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Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

by Evanthia Mantzouki 1,*, Miquel Lürling 2,3, Jutta Fastner 4, Lisette De Senerpont Domis 2,3, Elżbieta Wilk-Woźniak 5, Judita Koreivienė 6, Laura Seelen 2,3, Sven Teurlincx 3, Yvon Verstijnen 2, Wojciech Krztoń 5, Edward Walusiak 5, Jūratė Karosienė 6, Jūratė Kasperovičienė 6, Ksenija Savadova 6, Irma Vitonytė 6, Carmen Cillero-Castro 7, Agnieszka Budzyńska 8, Ryszard Goldyn 8, Anna Kozak 8, Joanna Rosińska 8, Elżbieta Szeląg-Wasielewska 8, Piotr Domek 8, Natalia Jakubowska-Krepska 8, Kinga Kwasizur 9, Beata Messyasz 9, Aleksandra Pełechata 9, Mariusz Pełechaty 9, Mikolaj Kokocinski 9, Ana García-Murcia 10, Monserrat Real 10, Elvira Romans 10, Jordi Noguero-Ribes 10, David Parreño Duque 10, Elísabeth Fernández-Morán 10, Nusret Karakaya 11, Kerstin Häggqvist 12, Nilsun Demir 13, Meryem Beklioğlu 14, Nur Filiz 14, Eti E. Levi 14, Uğur Iskin 14, Gizem Bezirci 14, Ülkü Nihan Tavşanoğlu 14, Koray Özhan 15, Spyros Gkelis 16, Manthos Panou 16, Özden Fakioglu 17, Christos Avagianos 18, Triantafyllos Kaloudis 18, Kemal Çelik 19, Mete Yilmaz 20, Rafael Marcé 21, Nuria Catalán 21,22, Andrea G. Bravo 22, Moritz Buck 22, William Colom-Montero 23, Kristiina Mustonen 23, Don Pierson 23, Yang Yang 23, Pedro M. Raposeiro 24, Vítor Gonçalves 24, Maria G. Antoniou 25, Nikoletta Tsiarta 25, Valerie McCarthy 26, Victor C. Perello 26, Tõnu Feldmann 27, Alo Laas 27, Kristel Panksep 27, Lea Tuvikene 27, Ilona Gagala 28, Joana Mankiewicz-Boczek 28, Meral Apaydın Yağcı 29, Şakir Çınar 29, Kadir Çapkın 29, Abdulkadir Yağcı 29, Mehmet Cesur 29, Fuat Bilgin 29, Cafer Bulut 29, Rahmi Uysal 29, Ulrike Obertegger 30, Adriano Boscaini 30, Giovanna Flaim 30, Nico Salmaso 30, Leonardo Cerasino 30, Jessica Richardson 31, Petra M. Visser 32, Jolanda M. H. Verspagen 32, Tünay Karan 33, Elif Neyran Soylu 34, Faruk Maraşlıoğlu 35, Agnieszka Napiórkowska-Krzebietke 36, Agnieszka Ochocka 37, Agnieszka Pasztaleniec 37, Ana M. Antão-Geraldes 38, Vitor Vasconcelos 39, João Morais 39, Micaela Vale 39, Latife Köker 40, Reyhan Akçaalan 40, Meriç Albay 40, Dubravka Špoljarić Maronić 41, Filip Stević 41, Tanja Žuna Pfeiffer 41, Jeremy Fonvielle 42, Dietmar Straile 43, Karl-Otto Rothhaupt 43, Lars-Anders Hansson 44, Pablo Urrutia-Cordero 22,44, Luděk Bláha 45, Rodan Geriš 46, Markéta Fránková 47, Mehmet Ali Turan Koçer 48, Mehmet Tahir Alp 49, Spela Remec-Rekar 50, Tina Elersek 51, Theodoros Triantis 52, Sevasti-Kiriaki Zervou 52, Anastasia Hiskia 52, Sigrid Haande 53, Birger Skjelbred 53, Beata Madrecka 54, Hana Nemova 55, Iveta Drastichova 55, Lucia Chomova 55, Christine Edwards 56, Tuğba Ongun Sevindik 57, Hatice Tunca 57, Burçin Önem 57, Boris Aleksovski 58, Svetislav Krstić 58, Itana Bokan Vucelić 59, Lidia Nawrocka 60, Pauliina Salmi 61, Danielle Machado-Vieira 62, Alinne Gurjão De Oliveira 62, Jordi Delgado-Martín 63, David García 63, Jose Luís Cereijo 63, Joan Gomà 64, Mari Carmen Trapote 64, Teresa Vegas-Vilarrúbia 64, Biel Obrador 64, Magdalena Grabowska 65, Maciej Karpowicz 65, Damian Chmura 66, Bárbara Úbeda 67, José Ángel Gálvez 67, Arda Özen 68, Kirsten Seestern Christoffersen 69, Trine Perlt Warming 69, Justyna Kobos 70, Hanna Mazur-Marzec 70, Carmen Pérez-Martínez 71, Eloísa Ramos-Rodríguez 71, Lauri Arvola 72, Pablo Alcaraz-Párraga 73, Magdalena Toporowska 74, Barbara Pawlik-Skowronska 74, Michał Niedźwiecki 74, Wojciech Pęczuła 74, Manel Leira 75, Armand Hernández 76, Enrique Moreno-Ostos 77, José María Blanco 77, Valeriano Rodríguez 77, Jorge Juan Montes-Pérez 77, Roberto L. Palomino 77, Estela