Accessible Requires Authentication Published by De Gruyter April 30, 2021

Effect of temperature and salinity on the growth and cell size of the first cultures of Gymnodinium aureolum from the Black Sea

Manuel Sala-Pérez, Anne E. Lockyer, Alexandre Anesio and Suzanne A. G. Leroy
From the journal Botanica Marina

Abstract

Algal blooms are natural phenomena that may cause human health problems, millions of dollars in losses and ecological disasters worldwide. Anthropogenic pressures like eutrophication may increase the frequency and intensity of these phenomena. The Black Sea is characterized by rapid changes in salinity and temperature in surface waters. In addition, it has suffered increasing environmental pressure from human activities. This work presents the first cultures of Gymnodinium aureolum to be isolated from the Black Sea. Morphological and phylogenetic analyses confirmed our strain as G. aureolum. The effects of temperature and salinity on growth were tested in experiments combining two temperatures and five salinities in 10 experimental treatments. This provides baseline data on the physiological adaption and acclimatization potential of the species to bloom under present and future climatic scenarios in the Black Sea. Gymnodinium aureolum grew exponentially in all experimental treatments, except for cultures at salinity 5. Growth rate increased significantly with increasing temperature reaching the maximum at 20 °C and salinity 15 (0.38 ± 0.02 d−1). This suggests an adaptation to the salinity and temperature of Black Sea waters and, together with previous records of G. aureolum in both water and sediments, supports the idea that this may be a bloom-forming population of G. aureolum.


Corresponding author: Manuel Sala-Pérez, School of Geographical Sciences and Cabot Institute, University of Bristol, Bristol, UK; and Baltic Marine Environment Protection Commission, Katajanokanlaituri 6 B, 00160Helsinki, Finland, E-mail:

Funding source: H2020 Marie Skłodowska-Curie Actions

Award Identifier / Grant number: 642973

Funding source: Wolfson College, University of Oxford

Acknowledgements

We would like to thank Dr. Silviu Radan and Dr. Ana Bianca Pavel from the GeoEcoMar team for helping with the organization and sampling collection during the fieldwork in the Black Sea. We thank Dr. Stuart Bellamy, Dr. Simon Cobb, Dr. Fotis Sgouridis and Dr. James Williams from the University of Bristol for their technical assistance during the lab culture work. The authors gratefully acknowledge the Wolfson Bioimaging Facility for their support and assistance in this work, especially to Judith Mantell, Chris Neal and Sally Hobson.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: The authors would like to thank the European Union’s Horizon 2020 research and innovation programme and the Innovative Training Network 2015–2019 Drivers of Pontocaspian Biodiversity Rise and Demise (PRIDE) under the Marie Sklodowska–Curie Grant Agreement No. 642973 for funding and supporting this research.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Aissaoui, A., Turki, S., and Ben Hassine, O.K. (2012). Occurence of harmful dinoflagellates in the punic harbors of Carthage (Gulf of Tunis) and their correlations with the physicochemical parameters. Bull. Inst. Nat. Sci. Tech. Merde Salammbô 39: 127–140. Search in Google Scholar

Anderson, D.M. (2009). Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag. 52: 342–347, https://doi.org/10.1016/j.ocecoaman.2009.04.006. Search in Google Scholar

Anderson, D.M., Cembella, A.D., and Hallegraeff, G.M. (2012). Progress in understanding harmful algal blooms (HABs): paradigm shifts and new technologies for research, monitoring and management. Ann. Rev. Mar. Sci. 4: 143–176, https://doi.org/10.1146/annurev-marine-120308-081121.Progress. Search in Google Scholar

Bachvaroff, T.R., Adolf, J.E., and Place, A.R. (2009). Strain variation in Karlodinium veneficum (dinophyceae): toxin profiles, pigments, and growth characteristics. J. Phycol. 45: 137–153, https://doi.org/10.1111/j.1529-8817.2008.00629.x. Search in Google Scholar

Bakan, G., and Buyukgungor, H. (2000). The Black Sea. Mar. Pollut. Bull. 41: 24–43, https://doi.org/10.1016/S0025-326X(00)00100-4. Search in Google Scholar

