Allelopathic effect of Ulva intestinalis thallus on selected Baltic cyanobacteria

Authors

  • Gracjana Budzałek Institute of Oceanography, University of Gdansk, Gdynia, Poland
  • Sylwia Śliwińska-Wilczewska Institute of Oceanography, University of Gdansk, Gdynia, Poland

DOI:

https://doi.org/10.24917/25438832.7.7

Keywords:

allelopathy, cyanobacteria, green macroalgae, growth, fluorescence, thallus

Abstract

Macroalgae have been found to produce active allelochemicals that inhibit of growth other organisms that compete with them for light and space. However, their allelopathic activity on Baltic cyanobacteria is still insufficiently recognised. Therefore, this study aimed to demonstrate the allelopathic effects of Baltic macroalga thallus (Ulva intestinalis) on the growth and photosynthetic activity of three bloom-forming cyanobacteria: Aphanizomenon sp., Nodularia spumigena, and Nostoc sp. This study investigated the cell count of the analysed cyanobacteria (N 105 mL-1), the maximum quantum yield of the second photosystem (PSII) in the dark (Fv/Fm), and the real quantum yield of PSII in the light (ΦPSII) (in the control and the experiments). After 7 days of exposure, the following were added: 0.01, 0.05, and 0.1 g mL-1 of U. intestinalis fresh thallus. It was found that thallus obtained from U. intestinalis had no statistically significant effect on the number of cells of the cyanobacterium Aphanizomenon sp. (at 0.05 and 0.1 g mL-1) and Nostoc sp. (at concentrations of 0.01 and 0.05 g mL−1). On the other hand, it was examined a stimulating effect of 0.01 g mL-1 of the fresh thallus on the number of Aphanizomenon sp. cells which constituted 168%, relative to the control. It was shown that the fresh thallus addition resulted in a decrease in the number of N. spumigena cells (45%, 27%, and 46% after addition of 0.01, 0.05, and 0.1 g wet weight mL−1 of fresh thallus, respectively). In experiments with Nostoc sp., the addition of U. intestinalis thallus has been a negative effect on cyanobacterial growth at 0.1 g mL−1 and constituted 97% of control. It was also found, that U. intestinalis had no allelopathic effect on fluorescence parameters of N. spumigena. All tested concentrations of thallus U. intestinalis (0.01, 0.05, and 0.1 g wet weight mL-1) stimulated the values of Fv/Fm or ΦPSII of cyanobacteria Aphanizomenon sp. and Nostoc sp. compared to the control. These studies help define the role of U. intestinalis allelopathy as a biological factor in the distribution of bloom-forming cyanobacteria in the coastal Baltic Sea region.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Anderson, D.M., Burkholder, J.M., Cochlan, W.P., Glibert, P.M., Gobler, C.J., Heil, C.A., Raphael, M.K., Parsons, M.L., Rensel, J.E., Townsend, D.W., Trainer, V.L., Vargo, G. A. (2008). Harmful algal blooms and eutrophication: examining linkages from selected coastal regions of the United States. Harmful algae, 8(1), 39–53. https://doi.org/10.1016/j.hal.2008.08.017

Berger, J., Schagerl, M. (2003). Allelopathic activity of Chara aspera. Hydrobiologia, 501(1), 109–115. https://doi.org/10.1023/A:1026263504260

Budzałek, G., Śliwińska-Wilczewska, S., Klin, M., Wiśniewska, K., Latała, A., Wiktor, J.M. (2021a). Changes in growth, photosynthesis performance, pigments, and toxin contents of bloom-forming cyanobacteria after exposure to macroalgal allelochemicals. Toxins, 13(8), 589. https://doi.org/10.3390/toxins13080589

Budzałek, G., Śliwińska-Wilczewska, S., Wiśniewska, K., Wochna, A., Bubak, I., Latała, A., Wiktor, J.M. (2021b). Macroalgal defense against competitors and herbivores. International Journal of Molecular Sciences, 22(15), 7865. https://doi.org/10.3390/ijms22157865

Budzałek, G., Śliwińska-Wilczewska, S., Latała, A. (2018). Allelopathic effect of Ulva intestinalis L. on the Baltic filamentous cyanobacterium Nostoc sp. Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 3, 80–89. http:doi.org/10.24917/25438832.3.6. ISSN 2543-8832.