Rodríguez-Pérez 77, Rafael Carballeira 78, Antonio Camacho 79, Antonio Picazo 79, Carlos Rochera 79, Anna C. Santamans 79, Carmen Ferriol 79, Susana Romo 80, Juan Miguel Soria 80, Julita Dunalska 81, Justyna Sieńska 81, Daniel Szymański 81, Marek Kruk 82, Iwona Kostrzewska-Szlakowska 83, Iwona Jasser 84, Petar Žutinić 85, Marija Gligora Udovič 85, Anđelka Plenković-Moraj 85, Magdalena Frąk 86, Agnieszka Bańkowska-Sobczak 87, Michał Wasilewicz 87, Korhan Özkan 88, Valentini Maliaka 2,89,90, Kersti Kangro 27,91, Hans-Peter Grossart 42,92, Hans W. Paerl 93, Cayelan C. Carey 94 and Bas W. Ibelings 1
1
Department F.-A. Forel for Environmental and Aquatic Sciences, University of Geneva, 1205 Geneva, Switzerland
2
Department of Environmental Sciences, Wageningen University & Research, 6700 Wageningen, The Netherlands
3
Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 6700 Wageningen, The Netherlands
4
German Environment Agency, Unit Drinking Water Resources and Water Treatment, Corrensplatz 1, 14195 Berlin, Germany
5
Institute of Nature Conservation, Polish Academy of Sciences, 31-120 Krakow, Poland
6
Institute of Botany, Nature Research Centre, Vilnius 08412, Lithuania
7
R&D Department Environmental Engineering, 3edata, 27004 Lugo, Spain
8
Department of Water Protection, Adam Mickiewicz University, 61614 Poznan, Poland
9
Department of Hydrobiology, Adam Mickiewicz University, 61614 Poznan, Poland
10
Department of Limnology and Water Quality, AECOM U.R.S, 08036 Barcelona, Spain
11
Department of Environmental Engineering, Abant Izzet Baysal University, 14280 Bolu, Turkey
12
Department of Science and Engineering, Åbo Akademi University, 20520 Åbo, Finland
13
Department of Fisheries and Aquaculture, Ankara University, 6100 Ankara, Turkey
14
Department of biology, Middle East Technical University, 6800 Ankara, Turkey
15
Institute of Marine Sciences, Department of Oceanography, Middle East Technical University, 06800 Ankara, Turkey
16
Department of Botany, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
17
Department of Basic Science, Ataturk University, 25240 Erzurum, Turkey
18
Water Quality Department, Athens Water Supply and Sewerage Company, 11146 Athens, Greece
19
Department of Biology, Balikesir University, 10145 Balikesir, Turkey
20
Department of Bioengineering, Bursa Technical University, 16310 Bursa, Turkey
21
Catalan Institute for Water Research (ICRA), 17003 Girona, Spain
22
Department of Ecology and Genetics, Limnology, Uppsala University, 75236 Uppsala, Sweden
23
Department of Ecology and Genetics, Erken Laboratory, Uppsala University, 76173 Norrtalje, Sweden
24
Research Center in Biodiversity and Genetic Resources (CIBIO-Azores), InBIO Associated Laboratory, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal
25
Department of Environmental Science and Technology, Cyprus University of Technology, 3036 Lemesos, Cyprus
26
Centre for Freshwater and Environmental Studies, Dundalk Institute of Technology, A91 K584 Dundalk, Ireland
27
Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, 51014 Tartu, Estonia
28
European Regional Centre for Ecohydrology of the Polish Academy of Sciences, 90364 Lodz, Poland
29
Republic of Turkey Ministry of Food Agriculture, Fisheries Research Institute, 32500 Eğirdir, Isparta, Turkey
30
Department of Sustainable Ecosystems and Bioresources, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy
31
Department of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK
32
Department of Freshwater and Marine Ecology, University of Amsterdam, 1090 GE Amsterdam, The Netherlands
33
Department of Molecular Biology and Genetics, Gaziosmanpasa University, 60250 Merkez, Turkey
