A snapshot of alien cyanobacteria found in northeastern European freshwaters - Lithuania case

Submitted: 20 March 2024
Accepted: 26 April 2024
Published: 14 May 2024
Abstract Views: 215
PDF: 82
HTML: 8
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

In recent years, cyanobacterial invasions have increased in European temperate lakes. Climate warming is highlighted as a key driver of the distribution and establishment of alien cyanobacteria, and water bodies in poor ecological status, characterized by meso-eutrophic conditions, are underlined as a suitable habitat for invasion. The establishment of newly arrived species is directly related to fluctuating physicochemical factors such as temperature, and nutrient concentrations, especially phosphorus and nitrogen, or biotic factors such as competition. Cyanobacterial invasions can have profound ecological impacts, such as displacing native species, causing the biodiversity loss of local communities, and modifying the ecosystem’s cyanotoxins profile. This study presents the occurrence of four alien bloom-forming potentially toxic cyanobacteria - Chrysosporum bergii, Cuspidothrix isstaschenkoi, Raphidiopsis raciborskii and Sphaerospermopsis aphanizomenoides - in the northern parts of their current range in temperate Europe and provides insights into their ecology. Special attention was paid to the lakes of Lithuania (Simnas, Jieznas and Gineitiškės), which is the northernmost location of distribution zone for some alien cyanobacteria and provides as a dispersion route to Norther Europe via the continental area. We i) described dynamics of indigenous cyanobacteria community invaded by alien cyanobacteria; ii) assessed concentrations of cyanotoxins in field and culture samples, and suggested toxin producers; and iii) detailed the correlation between the biomass of alien cyanobacteria and environmental conditions. These species were found in three human-affected shallow hyper-eutrophic lakes during warm period of the year; however, their biomass was low. We assume that present temperatures do not limit the occurrence of these alien species but are insufficient for their successful proliferation. In addition, we provided the first evidence of anatoxin-a production by isolated strains of C. issatschenkoi in Lithuania. Alien cyanobacteria were detected at an early stage of their development, however, a rise in global temperatures and the spread of strains with toxigenic potential could lead to increased proliferation and further northward expansion of these alien species.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Aguilera A, Gómez EB, Kaštovský J, Echenique RO, Salerno GL, 2018. The polyphasic analysis of two native Raphidiopsis isolates supports the unification of the genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 57:130-146. DOI: https://doi.org/10.2216/17-2.1
Antal O, Karisztl-Gácsi M, Farkas A, Kovács A, Ács A, Törő N, et al., 2011. Screening the toxic potential of Cylindrospermopsis raciborskii strains isolated from Lake Balaton, Hungary. Toxicon 57:831-840. DOI: https://doi.org/10.1016/j.toxicon.2011.02.007
Babanazarova O, Kurmayer R, Sidelev S, Aleksandrina E, Sakharova E, 2011. Phytoplankton structure and microcystine concentration in the highly eutrophic Nero Lake. Water Resour 38:229-236. DOI: https://doi.org/10.1134/S0097807811020023
Babanazarova O, Sidelev S, Fastner J, 2015. Northern expansion of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) observed in shallow highly eutrophic Lake Nero (Russia). Int J Algae 17:131-141. DOI: https://doi.org/10.1615/InterJAlgae.v17.i2.20
Ballot A, Fastner J, Lentz M, Wiedner C, 2010. First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in northeastern Germany. Toxicon 56:964-971. DOI: https://doi.org/10.1016/j.toxicon.2010.06.021
