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Effectively Safeguard Lake Balaton from Toxic Cyanobacterial Blooms?

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Effectively Safeguard Lake Balaton from Toxic Cyanobacterial Blooms? microorganisms Article Does the Kis-Balaton Water Protection System (KBWPS) Effectively Safeguard Lake Balaton from Toxic Cyanobacterial Blooms? Zoran Marinovi´c 1,2,*, Nada Tokodi 1,3 , Damjana Drobac Backovi´c 1, Ilija Š´ceki´c 2, Nevena Kitanovi´c 2 , Snežana B. Simi´c 4 , Nevena B. Ðordevi´c¯ 4 , Árpád Ferincz 5, Ádám Staszny 5, Tamara Duli´c 6, Jussi Meriluoto 1,6 ,Béla Urbányi 2, Jelena Luji´c 7,† and Zorica Svirˇcev 1,6,† 1 Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, 21000 Novi Sad, Serbia; [email protected] (N.T.); [email protected] (D.D.B.); Jussi.Meriluoto@abo.fi (J.M.); [email protected] (Z.S.) 2 Department of Aquaculture, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, 2100 Gödöll˝o,Hungary; [email protected] (I.Š.); [email protected] (N.K.); [email protected] (B.U.) 3 Laboratory of Metabolomics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, 30387 Krakow, Poland 4 Department of Biology and Ecology, Faculty of Science, University of Kragujevac, 34000 Kragujevac, Serbia; [email protected] (S.B.S.); [email protected] (N.B.Ð.) 5 Department of Freshwater Fish Ecology, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, 2100 Gödöll˝o,Hungary; [email protected] (Á.F.); [email protected] (Á.S.) Citation: Marinovi´c,Z.; Tokodi, N.; 6 Faculty of Science and Engineering, Biochemistry, Åbo Akademi University, 20520 Turku, Finland; Backovi´c,D.D.; Š´ceki´c,I.; Kitanovi´c, [email protected] N.; Simi´c,S.B.; Ðordevi´c,N.B.;¯ 7 Center for Reproductive Genomics, Department of Biomedical Sciences, Cornell University, Ithaca, Ferincz, Á.; Staszny, Á.; Duli´c,T.; et al. NY 14850, USA; [email protected] Does the Kis-Balaton Water * Correspondence: [email protected] Protection System (KBWPS) † Authors contributed equally to the manuscript. Effectively Safeguard Lake Balaton from Toxic Cyanobacterial Blooms?. Abstract: Lake Balaton is the largest shallow lake in Central Europe. Its water quality is affected by its Microorganisms 2021, 9, 960. biggest inflow, the Zala River. During late 20th century, a wetland area named the Kis-Balaton Water https://doi.org/10.3390/ Protection System (KBWPS) was constructed in the hopes that it would act as a filter zone and thus microorganisms9050960 ameliorate the water quality of Lake Balaton. The aim of the present study was to test whether the KBWPS effectively safeguards Lake Balaton against toxic cyanobacterial blooms. During April, May, Academic Editor: Assaf Sukenik July and September 2018, severe cyanobacterial blooming was observed in the KBWPS with numbers Received: 20 March 2021 reaching up to 13 million cells/mL at the peak of the bloom (July 2018). MC- and STX-coding genes Accepted: 26 April 2021 were detected in the cyanobacterial biomass. Five out of nine tested microcystin congeners were Published: 29 April 2021 detected at the peak of the bloom with the concentrations of MC-LR reaching 1.29 µg/L; however, accumulation of MCs was not detected in fish tissues. Histopathological analyses displayed severe Publisher’s Note: MDPI stays neutral hepatopancreas, kidney and gill alterations in fish obtained throughout the investigated period. In with regard to jurisdictional claims in Lake Balaton, on the other hand, cyanobacterial numbers were much lower; more than 400-fold fewer published maps and institutional affil- cells/mL were detected during June 2018 and cyanotoxins were not detected in the water. Hepatic, iations. kidney and gill tissue displayed few alterations and resembled the structure of control fish. We can conclude that the KBWPS acts as a significant buffering zone, thus protecting the water quality of Lake Balaton. However, as MC- and STX-coding genes in the cyanobacterial biomass were detected at both sites, regular monitoring of this valuable ecosystem for the presence of cyanobacteria and Copyright: © 2021 by the authors. cyanotoxins is of paramount importance. Licensee MDPI, Basel, Switzerland. This article is an open access article Keywords: cyanobacteria; cyanotoxins; microcystin; Hungary; histopathology distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Microorganisms 2021, 9, 960. https://doi.org/10.3390/microorganisms9050960 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 960 2 of 24 1. Introduction Lake Balaton is the largest Central European lake, located in Western Hungary [1,2]. With its large size, the lake has 51 inflows, with 20 of them being permanent [3]. The largest is the Zala River which accounts for approximately half of the water inflow. Due to this inflow capacity, and the fact that approximately 35–40% of the lake’s nutrient load originates from this river [2], it has a significant effect on the lake’s water quality. Zala enters the lake through a large wetland area named the Kis-Balaton Wetlands (KBW) which ‘filters’ sediments and nutrients