Campbell, D., Hurry, V., Clarke, A.K., Gustafsson, P., Öquist, G. (1998). Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews, 62, 667–683. https://doi.org/10.1128/mmbr.62.3.667-683.1998

Carmona, R., Kraemer, G.P., Yarish, C. (2006). Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish–algal aquaculture system. Aquaculture, 252(1), 54–65. https://doi.org/10.1016/j.aquaculture.2005.11.049

Chopin, T., Buschmann, A.H., Halling, C., Troell, M., Kautsky, N., Neori, A., Kraemer, G.P., Zertuche- Gonzalez, J., Yarish, C., Neefus, C. (2001). Integrating seaweeds into marine aquaculture systems: a key toward sustainability. Journal of Phycology, 37(6), 975–986. https://doi.org/10.1046/j.1529-8817.2001.01137.x

Chopin, T., Robinson, S.M.C., Troell, M., Neori, A., Buschmann, A., Fang, J. G. (2008). Ecological engineering: multi-trophic integration for sustainable marine aquaculture. In: Encyclopedia of Ecology. Amsterdam: Elsevier.

Drobnik, J. (2007). Zielnik i zielnikoznastwo (Herbarium and studies of herbarium). PWN, Warszawa. 293 pp. [In Polish]

Guillard, R.R., Sieracki, M.S. (2005). Counting cells in cultures with the light microscope. Algal Culturing Techniques, 239–252. https://doi.org/10.1016/B978-012088426-1%2F50017-2

Guillard, R.R.L. (1975). Culture of phytoplankton for feeding marine invertebrates. In: W.L. Smith, M.H. Chanley (eds.), Culture of Marine Invertebrate Animals. New York, USA: Plenum Press, 26–60. https://doi.org/10.1007/978-1-4615-8714-9_3.

Harlin, M.M., Rice, E.L. (1987). Allelochemistry in marine macroalgae. Critical Reviews in Plant Sciences, 5(3), 237–249. https://doi.org/10.1080/07352688709382241

Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M., Cochlan, W., Dennison, W.C., Dortch, Q., Gobler, C.J., Heil, C.A., Humphries, E., Lewitus, A., Magnien, R., Marshall, H.G., Seller, K., Stockwell, D.A., Stoecker, D.K., Suddleson, M. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful algae, 8(1), 3–13. https://doi.org/10.1016/j.hal.2008.08.006

Irfanullah, H.M., Moss, B. (2005). Allelopathy of filamentous green algae. Hydrobiologia, 543(1), 169–179. https://doi.org/10.1007/s10750-004-6955-8

Jarchow, M.E., Cook, B.J. (2009). Allelopathy as a mechanism for the invasion of Typha angustifolia. Plant Ecology, 204(1), 113–124. https://doi.org/10.1007/s11258-009-9573-8

Jeong, J.H., Jin, H.J., Sohn, C.H., Suh, K.H., Hong, Y.K. (2000). Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. Journal of applied Phycology, 12(1), 37–43. https://doi.org/10.1023/A:1008139129057

Jin, Q., Dong, S. (2003). Comparative studies on the allelopathic effects of two different strains of Ulva pertusa on Heterosigma akashiwo and Alexandrium tamarense. Journal of Experimental Marine Biology and Ecology, 293(1), 41–55. http://dx.doi.org/10.1016/S0022-0981(03)00214-4

Jin, Q., Dong, S., Wang, C. (2005). Allelopathic growth inhibition of Prorocentrum micans (Dinophyta) by Ulva pertusa and Ulva linza (Chlorophyta) in laboratory cultures. European Journal of Phycology, 40(1), 31–37. https://doi.org/10.1080/09670260400019741

Kahru, M., Elmgren, R., Kaiser, J., Wasmund, N., Savchuk, O. (2020). Cyanobacterial blooms in the Baltic Sea: Correlations with environmental factors. Harmful Algae, 92, 101739. https://doi.org/10.1016/j.hal.2019.101739

Kakisawa, H., Asari, F., Kusumi, T., Toma, T., Sakurai, T., Oohusa, T., Hara, Y., Chiharai, M. (1988). An allelopathic fatty acid from the brown alga Cladosiphon okamuranus. Phytochemistry, 27, 731–735. https://doi.org/10.1016/0031-9422(88)84084-6

Latała, A., Jodłowska, S., Pniewski, F. (2006). Culture Collection of Baltic Algae (CCBA) and characteristic of some strains by factorial experiment approach. Algological Studies/Archiv für Hydrobiologie, 122, 137–154. http://dx.doi.org/10.1127/1864-1318/2006/0122-0137

Lewis Jr, W.M., (1986). Evolutionary interpretations of allelochemical interactions in phytoplankton algae. The American Naturalist, 127, 184–194.