Bernard C, Ballot A, Thomazeau S, Maloufi S, Furey A, Mankiewicz-Boczek J, et al., 2017. Cyanobacteria associated with the production of cyanotoxins, p. 501-525. In: J. Meriluoto, L. Spoof and G.A. Codd (eds.), Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. Chichester, J. Wiley & Sons. DOI: https://doi.org/10.1002/9781119068761.app2
Buchberger F, Stockenreiter M, 2018. Unsuccessful invaders structure a natural freshwater phytoplankton community. Ecosphere 9:e02158. DOI: https://doi.org/10.1002/ecs2.2158
Budzyńska A, Gołdyn R, 2017. Domination of invasive Nostocales (Cyanoprokaryota) at 52°N latitude: Invasive Nostocales dominating at 52°N. Phycol Res 65:322-332. DOI: https://doi.org/10.1111/pre.12188
Budzyńska A, Rosińska J, Pełechata A, Toporowska M, Napiórkowska-Krzebietke A, Kozak A, et al., 2019. Environmental factors driving the occurrence of the invasive cyanobacterium Sphaerospermopsis aphanizomenoides (Nostocales) in temperate lakes. Sci Total Environ 650:1338-1347. DOI: https://doi.org/10.1016/j.scitotenv.2018.09.144
Gagnon A, Pick FR, 2012. Effect of nitrogen on cellular production and release of the neurotoxin anatoxin-a in a nitrogen-fixing cyanobacterium. Front Microbiol 3:211. DOI: https://doi.org/10.3389/fmicb.2012.00211
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T, 1999. Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403-424. DOI: https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Hodoki Y, Ohbayashi K, Kobayashi Y, Takasu H, Okuda N, Nakano S, 2013. Anatoxin-a-producing Raphidiopsis mediterranea Skuja var. Grandis Hill is one ecotype of non-heterocytous Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. in Japanese lakes. Harmful Algae 21-22:44-53. DOI: https://doi.org/10.1016/j.hal.2012.11.007
Karosienė J, Savadova-Ratkus K, Toruńska-Sitarz A, Koreiviene J, Kasperovičienė J, Vitonytė I, et al., 2020. First report of saxitoxins and anatoxin-a production by cyanobacteria from Lithuanian lakes. Eur J Phycol 55:1-12. DOI: https://doi.org/10.1080/09670262.2020.1734667
Kavaliauskienė J, 1996. [Algae of Lithuanian lakes].[Book in Lithuanian]. Vilnius, Institute of Geography.
Kaštovský J, Hauer T, Mareš J, Krautová M, Bešta T, Komárek J, et al., 2010. A review of the alien and expansive species of freshwater cyanobacteria and algae in the Czech Republic. Biol Invasions 12:3599-3625. DOI: https://doi.org/10.1007/s10530-010-9754-3
Kokociński M, Gągała I, Jasser I, Karosienė J, Kasperovičienė J, Kobos J, et al., 2017. Distribution of invasive Cylindrospermopsis raciborskii in the East-Central Europe is driven by climatic and local environmental variables. FEMS Microbiol Ecol 93:fix035. DOI: https://doi.org/10.1093/femsec/fix035
Kokociński M, Soininen J, 2012. Environmental factors related to the occurrence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range. Eur J Phycol 47:12-21. DOI: https://doi.org/10.1080/09670262.2011.645216
Komárek J, 2013. Cyanoprokaryota: 3rd Part: Heterocystous Genera. In: B. Büdel, G. Gärtner, L. Krienitz, and M. Schagerl (eds.), Süßwasserflora von Mitteleuropa. Berlin, Springer.
Koreivienė J, Kasperovičienė J, 2011. Alien cyanobacteria Anabaena bergii var. Limnetica Couté et Preisig from Lithuania: Some aspects of taxonomy, ecology and distribution. Limnologica 41:325-333. DOI: https://doi.org/10.1016/j.limno.2011.01.004
Lebret K, Kritzberg ES, Figueroa R, Rengefors K, 2012. Genetic diversity within and genetic differentiation between blooms of a microalgal species. Environ Microbiol 14:2395-2404. DOI: https://doi.org/10.1111/j.1462-2920.2012.02769.x
Ledreux A, Thomazeau S, Catherine A, Duval C, Yéprémian C, Marie A, Bernard C, 2010. Evidence for saxitoxins production by the cyanobacterium Aphanizomenon gracile in a French recreational water body. Harmful Algae 10:88-97. DOI: https://doi.org/10.1016/j.hal.2010.07.004
Mantzouki E, Campbell J, Wilk-Wozniak E, Krztoń W, Walusiak E, Pełechata A, et al., 2018. A European Multi Lake Survey dataset of environmental variables, phytoplankton pigments and cyanotoxins. Sci Data 5:180226.