Boicenco, L. (2010). Spatio-temporal dynamics of phytoplankton composition and abundance from the Romanian Black Sea coast. Ovidius Univ. Ann. Nat. Sci. Biol.-Ecol. Ser. 14: 163–169. Search in Google Scholar

Botes, L., Price, B., Waldron, M., and Pitcher, G.C. (2002). A simple and rapid scanning electron microscope preparative technique for delicate “gymnodinioid” dinoflagellates. Microsc. Res. Tech. 59: 128–130, https://doi.org/10.1002/jemt.10184. Search in Google Scholar

Botes, L., Smit, A.J., and Cook, P.A. (2003). The potential threat of algal blooms to the abalone (Haliotis midae) mariculture industry situated around the South African coast. Harmful Algae 2: 247–259, https://doi.org/10.1016/s1568-9883(03)00044-1. Search in Google Scholar

Brand, L.E. (1981). Genetic variability in reproduction rates in marine phytoplankton populations. Evolution 35: 1117–1127, https://doi.org/10.1111/j.1558-5646.1981.tb04981.x. Search in Google Scholar

Caperon, J., and Meyer, J. (1972). Nitrogen-limited growth of marine phytoplankton changes in population characteristics with steady-state growth rate. Deep-Sea Res. Oceanogr. Abstr. 19: 601–618, https://doi.org/10.1016/0011-7471(72)90089-7. Search in Google Scholar

Chen, Y., Yan, T., Yu, R., and Zhou, M. (2011). Toxic effects of Karenia mikimotoi extracts on mammalian cells. Chin. J. Oceanol. Limnol. 29: 860–868, https://doi.org/10.1007/s00343-011-0514-8. Search in Google Scholar

Costas, E. (1990). Genetic variability in growth rates of marine dinoflagellates. Genetica 82: 99–102, https://doi.org/10.1007/BF00124638. Search in Google Scholar

Daugbjerg, N., Hansen, G., Larsen, J., and 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, https://doi.org/10.2216/i0031-8884-39-4-302.1. Search in Google Scholar

de Salas, M.F., Bolch, C.J.S., Botes, L., Nash, G., Wright, S.W., and Hallegraeff, G.M. (2003). Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J. Phycol. 39: 1233–1246, https://doi.org/10.1111/j.0022-3646.2003.03-019.x. Search in Google Scholar

de Salas, M.F., Rhodes, L.L., Mackenzie, L.A., and Adamson, J.E. (2005). Gymnodinoid genera Karenia and Takayama (Dinophyceae) in New Zealand coastal waters. N. Z. J. Mar. Freshw. Res. 39: 135–139, https://doi.org/10.1080/00288330.2005.9517296. Search in Google Scholar

Dzhembekova, N., Moncheva, S., Ivanova, P., Slabakova, N., and Nagai, S. (2018). Biodiversity of phytoplankton cyst assemblages in surface sediments of the Black Sea based on metabarcoding. Biotechnol. Biotechnol. Equip. 32: 1507–1513, https://doi.org/10.1080/13102818.2018.1532816. Search in Google Scholar

Edwards, K.F., Thomas, M.K., Klausmeier, C.A., and Litchman, E. (2012). Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol. Oceanogr. 57: 554–566, https://doi.org/10.4319/lo.2012.57.2.0554. Search in Google Scholar

Eker-Develi, E., Berthon, J.F., Canuti, E., Slabakova, N., Moncheva, S., Shtereva, G., and Dzhurova, B. (2012). Phytoplankton taxonomy based on CHEMTAX and microscopy in the northwestern Black Sea. J. Mar. Syst. 94: 18–32, https://doi.org/10.1016/j.jmarsys.2011.10.005. Search in Google Scholar

Fu, F. X., Tatters, A.O., and Hutchins, D.A. (2012). Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470: 207–233, https://doi.org/10.3354/meps10047. Search in Google Scholar