Maehnert, B., Schagerl, M., Krenn, L. (2017). Allelopathic potential of stoneworts. Fottea, Olomouc, 17(2), 137–149. http://dx.doi.org/10.5507/fot.2016.024

Molisch, H. (1937). Der Einfluss einer Pflanze auf die andere, Allelopathie (The influence of one plant on the other, allelopathy). Jena: Gustav Fischer. https://doi.org/10.1038/141493a0

Mulderij, G., Van Donk, E., Roelofs, J.G.M. (2003). Differential sensitivity of green algae to allelopathic substances from Chara. Hydrobiologia, 491(1–3), 261–271. https://doi.org/10.1023/A:1024483704903

Nan, C., Zhang, H., Zhao, G. (2004). Allelopathic interactions between the macroalga Ulva pertusa and eight microalgal species. Journal of Sea Research, 52(4), 259–268. https://doi.org/10.1016/j.seares.2004.04.001

Neori, A., Chopin, T., Troell, M., Buschmann, A. H., Kraemer, G. P., Halling, C., Shpigel, M., Yarish, C. (2004). Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture, 231(1–4), 361–391. https://doi.org/10.1016/j.aquaculture.2003.11.015

Pakdel, F.M., Sim, L., Beardall, J., Davis, J. (2013). Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany, 110, 24–30. https://doi.org/10.1016/j.aquabot.2013.04.005

Reichwaldt, E.S., Ghadouani, A. (2012). Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: between simplistic scenarios and complex dynamics. Water Research, 46(5), 1372–1393. https://doi.org/10.1016/j.watres.2011.11.052

Rybak, A.S. (2018). The Ulva flexuosa complex (Ulvaceae, Chlorophyta): An updated identification key with special reference to the freshwater and hyperhaline taxa. Phytotaxa, 345(2), 83–103.

Schreiber, U., Endo, T., Mi, H., Asada, K. (1995). Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant and Cell Physiology, 36, 873–882.

Škaloud, P., Rindi, F., Boedeker, C., Leliaert, F. (2018). Freshwater Flora of Central Europe, Vol 13: Chlorophyta: Ulvophyceae (Süßwasserflora von Mitteleuropa, Bd. 13: Chlorophyta: Ulvophyceae). Springer Berlin Heidelberg, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-55495-1

Song, H., Lavoie, M., Fan, X., Tan, H., Liu, G., Xu, P., Fu, Z., Paerl, H.W., Qian, H. (2017). Allelopathic interactions of linoleic acid and nitric oxide increase the competitive ability of Microcystis aeruginosa. The ISME Journal, 11, 1865–1876. https://doi.org/10.1038/ismej.2017.45

Starmach, K., 1972. Filamentous green algae. Freshwater flora of Poland, PWN, Warszawa-Kraków, 163 pp.

Stebbing, A.R.D. (1982). Hormesis – the stimulation of growth by low levels of inhibitors. Science of the Total Environment, 22, 213–234. https://doi.org/10.1016/0048-9697(82)90066-3

Surakka, A., Sihvonen, L.M., Lehtimäki, J.M., Wahlsten, M., Vuorela, P., Sivonen, K. (2005). Benthic cyanobacteria from the Baltic Sea contain cytotoxic Anabaena, Nodularia, and Nostoc strains and an apoptosis‐inducing Phormidium strain. Environmental Toxicology: An International Journal, 20(3), 285–292. https://doi.org/10.1002/tox.20119

Svirski, E., Beer, S., Friedlander, M. (1993). Gracilaria conferta and its epiphytes:(2) Interrelationship between the red seaweed and Ulva cf. lactuca. Hydrobiologia, 260(1), 391–396. https://doi.org/10.1007/BF00049046

Śliwińska-Wilczewska, S., Wiśniewska, K., Konarzewska, Z., Cieszyńska, A., Felpeto, A., Lewandowska, A.U., Latała, A. (2021). The current state of knowledge on taxonomy, modulating factors, ecological roles, and mode of action of phytoplankton allelochemicals. Science of the Total Environment, 773, 145681. https://doi.org/10.1016/j.scitotenv.2021.145681

Tait, L.W., Schiel, D.R. (2011). Dynamics of productivity in naturally structured macroalgal assemblages: importance of canopy structure on light-use efficiency. Marine Ecology Progress Series, 421, 97–107.