34
Department of Biology, Giresun University, 28100 Giresun, Turkey
35
Department of Biology, Hitit University, 19040 Corum, Turkey
36
Department of Icthyology, Hydrobiology and Aquatic Ecology, Inland Fisheries Institute, 10719 Olsztyn, Poland
37
Department of Freshwater Protection, Institute of Environmental Protection- National Research Institute, 01-692 Warsaw, Poland
38
Centro de Investigação da Montanha, Instituto Politécnico de Bragança, Campus de Santa Apolónia, 5300-253 Bragança, Portugal
39
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR) and University of Porto, 4450-208 Matosinhos, Portugal
40
Department of Freshwater Resource and Management, Faculty of Aquatic Sciences, Istanbul University, 34134 Istanbul, Turkey
41
Department of Biology, Josip Juraj Strossmayer University of Osijek, 31000 Osijek, Croatia
42
Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, 16775 Stechlin, Germany
43
Department of Biology, Limnological Institute, University of Konstanz, 78464 Konstanz, Germany
44
Department of Biology, Lund University, 22362 Lund, Sweden
45
RECETOX, Faculty of Science, Masaryk University, 62500 Brno, Czech Republic
46
Department of Hydrobiology, Morava Board Authority, 60200 Brno, Czech Republic
47
Laboratory of Paleoecology, Institute of Botany, The Czech Academy of Sciences, 60200 Brno, Czech Republic
48
Department of Environment and Resource Management, Mediterranean Fisheries Research Production and Training Institute, 7090 Antalya, Turkey
49
Faculty of Aquaculture, Mersin University, 33160 Mersin, Turkey
50
Department of Water Quality, Slovenian Environmental Agency, 1000 Ljubljana, Slovenia
51
Department of Genetic Toxicology and Cancer Biology, National Institute of Biology, 1000 Ljubljana, Slovenia
52
Institute of Nanoscience and Nanotechnology, National Center for Scientific Research «DEMOKRITOS», 15341 Attiki, Greece
53
Department of Freshwater Ecology, Norwegian Institute for Water Research, 0349 Oslo, Norway
54
Institute of Environmental Engineering, Poznan University of Technology, 60965 Poznan, Poland
55
National Reference Center for Hydrobiology, Public Health Authority of the Slovak Republic, 82645 Bratislava, Slovakia
56
School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen AB10 7GJ, UK
57
Department of Biology, Sakarya University, 54187 Sakarya, Turkey
58
Faculty of Natural Sciences and Mathematics, SS Cyril and Methodius University, 1000 Skopje, Macedonia
59
Department for Ecotoxicology, Teaching Institute of Public Health of Primorje-Gorski Kotar County, 51000 Rijeka, Croatia
60
Institute of Technology, The State University of Applied Sciences, 82300 Elblag, Poland
61
Department of Biological and Environmental Science, University of Jyväskylä, 40014 Jyväskylä, Finland
62
Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, 58059-970 Paraíba, Brasil
63
Department of Civil Engineering, University of A Coruña, 15192 A Coruña, Spain
64
Department of Evolutionary Biology, Ecology, and Environmental Sciences, University of Barcelona, 08028 Barcelona, Spain
65
Department of Hydrobiology, University of Bialystok, 15245 Bialystok, Poland
66
Institute of Environmental Protection and Engineering, University of Bielsko-Biala, 43309 Bielsko-Biala, Poland
67
Department of Biology, University of Cádiz, 11510 Puerto Real, Cádiz, Spain
68
Department of Forest Engineering, University of Cankiri Karatekin, 18200 Cankiri, Turkey
69
Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark
70
Department of Marine Biotechnology, University of Gdansk, 81378 Gdynia, Poland
71
Department of Ecology, University of Granada, 18071 Granada, Spain