Glibert, P.M., Anderson, D.M., Gentien, P., Granéli, E., and Sellner, K.G. (2005). The global, complex phenomena of harmful algal blooms. Oceanography 18: 136–147, https://doi.org/10.5670/oceanog.2005.49. Search in Google Scholar

Gobler, C.J. (2020). Climate change and harmful algal blooms: insights and perspective. Harmful Algae 91: 101731, https://doi.org/10.1016/j.hal.2019.101731. Search in Google Scholar

Guillard, R.R.L. (1973). Division rates. In: Stein, J.R. (Ed.), Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, England, pp. 290–311. Search in Google Scholar

Haapala, O.K., and Soyer, M.O. (1974). Size of circular chromatids and amounts of haploid DNA in the dinoflagellates Gyrodinium cohnii and Prorocentrum micans. Hereditas 76: 83–90, https://doi.org/10.1111/j.1601-5223.1974.tb01179.x. Search in Google Scholar

Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98. Search in Google Scholar

Hallegraeff, G.M. (1993). A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79–99, https://doi.org/10.2216/i0031-8884-32-2-79.1. Search in Google Scholar

Hallegraeff, G.M. (2010). Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46: 220–235, https://doi.org/10.1111/j.1529-8817.2010.00815.x. Search in Google Scholar

Hällfors, G. (2004). Checklist of Baltic Sea phytoplankton species. Baltic Sea Environ. Proc. 95: 1–208 (Helsinki Commission, Baltic Marine Protection Commission). Search in Google Scholar

Hansen, G. (2001). Ultrastructure of Gymnodinium aureolum (dinophyceae): toward a further redefinition of Gymnodinium sensu stricto. J. Phycol. 37: 612–624, https://doi.org/10.1046/j.1529-8817.2001.037004612.x. Search in Google Scholar

Hansen, G., Daugbjerg, N., and Henriksen, P. (2000). Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (=Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. J. Phycol. 36: 394–410, https://doi.org/10.1046/j.1529-8817.2000.99172.x. Search in Google Scholar

Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M., Cochlan, W., Dennison, W.C., Dortch, Q., Gobler, C.J., Heil, C.A., and Humphries, E., et al.. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8: 3–13, https://doi.org/10.1016/j.hal.2008.08.006. Search in Google Scholar

Hulburt, E.M. (1957). The taxonomy of unarmored Dinophyceae of shallow embayments of Cape Cod, Massachusetts. Biol. Bull. 112: 196–219, https://doi.org/10.2307/1539198. Search in Google Scholar

Jeong, H.J., Du Yoo, Y., Kang, N.S., Rho, J.R., Seong, K.A., Park, J.W., Nam, G.S., and Yih, W. (2010). Ecology of Gymnodinium aureolum. I. Feeding in western Korean waters. Aquat. Microb. Ecol. 59: 239–255, https://doi.org/10.3354/ame01394. Search in Google Scholar

Juhl, A.R., Velazquez, V., and Latz, M.I. (2000). Effect of growth conditions on flow-induced inhibition of population growth of a red-tide dinoflagellate. Limnol. Oceanogr. 45: 905–915, https://doi.org/10.4319/lo.2000.45.4.0905. Search in Google Scholar

Kang, N.S., Lee, K.H., Jeong, H.J., Du Yoo, Y., Seong, K.A., Potvin, É., Hwang, Y.J., and Yoon, E.Y. (2013). Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30: S114–S130, https://doi.org/10.1016/j.hal.2013.10.011. Search in Google Scholar

Lakeman, M.B., von Dassow, P., and Cattolico, R.A. (2009). The strain concept in phytoplankton ecology. Harmful Algae 8: 746–758, https://doi.org/10.1016/j.hal.2008.11.011. Search in Google Scholar

Larsen, A., and Bryant, S. (1998). Growth rate and toxicity of Prymnesium parvum and Prymnesium patelliferum (Haptophyta) in response to changes in salinity, light and temperature. Sarsia 83: 409–418, https://doi.org/10.1080/00364827.1998.10413700. Search in Google Scholar

Lewis, J., Taylor, J.D., Neale, K., and Leroy, S.A.G. (2018). Expanding known dinoflagellate distributions: investigations of slurry cultures from Caspian Sea sediment. Bot. Mar. 61: 21–31, https://doi.org/10.1515/bot-2017-0041. Search in Google Scholar

