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. 2018 Apr 13;10(4):156.
doi: 10.3390/toxins10040156.

Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

Evanthia Mantzouki  1 , Miquel Lürling  2   3 , Jutta Fastner  4 , Lisette de Senerpont Domis  5   6 , Elżbieta Wilk-Woźniak  7 , Judita Koreivienė  8 , Laura Seelen  9   10 , Sven Teurlincx  11 , Yvon Verstijnen  12 , Wojciech Krztoń  13 , Edward Walusiak  14 , Jūratė Karosienė  15 , Jūratė Kasperovičienė  16 , Ksenija Savadova  17 , Irma Vitonytė  18 , Carmen Cillero-Castro  19 , Agnieszka Budzyńska  20 , Ryszard Goldyn  21 , Anna Kozak  22 , Joanna Rosińska  23 , Elżbieta Szeląg-Wasielewska  24 , Piotr Domek  25 , Natalia Jakubowska-Krepska  26 , Kinga Kwasizur  27 , Beata Messyasz  28 , Aleksandra Pełechaty  29 , Mariusz Pełechaty  30 , Mikolaj Kokocinski  31 , Ana García-Murcia  32 , Monserrat Real  33 , Elvira Romans  34 , Jordi Noguero-Ribes  35 , David Parreño Duque  36 , Elísabeth Fernández-Morán  37 , Nusret Karakaya  38 , Kerstin Häggqvist  39 , Nilsun Demir  40 , Meryem Beklioğlu  41 , Nur Filiz  42 , Eti E. Levi  43 , Uğur Iskin  44 , Gizem Bezirci  45 , Ülkü Nihan Tavşanoğlu  46 , Koray Özhan  47 , Spyros Gkelis  48 , Manthos Panou  49 , Özden Fakioglu  50 , Christos Avagianos  51 , Triantafyllos Kaloudis  52 , Kemal Çelik  53 , Mete Yilmaz  54 , Rafael Marcé  55 , Nuria Catalán  56   57 , Andrea G. Bravo  58 , Moritz Buck  59 , William Colom-Montero  60 , Kristiina Mustonen  61 , Don Pierson  62 , Yang Yang  63 , Pedro M. Raposeiro  64 , Vítor Gonçalves  65 , Maria G. Antoniou  66 , Nikoletta Tsiarta  67 , Valerie McCarthy  68 , Victor C. Perello  69 , Tõnu Feldmann  70 , Alo Laas  71 , Kristel Panksep  72 , Lea Tuvikene  73 , Ilona Gagala  74 , Joana Mankiewicz-Boczek  75 , Meral Apaydın Yağcı  76 , Şakir Çınar  77 , Kadir Çapkın  78 , Abdulkadir Yağcı  79 , Mehmet Cesur  80 , Fuat Bilgin  81 , Cafer Bulut  82 , Rahmi Uysal  83 , Ulrike Obertegger  84 , Adriano Boscaini  85 , Giovanna Flaim  86 , Nico Salmaso  87 , Leonardo Cerasino  88 , Jessica Richardson  89 , Petra M. Visser  90 , Jolanda M. H. Verspagen  91 , Tünay Karan  92 , Elif Neyran Soylu  93 , Faruk Maraşlıoğlu  94 , Agnieszka Napiórkowska-Krzebietke  95 , Agnieszka Ochocka  96 , Agnieszka Pasztaleniec  97 , Ana M. Antão-Geraldes  98 , Vitor Vasconcelos  99 , João Morais  100 , Micaela Vale  101 , Latife Köker  102 , Reyhan Akçaalan  103 , Meriç Albay  104 , Dubravka Špoljarić Maronić  105 , Filip Stević  106 , Tanja Žuna Pfeiffer  107 , Jeremy Fonvielle  108 , Dietmar Straile  109 , Karl-Otto Rothhaupt  110 , Lars-Anders Hansson  111 , Pablo Urrutia-Cordero  112   113 , Luděk Bláha  114 , Rodan Geriš  115 , Markéta Fránková  116 , Mehmet Ali Turan Koçer  117 , Mehmet Tahir Alp  118 , Spela Remec-Rekar  119 , Tina Elersek  120 , Theodoros Triantis  121 , Sevasti-Kiriaki Zervou  122 , Anastasia Hiskia  123 , Sigrid Haande  124 , Birger Skjelbred  125 , Beata Madrecka  126 , Hana Nemova  127 , Iveta Drastichova  128 , Lucia Chomova  129 , Christine Edwards  130 , Tuğba Ongun Sevindik  131 , Hatice Tunca  132 , Burçin Önem  133 , Boris Aleksovski  134 , Svetislav Krstić  135 , Itana Bokan Vucelić  136 , Lidia Nawrocka  137 , Pauliina Salmi  138 , Danielle Machado-Vieira  139 , Alinne Gurjão de Oliveira  140 , Jordi Delgado-Martín  141 , David García  142 , Jose Luís Cereijo  143 , Joan Gomà  144 , Mari Carmen Trapote  145 , Teresa Vegas-Vilarrúbia  146 , Biel Obrador  147 , Magdalena Grabowska  148 , Maciej Karpowicz  149 , Damian Chmura  150 , Bárbara Úbeda  151 , José Ángel Gálvez  152 , Arda Özen  153 , Kirsten Seestern Christoffersen  154 , Trine Perlt Warming  155 , Justyna Kobos  156 , Hanna Mazur-Marzec  157 , Carmen Pérez-Martínez  158 , Eloísa Ramos-Rodríguez  159 , Lauri Arvola  160 , Pablo Alcaraz-Párraga  161 , Magdalena Toporowska  162 , Barbara Pawlik-Skowronska  163 , Michał Niedźwiecki  164 , Wojciech Pęczuła  165 , Manel Leira  166 , Armand Hernández  167 , Enrique Moreno-Ostos  168 , José María Blanco  169 , Valeriano Rodríguez  170 , Jorge Juan Montes-Pérez  171 , Roberto L. Palomino  172 , Estela Rodríguez-Pérez  173 , Rafael Carballeira  174 , Antonio Camacho  175 , Antonio Picazo  176 , Carlos Rochera  177 , Anna C. Santamans  178 , Carmen Ferriol  179 , Susana Romo  180 , Juan Miguel Soria  181 , Julita Dunalska  182 , Justyna Sieńska  183 , Daniel Szymański  184 , Marek Kruk  185 , Iwona Kostrzewska-Szlakowska  186 , Iwona Jasser  187 , Petar Žutinić  188 , Marija Gligora Udovič  189 , Anđelka Plenković-Moraj  190 , Magdalena Frąk  191 , Agnieszka Bańkowska-Sobczak  192 , Michał Wasilewicz  193 , Korhan Özkan  194 , Valentini Maliaka  195   196   197 , Kersti Kangro  198   199 , Hans-Peter Grossart  200   201 , Hans W. Paerl  202 , Cayelan C. Carey  203 , Bas W. Ibelings  204
Affiliations

Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

Evanthia Mantzouki et al. Toxins (Basel). .

Abstract

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.

Keywords: European Multi Lake Survey; anatoxin; cylindrospermopsin; direct effects; indirect effects; microcystin; spatial distribution; temperature.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Percentages of (a) toxin concentrations (μg/L) and (b) toxin quota (μg toxin/μg chlorophyll-a) of each toxin, of the 137 EMLS lakes used in the analyses. Blue shades correspond to the five microcystin variants (MC-YR; MC-dmLR; MC-LR; MC-RR; MC-dmRR), yellow to cylindrospermospin (CYN) and red to anatoxin (ATX). The radius of the pie charts corresponds to (a) the total toxin concentrations and (b) to the total toxin quota.
Figure 1
Figure 1
Percentages of (a) toxin concentrations (μg/L) and (b) toxin quota (μg toxin/μg chlorophyll-a) of each toxin, of the 137 EMLS lakes used in the analyses. Blue shades correspond to the five microcystin variants (MC-YR; MC-dmLR; MC-LR; MC-RR; MC-dmRR), yellow to cylindrospermospin (CYN) and red to anatoxin (ATX). The radius of the pie charts corresponds to (a) the total toxin concentrations and (b) to the total toxin quota.
Figure 2
Figure 2
RDA biplot of the toxin quota (toxin μg/chlorophyll-a μg; Hellinger transformed due to many zeros) of the five microcystin variants (MC-YR; MC-dmLR; MC-LR; MC-RR; MC-dmRR), cylindrospermopsin (CYN) and anatoxin (ATX). The vectors represent the environmental variables: epilimnetic temperature (T_Epi), surface temperature (T_Surf) and the log transformed Secchi depth (Secchi) and maximum buoyancy frequency (BuoyFreq). Length and direction of vectors indicate the strength and direction of the relationship.
Figure 3
Figure 3
Map of the Toxin Diversity Index (TDI) of the 137 EMLS lakes, calculated using the Shannon equation. TDI is categorized in four classes with higher colour density (red) representing higher toxin diversity and lower colour density (white) lower toxin diversity. The radius of the markers corresponds to the total toxin concentration in μg/L.
See this image and copyright information in PMC

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