Kim JS, Yoo YD, Kim ST, Song JY, Kim TH, Seong KA, Kang NS, Kim MS, Kim JH, Kim S, Ryu J, Lee HM, Yih WH (2008) Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7:368–377

    Article  Google Scholar 

  • Jungo E, Visser PM, Stroom J, Mur LR (2001) Artificial mixing to reduce growth of the blue-green alga Microcystis in Lake Nieuwe Meer, Amsterdam: an evaluation of 7 years of experience. Water Sci Technol Water Supply 1:17–23

    CAS  Google Scholar 

  • Kang Y-H, Jung SW, Jo S-H, Han M-S (2011) Field assessment of the potential of algicidal bacteria against diatom blooms. Biocontrol Sci Techn 21:969–984

    Article  Google Scholar 

  • Kim HG (2006) Mitigation and controls of HABs. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin, pp 327–338

    Chapter  Google Scholar 

  • Kim B-H, Sang M, Hwang S-J, Han M-S (2008) In situ bacterial mitigation of the toxic cyanobacterium Microcystis aeruginosa: implications for biological bloom control. Limnol Oceanog-Meth 6:513–522

    Article  CAS  Google Scholar 

  • Kim Y-M, Wu Y, Duong TU, Ghodake GS, Kim SW, Jin ES, Cho H (2010) Thiazolidinediones as a novel class of algicides against red tide harmful algal species. Appl Biochem Biotechnol 162:2273–2283

    Article  PubMed  CAS  Google Scholar 

  • Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106

    Article  PubMed  CAS  Google Scholar 

  • Legrande C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Article  Google Scholar 

  • Leu E, Krieger-Liszkay A, Goussias C, Gross EM (2002) Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiol 130:2011–2018

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lu Y, Wang J, Yu Y, Su W, Kong F (2013) Inhibition of Camellia sinensis (L.) O. Kuntze on Microcystis aeruginosa and isolation of the inhibition factors. Biotechnol Lett. doi:10.1007/s10529-013-1188-4

    Google Scholar 

  • Matthijs HCP, Visser PM, Reeze B, Meeuse J, Slot PC, Wijn G, Talens R, Huisman J (2012) Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46:1460–1472

    Article  PubMed  CAS  Google Scholar 

  • Mayali X, Franks PJS, Azam F (2007) Bacterial induction of temporary cyst formation by the dinoflagellate Lingulodinium polyedrum. Aquat Microb Ecol 50:51–62

    Article  Google Scholar 

  • Mcleod DJ, Hallegraeff GM, Hosie GW, Richardson AJ (2012) Climate-driven range expansion of the red-tide dinoflagellate Noctiluca scintillans into the Southern Ocean. J Plankton Res 34:332–337

    Article  Google Scholar 

  • Moore SK, Trainer VL, Mantua NJ, Parker MS, Laws EA, Backer LC, Fleming LE (2008) Impacts of climate variability and future climate change on harmful algal blooms and human health. Environ Health. doi:10.1186/1476-069X-7-S2-S4

    Google Scholar 

  • Mu R, He Y, Liu S, Wang X, Fan Z (2009) The algicidal characteristics of one algae-lysing FDT5 bacterium on Microcystis aeruginosa. Geomicrobiol J 26:516–521

    Article  CAS  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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Patron NJ, Waller RF, Keeling PJ (2006) A tertiary plastid uses genes from two endosymbionts. J Mol Biol 357:1373–1382

    Article  PubMed  CAS  Google Scholar 

  • Paul C, Pohnert G (2012) Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS ONE 6(6):e21032

    Article  Google Scholar 

  • Peters E, Thomas DN (1996) Prolonged darkness and diatom mortality: I. Marine Antarctic species. J Exp Mar Biol Ecol 207:25–41

    Article  Google Scholar 

  • Pokrzywinski KL, Place AR, Warner ME, Coyne KJ (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 

  • Popels LC, MacIntyre HL, Warner ME, Zhang YH, Hutchins DA (2007) Physiological responses during dark survival and recovery in Aureococcus anophagefferens (Pelagophyceae). J Phycol 43:32–42

    Article  CAS  Google Scholar 

  • Rensel JE, Whyte JNC (2003) Finfish mariculture and harmful algal blooms. In: Hallegraeff, GM, Anderson DM, Cembella AD (eds) Manual on harmful marine algae, revised edn. IOC UNESCO, pp 693–722

  • Rounsefell GA, Evans JE (1958) Large-scale experimental test of copper sulfate as a control for the Florida red tide. US Fish Wld S Spec Sci Rep 270