Tang, Y.Z., Gobler, C.J. (2011). The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae, 10(5), 480–488. https://doi.org/10.1016/j.hal.2011.03.003

Uchida, M., Aoyama, Y., Eda, N., Ohta, A. (1995). Investigation of the microstructure in the catalyst layer and effects of both perfluorosulfonate ionomer and PTFE‐loaded carbon on the catalyst layer of polymer electrolyte fuel cells. Journal of the Electrochemical Society, 142(12), 4143. https://doi.org/10.1149/1.2048477

Valiela, I., McClelland, J., Hauxwell, J., Behr, P.J., Hersh, D., Foreman, K. (1997). Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography, 42(5part2), 1105–1118. https://doi.org/10.4319/lo.1997.42.5_part_2.1105

Van Donk, E., van de Bund, W.J. (2002). Impact of submerged macrophytes including charophytes on phyto-and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany, 72(3–4), 261–274. https://doi.org/10.1016/S0304-3770(01)00205-4

Wang, R., Xiao, H., Zhang, P., Qu, L., Cai, H., Tang, X. (2007). Allelopathic effects of Ulva pertusa, Corallina pilulifera and Sargassum thunbergii on the growth of the dinoflagellates Heterosigma akashiwo and Alexandrium tamarense. Journal of Applied Phycology, 19, 109–121. https://dx.doi.org/10.1007%2Fs10811-006-9117-8

Wasmund, N. (1997). Occurrence of cyanobacterial blooms in the Baltic Sea in relation to environmental conditions. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 82(2), 169–184. https://doi.org/10.1002/iroh.19970820205

White, L. F., Shurin, J. B. (2011). Density dependent effects of an exotic marine macroalga on native community diversity. Journal of Experimental Marine Biology and Ecology, 405(1–2), 111–119. http://dx.doi.org/10.1016/j.jembe.2011.05.024

Xu, D., Gao, Z., Zhang, X., Fan, X., Wang, Y., Li, D., Wei, W., Zhimeng, Z., Ye, N. (2012). Allelopathic interactions between the opportunistic species Ulva prolifera and the native macroalga Gracilaria lichvoides. Plos One, 7(4). https://doi.org/10.1371/journal.pone.0033648

Zertuche-González, J.A., Camacho-Ibar, V.F., Pacheco-Ruíz, I., Cabello-Pasini, A., Galindo-Bect, L.A., Guzmán-Calderón, J.M., Carranza-Macias, V., Espinoza-Avalos, J. (2009). The role of Ulva spp. as a temporary nutrient sink in a coastal lagoon with oyster cultivation and upwelling influence. Journal of Applied Phycology, 21(6), 729. https://doi.org/10.1007/s10811-009-9408-y

Zillén, L., Conley, D.J. (2010). Hypoxia and cyanobacterial blooms are not natural features of the Baltic Sea. Biogeosciences Discussions, 7(2), 1783–1812. http://dx.doi.org/10.5194/bgd-7-1783-2010

Złoch, I., Śliwińska-Wilczewska, S., Kucharska, M., Kozłowska, W. (2018). Allelopathic effects of Chara species (C. aspera, C. baltica, and C. canescens) on the bloom-forming picocyanobacterium Synechococcus sp. Environmental Science and Pollution Research, 25, 36403–36411. https://doi.org/10.1007/s11356-018-3579-5

Downloads

Published

2022-03-25

How to Cite

Budzałek, G., & Śliwińska-Wilczewska, S. (2022). Allelopathic effect of Ulva intestinalis thallus on selected Baltic cyanobacteria. Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 7, 111–126. https://doi.org/10.24917/25438832.7.7

Issue

Section

Experimental Biology

Most read articles by the same author(s)