Li, X., Yan, T., Yu, R., and Zhou, M. (2019). A review of Karenia mikimotoi: bloom events, physiology, toxicity and toxic mechanism. Harmful Algae 90: 101702, https://doi.org/10.1016/j.hal.2019.101702. Search in Google Scholar

Lilly, E.L., Halanych, K.M., and Anderson, D.M. (2007). Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol. 43: 1329–1338, https://doi.org/10.1111/j.1529-8817.2007.00420.x. Search in Google Scholar

Mikaelyan, A.S., Pautova, L.A., Chasovnikov, V.K., Mosharov, S.A., and Silkin, V.A. (2015). Alternation of diatoms and coccolithophores in the north-eastern Black Sea: a response to nutrient changes. Hydrobiologia 755: 89–105, https://doi.org/10.1007/s10750-015-2219-z. Search in Google Scholar

Mitchell, S. and Rodger, H. (2007). Pathology of wild and cultured fish affected by a Karenia mikimotoi bloom in Ireland, 2005. Bull. Eur. Assoc. Fish Pathol. 27: 39–42. Search in Google Scholar

Morton, S.L., Vershinin, A., Smith, L.L., Leighfield, T.A., Pankov, S., and Quilliam, M.A. (2009). Seasonality of Dinophysis spp. and Prorocentrum lima in Black Sea phytoplankton and associated shellfish toxicity. Harmful Algae 8: 629–636, https://doi.org/10.1016/j.hal.2008.10.011. Search in Google Scholar

Nézan, E., Siano, R., Boulben, S., Six, C., Bilien, G., Chèze, K., Duval, A., Le Panse, S., Quéré, J., and Chomérat, N. (2014). Genetic diversity of the harmful family Kareniaceae (Gymnodiniales, Dinophyceae) in France, with the description of Karlodinium gentienii sp. nov.: a new potentially toxic dinoflagellate. Harmful Algae 40: 75–91, https://doi.org/10.1016/j.hal.2014.10.006. Search in Google Scholar

Paerl, H.W. (1997). Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnol. Oceanogr. 42: 1154–1165, https://doi.org/10.4319/lo.1997.42.5_part_2.1154. Search in Google Scholar

Peacock, M.B., and Kudela, R.M. (2014). Evidence for active vertical migration by two dinoflagellates experiencing iron, nitrogen, and phosphorus limitation. Limnol. Oceanogr. 59: 660–673, https://doi.org/10.4319/lo.2014.59.3.0660. Search in Google Scholar

Reñé, A., Camp, J., and Garcés, E. (2015). Diversity and phylogeny of Gymnodiniales (Dinophyceae) from the NW Mediterranean Sea revealed by a morphological and molecular approach. Protist 166: 234–263, https://doi.org/10.1016/j.protis.2015.03.001. Search in Google Scholar

Sala-Pérez, M., Alpermann, T.J., Krock, B., and Tillmann, U. (2016). Growth and bioactive secondary metabolites of arctic Protoceratium reticulatum (Dinophyceae). Harmful Algae 55: 85–96, https://doi.org/10.1016/j.hal.2016.02.004. Search in Google Scholar

Sathyendranath, S., Stuart, V., Nair, A., Oka, K., Nakane, T., Bouman, H., Forget, M.H., Maass, H., and Platt, T. (2009). Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea. Mar. Ecol. Prog. Ser. 383: 73–84, https://doi.org/10.3354/meps07998. Search in Google Scholar

Scholin, C.A., Herzog, M., Sogin, M., and Anderson, D.M. (1994). Identification of group and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30: 999–1011, https://doi.org/10.1111/j.0022-3646.1994.00999.x. Search in Google Scholar

Sellner, K.G., Doucette, G.J., and Kirkpatrick, G.J. (2003). Harmful algal blooms: causes, impacts and detection. J. Ind. Microbiol. Biotechnol. 30: 383–406, https://doi.org/10.1007/s10295-003-0074-9. Search in Google Scholar

Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., and Söding, J., et al.. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, https://doi.org/10.1038/msb.2011.75. Search in Google Scholar

Smayda, T.J. (1997). Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42: 1137–1153, https://doi.org/10.4319/lo.1997.42.5_part_2.1137. Search in Google Scholar

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313, https://doi.org/10.1093/bioinformatics/btu033. Search in Google Scholar

Stanev, E.V. (2005). Understanding Black Sea dynamics. Oceanography 18: 56–75, https://doi.org/10.5670/oceanog.2005.42. Search in Google Scholar

Tang, Y.Z., Egerton, T.A., Kong, L., and Marshall, H.G. (2008). Morphological variation and phylogenetic analysis of the dinoflagellate Gymnodinium aureolum from a tributary of Chesapeake Bay. J. Eukaryot. Microbiol. 55: 91–99, https://doi.org/10.1111/j.1550-7408.2008.00305.x. Search in Google Scholar

Tang, Y.Z., Kong, L., and Holmes, M.J. (2007). Dinoflagellate Alexandrium leei (Dinophyceae) from Singapore coastal waters produces a water-soluble ichthyotoxin. Mar. Biol. 150: 541–549, https://doi.org/10.1007/s00227-006-0396-z. Search in Google Scholar

Team, R.C. (2016). A language and environment for statistical computing, version 3.3.0. R Foundation for Statistical Computing, Vienna, Austria, Available at: https://www.R-project. org/ (Accessed October 2018). Search in Google Scholar

Terenko, L.M. (2005). New dinoflagellate (Dinoflagellata) species from the Odessa Bay of the Black Sea. Oceanol. Hydrobiol. Stud. 37(Suppl. 3): 205–216. Search in Google Scholar

Terenko, L.M. (2006). Species composition and distribution of Dinophyta in the Black Sea. Int. J. Algae 8: 345–364, https://doi.org/10.1615/InterJAlgae.v8.i4.50. Search in Google Scholar

Velikova, V., Cociasu, A., Popa, L., Boicenco, L., and Petrova, D. (2005). Phytoplankton community and hydrochemical characteristics of the Western Black Sea. Water Sci. Technol. 51: 9–18, https://doi.org/10.2166/wst.2005.0385. Search in Google Scholar

Wardiatno, Y., Damar, A., and Sumartono, B. (2004). A short review on the recent problem of red tide in Jakarta Bay: effect of red tide on fish and human. Jurnal Ilmu-ilmu Perairan dan Perikanan Indonesia 11: 67–71. Search in Google Scholar

Wells, M.L., Trainer, V.L., Smayda, T.J., Karlson, B.S., Trick, C.G., Kudela, R.M., Ishikawa, A., Bernard, S., Wulff, A., and Anderson, D.M., et al.. (2015). Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harmful Algae 49: 68–93, https://doi.org/10.1016/j.hal.2015.07.009. Search in Google Scholar

Yoo, Y., Du Jeong, H.J., Kang, N.S., Kim, J.S., Kim, T.H., and Yoon, E.Y. (2010). Ecology of Gymnodinium aureolum. II. Predation by common heterotrophic dinoflagellates and a ciliate. Aquat. Microb. Ecol. 59: 257–272, https://doi.org/10.3354/ame01401. Search in Google Scholar

Zaitsev, Y.P., Alexandrov, B.G., Berlinsky, N.A., and Zenetos, A. (2001). An introduction to Black Sea ecology. Odessa, Smil Editing & Publishing Agency Ltd. Search in Google Scholar

Zingone, A., Siano, R., D’Alelio, D., and Sarno, D. (2006). Potentially toxic and harmful microalgae from coastal waters of the Campania region (Tyrrhenian Sea, Mediterranean Sea). Harmful Algae 5: 321–337, https://doi.org/10.1016/j.hal.2005.09.002. Search in Google Scholar

Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0076).

Received: 2020-12-02
Accepted: 2021-04-13
Published Online: 2021-04-30
Published in Print: 2021-06-25

© 2021 Walter de Gruyter GmbH, Berlin/Boston