which would otherwise enter the lake [1]. In the 18th and 19th century, this area was a large open water body surrounded by extensive wetland vegetation, including a wetland forest which concealed the Zala River flowing into Lake Balaton. This provided hydraulic resistance for Zala’s water and enabled eutrophication to occur before the water entered Balaton. However, the filtering capacity of the KBW was greatly compromised in the 19th and 20th century when the Sió Canal (the lake’s only outflow) was first widened to lower the water level of Lake Balaton in order to protect the newly built Budapest-Rijeka railway from flooding [2]. This caused a significant drainage of the KBW as well. KBW marshland was further drained by constructing large numbers of drainage canals in order to create additional agricultural land. With the KBW severely compromised, and with an increased utilization of phosphorus-rich artificial fertilizers in agricultural practice and increased sewage effluents from rapidly developing towns, as well as discharges from animal farms, an intense eutrophication of Lake Balaton started to occur in 1930s and 1940s [1,4]. The lake suffered its highest eutrophication in 1960s and 1970s when intensive cyanobacterial blooms started to occur [1,4]. At this time, it became evident that measures for alleviating this pressure on Balaton needed to be conducted, otherwise its developing economic potential as a tourist destination would be greatly threatened. In order to decrease cyanobacterial blooms and further deterioration of water quality, inflow of organic nutrients needed to be reduced [2]. As wetlands are known to retain nutrients through several physical, chemical and biological factors such as physical sedi- mentation, adsorption of nutrients by the sediment, enhanced denitrification and uptake of nutrients by macrophytes or algae [5], re-flooding of the KBW (which would once again act as a ‘filter’ for Balaton) was planned under the framework of the Kis-Balaton Water Protection System (KBWPS). Re-flooding was planned in two phases: the first step would be the flooding of the Lower Zala Valley, while the second would be the flooding of the Kis-Balaton Basin [1]. Phase 1 was conducted in 1985 by a five-step flooding interven- tion and creation of an open waterspace (Hídvégi Pond) with a water retention time of 30 days [2,4,6,7]. Phase 2 was initiated in 1992 when a part of the 57 km2 Fenéki Pond was flooded. Only 16 km2 were flooded (with hydraulic retention time of 90 days) and they represent a typical wetland covered with macrophytes, primarily reeds. After Phase 1, 60% of the suspended solids coming from Zala River were retained in the first ponds, while after Phase 2, an additional 75% of suspended solids coming from Hídvégi Pond was retained [4]. Cyanobacterial blooms characterized by an overgrowth of cyanobacteria have become a great global problem, and their occurrence is continuously increasing [8–10]. These events cause major problems for water quality, for example, blooms can cause oxygen depletion in the ecosystem, sometimes even leading to hypoxia which can have severe negative consequences for the organisms living in such ecosystems [11]; increased turbidity that can smother aquatic vegetation [8]; and they can even produce a distinct taste and odor which can interfere with the function and use of the reservoir affected. Cyanobacterial blooms can pose a serious threat to public health when associated with the production of toxic compounds known as cyanotoxins [9,10,12]. Cyanotoxins are very diverse in their chemical structure and functional properties; based on their structure, they can be cyclic peptides, alkaloids, lipopeptides, non-protein amino acids and lipoglycans, while based on their functional properties they can be hepatotoxins, neurotoxins, cytotoxins and dermatotoxins [13,14]. Due to the negative effects cyanobacteria and their toxins can have Microorganisms 2021, 9, 960 3 of 24 on the environment and public health, regular monitoring of ecosystems susceptible to blooming is of great importance. Lake Balaton has been extensively studied with respect to its nutrient status and cyanobacterial blooms since the 1960s [1,4,6,15]. However, the toxicity of these blooms and their effects on biota have not been considered to date. The aim of this study was to verify whether the KBWPS indeed acts as a ‘filter’ for Lake Balaton and ‘protects’ it from cyanobacterial blooms by: (1) assessing the overall water quality parameters for both ecosystems; (2) determining the qualitative and quantitative structure of the cyanobacterial communities; (3) testing for the presence of cyanotoxin-coding genes within the collected biomass; (4) analyzing the cyanotoxin presence in the water and cyanobacterial biomass; (5) assessing potential cyanotoxin accumulation in fish tissues; (6) determining possible cyanotoxin effects on fish tissues through histological analyses of various organs of fish from both the KBWPS and Lake Balaton.
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