72
Lammi Biological Station, University of Helsinki, 16900 Lammi, Finland
73
Department of Animal Biology, Plant Biology and Ecology, University of Jaen, 23701 Jaen, Spain
74
Department of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, 20262 Lublin, Poland
75
Instituto Dom Luiz, University of Lisbon, 1749016 Lisbon, Portugal
76
Institute of Earth Sciences Jaume Almera, ICTJA, CSIC, 08028 Barcelona, Spain
77
Department of Ecology, University of Malaga, 29071 Malaga, Spain
78
Centro de Investigacións Cientificas Avanzadas (CICA), Facultade de Ciencias, Universidade da Coruña, 15071 A Coruña, Spain
79
Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, 46980 Paterna Valencia, Spain
80
Department of Microbiology and Ecology, University of Valencia, 46100 Burjassot, Spain
81
Department of Water Protection Engineering, University of Warmia and Mazury, 10-720 Olsztyn, Poland
82
Department of Tourism, Recreation and Ecology, University of Warmia and Mazury, 10-720 Olsztyn, Poland
83
Faculty of Biology, University of Warsaw, 02-096 Warsaw, Poland
84
Department of Plant Ecology and Environmental Conservation, Faculty of Biology, University of Warsaw, 02-089 Warsaw, Poland
85
Department of Biology, Faculty of Science, University of Zagreb, 10000 Zagreb, Croatia
86
Department of Environmental Improvement, Faculty of Civil and Environmental Engineering, Warsaw University of Life Sciences—SGGW, 02-787 Warsaw, Poland
87
Department of Hydraulic Engineering, Faculty of Civil and Environmental Engineering, Warsaw University of Life Sciences—SGGW, 02-787 Warsaw, Poland
88
Institute of Marine Sciences, Marine Biology and Fisheries, Middle East Technical University, 06800 Ankara, Turkey
89
Society for the Protection of Prespa, 53077 Agios Germanos, Greece
90
Institute for Water and Wetland Research, Department of Aquatic Ecology and Environmental Biology, Radboud University Nijmegen, 6525 AJ Nijmegen, The Netherlands
91
Tartu Observatory, Faculty of Science and Technology, University of Tartu, 61602 Tartu, Estonia
92
Institute of Biochemistry and Biology, Potsdam University, 14469 Potsdam, Germany
93
Institute of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 28557, USA
94
Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA
*
Author to whom correspondence should be addressed.
Toxins 2018, 10(4), 156; https://doi.org/10.3390/toxins10040156
Received: 15 February 2018 / Revised: 27 March 2018 / Accepted: 29 March 2018 / Published: 13 April 2018
Insight into how environmental change determines the production and distribution of cyanobacterial toxins is necessary for risk assessment. Management guidelines currently focus on hepatotoxins (microcystins). Increasing attention is given to other classes, such as neurotoxins (e.g., anatoxin-a) and cytotoxins (e.g., cylindrospermopsin) due to their potency. Most studies examine the relationship between individual toxin variants and environmental factors, such as nutrients, temperature and light. In summer 2015, we collected samples across Europe to investigate the effect of nutrient and temperature gradients on the variability of toxin production at a continental scale. Direct and indirect effects of temperature were the main drivers of the spatial distribution in the toxins produced by the cyanobacterial community, the toxin concentrations and toxin quota. Generalized linear models showed that a Toxin Diversity Index (TDI) increased with latitude, while it decreased with water stability. Increases in TDI were explained through a significant increase in toxin variants such as MC-YR, anatoxin and cylindrospermopsin, accompanied by a decreasing presence of MC-LR. While global warming continues, the direct and indirect effects of increased lake temperatures will drive changes in the distribution of cyanobacterial toxins in Europe, potentially promoting selection of a few highly toxic species or strains. View Full-Text