Mehnert G, Leunert F, Cirés S, Jöhnk KD, Rücker J, Nixdorf B, Wiedner C, 2010. Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions. J Plankton Res 32:1009-1021. DOI: https://doi.org/10.1093/plankt/fbq033
Meriggi C, Drakare S, Polaina Lacambra E, Johnson RK, Laugen AT, 2022. Species distribution models as a tool for early detection of the invasive Raphidiopsis raciborskii in European lakes. Harmful Algae 113:102202. DOI: https://doi.org/10.1016/j.hal.2022.102202
Milardi M, Gavioli A, Soininen J, Castaldelli G, 2019. Exotic species invasions undermine regional functional diversity of freshwater fish. Sci Rep 9:17921. DOI: https://doi.org/10.1038/s41598-019-54210-1
Napiórkowska-Krzebietke A, Dunalska JA, Bogacka-Kapusta E, 2023. Ecological implications in a human-impacted lake-A case study of cyanobacterial blooms in a recreationally used water body. Int J Environ Res Public Health 20:5063. DOI: https://doi.org/10.3390/ijerph20065063
Nixdorf B, Mischke U, Rücker J, 2003. Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes - an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiologia 502:111-121. DOI: https://doi.org/10.1007/978-94-017-2666-5_10
Nunes A, Tricarico E, Panov V, Cardoso A, Katsanevakis S, 2015. Pathways and gateways of freshwater invasions in Europe. Aquat Invasions 10:359-370. DOI: https://doi.org/10.3391/ai.2015.10.4.01
Osswald J, Rellán S, Gago-Martinez A, Vasconcelos V, 2009. Production of anatoxin-a by cyanobacterial strains isolated from Portuguese fresh water systems. Ecotoxicology 18:1110-1115. DOI: https://doi.org/10.1007/s10646-009-0375-5
Pomati F, Kellmann R, Cavalieri R, Burns BP, Neilan BA, 2006. Comparative gene expression of PSP-toxin producing and non-toxic Anabaena circinalis strains. Environ Int 32:743-748. DOI: https://doi.org/10.1016/j.envint.2006.03.010
Poniedziałek B, Rzymski P, Kokociński M, Karczewski J, 2015. Toxic potencies of metabolite(s) of non-cylindrospermopsin producing Cylindrospermopsis raciborskii isolated from temperate zone in human white cells. Chemosphere 120:608-614. DOI: https://doi.org/10.1016/j.chemosphere.2014.09.067
Rajaniemi P, Hrouzek P, Kaštovská K, Willame R, Rantala A, Hoffmann L, et al., 2005. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 55:11-26. DOI: https://doi.org/10.1099/ijs.0.63276-0
Ricciardi A, Cohen J, 2007. The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309-315. DOI: https://doi.org/10.1007/s10530-006-9034-4
Sabour B, Loudiki M, Oudra B, Vasconcelos V, Oubraim S, Fawzi B, 2005. Dynamics and toxicity of Anabaena aphanizomenoides (Cyanobacteria) waterblooms in the shallow brackish Oued Mellah lake (Morocco). Aquat Ecosyst Health Manag 8:95-104. DOI: https://doi.org/10.1080/14634980590914944
Savadova K, Mazur-Marzec H, Karosienė J, Kasperovičienė J, Vitonytė I, Toruńska-Sitarz A, Koreivienė J, 2018. Effect of increased temperature on native and alien nuisance cyanobacteria from temperate lakes: an experimental approach. Toxins 10:445. DOI: https://doi.org/10.3390/toxins10110445
Savadova-Ratkus K, Mazur-Marzec H, Karosienė J, Kasperovičienė J, Paškauskas R, Vitonytė I, Koreivienė J, 2021. Interplay of nutrients, temperature, and competition of native and alien cyanobacteria species growth and cyanotoxin production in temperate lakes. Toxins 13:23. DOI: https://doi.org/10.3390/toxins13010023
Stefaniak K, Kokocinski M, 2005. Occurrence of invasive Cyanobacteria species in polimictic lakes of the Wielkopolska region (Western Poland). Oceanol Hydrobiol Stud 34:137-148.