  • Saradadevi K, Raghavendra S (1992) Dark respiration protects photosynthesis against photoinhibition in mesophyll protoplasts of pea (Pisum sativum). Plant Physiol 99:1232–1237

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Segovia M, Berges JA (2005) Effect of inhibitors of protein synthesis and DNA replication on the induction of proteolytic activities, caspase-like activities and cell death in the unicellular chlorophyte Dunaliella tertiolecta. Eur J Phycol 40:21–30

    Article  CAS  Google Scholar 

  • Sengco MR (2009) Prevention and control of Karenia brevis blooms. Harmful Algae 8:623–628

    Article  CAS  Google Scholar 

  • Sengco MR, Anderson DM (2004) Controlling harmful algal blooms through clay flocculation. J Eukaryot Microbiol 51:169–172

    Article  PubMed  CAS  Google Scholar 

  • Shi S, Tang D, Liu Y (2009) Effects of an algicidal bacterium Pseudomonas mendocina on the growth and antioxidant system of Aphanizomenon flos-aquae. Curr Microbiol 59:107–112

    Article  PubMed  CAS  Google Scholar 

  • Smayda TJ (2007) Reflections on the ballast water dispersal—harmful algal bloom paradigm. Harmful Algae 6:601–622

    Article  Google Scholar 

  • Smayda TJ, Mitchell-Innes B (1974) Dark survival of autotrophic, planktonic marine diatoms. Mar Biol 25:195–202

    Article  Google Scholar 

  • Smith GD, Doan NT (1999) Cyanobacterial metabolites with bioactivity against photosynthesis in cyanobacteria, algae and higher plants. J Appl Phycol 11:337–344

    Article  CAS  Google Scholar 

  • Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol Evol 24:201–207

    Article  PubMed  Google Scholar 

  • Sotirova AV, Spasova DI, Galabova DN, Karpenko E, Shulga A (2008) Rhamnolipid-biosurfactant permeabilizing effects on gram-positive and gram-negative bacterial strains. Curr Microbiol 56:639–647

    Article  PubMed  CAS  Google Scholar 

  • Takamura Y, Yamada T, Kimoto A, Kanehama N, Tanaka T, Nakadaira S, Yagi O (2004) Growth inhibition of Microcystis cyanobacteria by l-lysine and disappearance of natural Microcystis blooms with spraying. Microbes Environ 19:31–39

    Article  Google Scholar 

  • Terlizzi DE, Ferrier MD, Armbrester EA, Anlauf KA (2002) Inhibition of dinoflagellate growth by extracts of barley straw (Hordeum vulgare). J Appl Phycol 14:275–280

    Article  CAS  Google Scholar 

  • Trainer VM, Suddleson M (2005) Monitoring approaches for early warning of domoic acid events in Washington State. Oceanography 18:228–237

    Article  Google Scholar 

  • Van Dolah FV (2000) Marine algal toxins: origins, health effects, and their increased occurrence. Environ Health Persp 108:133–141

    Article  Google Scholar 

  • Wang X, Gong L, Liang S, Han X, Zhu C, Li Y (2005) Algicidal activity of rhamnolipid biosurfactants produced by Pseudomonas aeruginosa. Harmful Algae 4:433–443

    Article  CAS  Google Scholar 

  • Wisecaver JH, Hackett JD (2011) Dinoflagellate genome evolution. Annu Rev Microbiol 65:369–387

    Article  PubMed  CAS  Google Scholar 

  • Wu J-T, Chiang Y-R, Huang W-Y, Jane W-N (2006) Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria. Aquat Toxicol 80:338–345

    Article  PubMed  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Van Dolah FM, Nosenko T, Lidie KL, Bhattacharya D (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol 22:1299–1308

    Article  PubMed  CAS  Google Scholar 

  • Zingone A, Enevoldsen HO (2000) The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast Manage 43:725–748

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Oceanic and Atmospheric Association (NOAA) Prevention, Control and Mitigation of HABs (PCM HAB) program (Grant #NA10NOS4780136 to KJC and MEW).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles L. Tilney.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tilney, C.L., Pokrzywinski, K.L., Coyne, K.J. et al. Growth, death, and photobiology of dinoflagellates (Dinophyceae) under bacterial-algicide control. J Appl Phycol 26, 2117–2127 (2014). https://doi.org/10.1007/s10811-014-0248-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-014-0248-z

Keywords

Navigation