Keywords: microcystin; anatoxin; cylindrospermopsin; temperature; direct effects; indirect effects; spatial distribution; European Multi Lake Survey microcystin; anatoxin; cylindrospermopsin; temperature; direct effects; indirect effects; spatial distribution; European Multi Lake Survey
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Mantzouki, E.; Lürling, M.; Fastner, J.; De Senerpont Domis, L.; Wilk-Woźniak, E.; Koreivienė, J.; Seelen, L.; Teurlincx, S.; Verstijnen, Y.; Krztoń, W.; Walusiak, E.; Karosienė, J.; Kasperovičienė, J.; Savadova, K.; Vitonytė, I.; Cillero-Castro, C.; Budzyńska, A.; Goldyn, R.; Kozak, A.; Rosińska, J.; Szeląg-Wasielewska, E.; Domek, P.; Jakubowska-Krepska, N.; Kwasizur, K.; Messyasz, B.; Pełechata, A.; Pełechaty, M.; Kokocinski, M.; García-Murcia, A.; Real, M.; Romans, E.; Noguero-Ribes, J.; Duque, D.P.; Fernández-Morán, E.; Karakaya, N.; Häggqvist, K.; Demir, N.; Beklioğlu, M.; Filiz, N.; Levi, E.E.; Iskin, U.; Bezirci, G.; Tavşanoğlu, Ü.N.; Özhan, K.; Gkelis, S.; Panou, M.; Fakioglu, Ö.; Avagianos, C.; Kaloudis, T.; Çelik, K.; Yilmaz, M.; Marcé, R.; Catalán, N.; Bravo, A.G.; Buck, M.; Colom-Montero, W.; Mustonen, K.; Pierson, D.; Yang, Y.; Raposeiro, P.M.; Gonçalves, V.; Antoniou, M.G.; Tsiarta, N.; McCarthy, V.; Perello, V.C.; Feldmann, T.; Laas, A.; Panksep, K.; Tuvikene, L.; Gagala, I.; Mankiewicz-Boczek, J.; Yağcı, M.A.; Çınar, Ş.; Çapkın, K.; Yağcı, A.; Cesur, M.; Bilgin, F.; Bulut, C.; Uysal, R.; Obertegger, U.; Boscaini, A.; Flaim, G.; Salmaso, N.; Cerasino, L.; Richardson, J.; Visser, P.M.; Verspagen, J.M.H.; Karan, T.; Soylu, E.N.; Maraşlıoğlu, F.; Napiórkowska-Krzebietke, A.; Ochocka, A.; Pasztaleniec, A.; Antão-Geraldes, A.M.; Vasconcelos, V.; Morais, J.; Vale, M.; Köker, L.; Akçaalan, R.; Albay, M.; Špoljarić Maronić, D.; Stević, F.; Žuna Pfeiffer, T.; Fonvielle, J.; Straile, D.; Rothhaupt, K.-O.; Hansson, L.-A.; Urrutia-Cordero, P.; Bláha, L.; Geriš, R.; Fránková, M.; Koçer, M.A.T.; Alp, M.T.; Remec-Rekar, S.; Elersek, T.; Triantis, T.; Zervou, S.-K.; Hiskia, A.; Haande, S.; Skjelbred, B.; Madrecka, B.; Nemova, H.; Drastichova, I.; Chomova, L.; Edwards, C.; Sevindik, T.O.; Tunca, H.; Önem, B.; Aleksovski, B.; Krstić, S.; Vucelić, I.B.; Nawrocka, L.; Salmi, P.; Machado-Vieira, D.; De Oliveira, A.G.; Delgado-Martín, J.; García, D.; Cereijo, J.L.; Gomà, J.; Trapote, M.C.; Vegas-Vilarrúbia, T.; Obrador, B.; Grabowska, M.; Karpowicz, M.; Chmura, D.; Úbeda, B.; Gálvez, J.Á.; Özen, A.; Christoffersen, K.S.; Warming, T.P.; Kobos, J.; Mazur-Marzec, H.; Pérez-Martínez, C.; Ramos-Rodríguez, E.; Arvola, L.; Alcaraz-Párraga, P.; Toporowska, M.; Pawlik-Skowronska, B.; Niedźwiecki, M.; Pęczuła, W.; Leira, M.; Hernández, A.; Moreno-Ostos, E.; Blanco, J.M.; Rodríguez, V.; Montes-Pérez, J.J.; Palomino, R.L.; Rodríguez-Pérez, E.; Carballeira, R.; Camacho, A.; Picazo, A.; Rochera, C.; Santamans, A.C.; Ferriol, C.; Romo, S.; Soria, J.M.; Dunalska, J.; Sieńska, J.; Szymański, D.; Kruk, M.; Kostrzewska-Szlakowska, I.; Jasser, I.; Žutinić, P.; Gligora Udovič, M.; Plenković-Moraj, A.; Frąk, M.; Bańkowska-Sobczak, A.; Wasilewicz, M.; Özkan, K.; Maliaka, V.; Kangro, K.; Grossart, H.-P.; Paerl, H.W.; Carey, C.C.; Ibelings, B.W. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins. Toxins 2018, 10, 156.

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