Stoyneva-Gärtner M, Stefanova K, Uzunov B, Radkova M, Gärtner G, 2022. Cuspidothrix is the first genetically proved anatoxin a producer in Bulgarian lakes and reservoirs. Toxins 14:778. DOI: https://doi.org/10.3390/toxins14110778
Stüken A, Rücker J, Endrulat T, Preussel K, Hemm M, Nixdorf B, et al., 2006. Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696-703. DOI: https://doi.org/10.2216/05-58.1
Šuikaitė I, Vansevičiūtė G, Koreiviene J, 2023. An overview of the distribution and ecology of the alien cyanobacteria species Raphidiopsis raciborskii, Sphaerospermopsis aphanizomenoides and Chrysosporum bergii in Europe. Oceanol Hydrobiol Stud 52:312-332. DOI: https://doi.org/10.26881/oahs-2023.3.06
Sukenik A, Hadas O, Kaplan A, Quesada A, 2012. Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes – Physiological, regional, and global driving forces. Front Microbiol 3:86. DOI: https://doi.org/10.3389/fmicb.2012.00086
Sukenik A, Quesada A, Salmaso N, 2015. Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers Conserv 24:889-908. DOI: https://doi.org/10.1007/s10531-015-0905-9
Vezie C, Brient, Sivonen K, Bertru G, Lefeuvre JC, Salkinoja-Salonen M, 1998. Variation of microcystin content of cyanobacterial blooms and isolated strains in Lake Grand-Lieu (France). Microb Ecol 35:126-135. DOI: https://doi.org/10.1007/s002489900067
Vico P, Bonilla S, Cremella B, Aubriot L, Iriarte A, Piccini C, 2020. Biogeography of the cyanobacterium Raphidiopsis (Cylindrospermopsis) raciborskii: Integrating genomics, phylogenetic and toxicity data. Mol Phylogenet Evol 148:106824. DOI: https://doi.org/10.1016/j.ympev.2020.106824
Vollenweider RA, Kerekes J, 1982. Eutrophication of waters: monitoring, assessment and control. Report of the Cooperative Program on Eutrophication. OECD, Paris: 154 pp.
Weithoff G, Taube A, Bolius S, 2017. The invasion success of the cyanobacterium Cylindrospermopsis raciborskii in experimental mesocosms: genetic identity, grazing loss, competition and biotic resistance. Aquat Invasions 12:333-341. DOI: https://doi.org/10.3391/ai.2017.12.3.07
World Health Organization, 2021. Guidelines on recreational water quality. Volume 1: coastal and fresh waters. Available from: https://www.who.int/publications/i/item/9789240031302
Wilk-Woźniak E, Najberek K, 2013. Towards clarifying the presence of alien algae in inland waters - can we predict places of their occurrence? Biologia 68:838-844. DOI: https://doi.org/10.2478/s11756-013-0221-3
Zapomělová E, Skácelová O, Pumann P, Kopp R, Janeček E, 2012. Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. Nov.) and A. Tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. Nova). Hydrobiologia 698:353-365. DOI: https://doi.org/10.1007/s10750-012-1034-z

Edited by

Diego Fontaneto, National Research Council, Water Research Institute (CNR-IRSA), Verbania Pallanza, Italy

How to Cite

Šuikaitė, Izabelė, Jūratė Karosienė, and Judita Koreivienė. 2024. “A Snapshot of Alien Cyanobacteria Found in Northeastern European Freshwaters - Lithuania Case”. Journal of Limnology 83 (1). https://doi.org/10.4081/jlimnol.2024.2183.