Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake

Salah ARIF; Nawel DJEBBARI; Saber BELHAOUES; Hassen TOUATI; Mourad BENSOUILAH

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Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake

Ecology | Updated：2024-10-14

- Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake
- Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake
- 海洋湖沼学报(英文) 2023年41卷第5期页码：1834-1848
- Affiliations：
  
  Eco-biology Laboratory for Marine Environments and Coastal Areas, Faculty of Sciences, Marine Sciences Department, University of Badji Mokhtar, Annaba 23000, Algeria
- Author bio：
  
  arifsalah23@hotmail.com
- Funds：
  
  the General Directorate for Scientific Research and Technological Development, Algeria(D00L03UN230120150002)
- DOI：
  中图分类号：
- 收稿：2021-09-28，
  
  录用：2021-11-11，
  
  网络首发：2022-06-27，
  
  纸质出版：2023-09-01
- Accepted：
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Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake[J]. 海洋湖沼学报(英文), 2023,41(5):1834-1848.

ARIF Salah,DJEBBARI Nawel,BELHAOUES Saber,et al.Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake[J].Journal of Oceanology and Limnology,2023,41(05):1834-1848.
Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake[J]. 海洋湖沼学报(英文), 2023,41(5):1834-1848. DOI：

ARIF Salah,DJEBBARI Nawel,BELHAOUES Saber,et al.Spatio-temporal dynamics of cyanobacterial abundance and toxicity in a Mediterranean hypereutrophic lake[J].Journal of Oceanology and Limnology,2023,41(05):1834-1848. DOI：

摘要

Abstract

The Mediterranean basin is considered one of the most vulnerable areas in the world under the impacts of global warming and changes in precipitation patterns. Oubeira

a shallow and

polymictic freshwater lake located in northeastern Algeria (36‍°‍50′N

08°‍23′E)

has recently experienced a significant proliferation of harmful cyanobacteria resulting in the generation of toxins. We carried out this study in order to understand the succession patterns of dominant cyanobacteria and cyanotoxin production and the factors driving this in Oubeira Lake. A total of 26 cyanobacterial genera were identified

and among them

Microcystis

and

Planktothrix

accounted for more than 60% of the overall cell abundance. The summer/fall period was dominated by

Microcystis

Planktothrix

and in lesser extend by

Cylindrospermum

Cylindrospermopsis

. During the fall/winter transition

Dolichospermum

Pseudanabaena

and

Aphanizomenon

were the dominant genera. Statistically

the bloom-forming cyanobacteria showed significant differences between months but not between stations. Intracellular microcystins (MC-LR) was detected in all collected samples (0.62- and 19.14-‍μg MC-LR equivalent/L)

but

appeared in high concentrations throughout the period of dominance of

Microcystis

and

Planktothrix

Microcystis

was more sensitive to nutrients than to temperature.

Planktothrix

was more dependent on temperature than on nutrients

which explains their coexistence during summer-fall period. However

both genera are positively correlated with MC-LR and would probably be the main producers of microcystins.

Pseudanabaena

Dolichospermum

and

Aphanizomenon

co-occurred at the end of

Planktothrix

dominance period (December).

Aphanizomenon

and

Pseudanabaena

were correlated negatively with temperature and positively with water conductivity.

Dolichospermum

showed a strong positive correlation wi

th MC-LR. Oubeira Lake

could serve as a model of how cyanobacteria blooms may develop in lakes within Mediterranean climates.

关键词

Keywords

references

Afnor N F . 2005 . Qualité de l'eau- dosage des matières en suspension- méthode par filtration sur filtre en fibres de verre (NF EN 872 Juin 2005 / T90 -105 . (in French)

American Public Health Association , American Water Works Association , Water Environment Association , 1998 . Standard Methods for the Examination of Water and Wastewater . 20 th ed n. American Public Health Association , Washington .

Amrani A , Nasri H , Azzouz A et al . 2014 . Variation in cyanobacterial hepatotoxin (microcystin) content of water samples and two species of fishes collected from a shallow lake in Algeria . Archives of Environmental Contamination and Toxicology , 66 ( 3 ): 379 - 389 , https://doi.org/10.1007/s00244-013-9993-2 https://doi.org/10.1007/s00244-013-9993-2 .

Arfa A M T , El Habib Benderradji M , Saint-Gérand T et al . 2019 . Cartographie du risque feu de forêt dans le Nord-est algérien: cas de la wilaya d‍'‍El Tarf. France: Unité Mixte de Recherche 8504 Géographie-cités , https://doi.org/10.4000/cybergeo.32304 https://doi.org/10.4000/cybergeo.32304 .

Bouaicha N , Nasri A B . 2004 . First report of cyanobacterium Cylindrospermopsis raciborskii from Algerian freshwaters . Environmental Toxicology , 19 ( 5 ): 541 - 543 , https://doi.org/10.1002/tox.20058 https://doi.org/10.1002/tox.20058 .

Bouhaddada R , Nélieu S , Nasri H et al . 2016 . High diversity of microcystins in a Microcystis bloom from an Algerian lake . Environmental Pollution , 216 : 836 - 844 , http://doi.org/10.1016/j.envpol.2016.06.055 http://doi.org/10.1016/j.envpol.2016.06.055 .

Boussadia M I , Sehili N , Bousbia A et al . 2015 . The effect of environmental factors on cyanobacteria abundance in Oubeira Lake (Northeast Algeria) . Research Journal of Fisheries and Hydrobiology , 10 ( 14 ): 157 - 168 .

Brient L , Lengronne M , Bertrand E et al . 2008 . A phycocyanin probe as a tool for monitoring cyanobacteria in freshwater bodies . Journal of Environmental Monitoring , 10 ( 2 ): 248 - 255 , https://doi.‍org/10.1039/b714238b https://doi.‍org/10.1039/b714238b . https://do 10.1039/b714238b http://dx.doi.org/10.1039/b714238b

Carey C C , Ibelings B W , Hoffmann E P et al . 2012 . Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate . Water Research , 46 ( 5 ): 1394 - 1407 , https://doi.‍org/10.‍1016/j.‍watres.2011.12.016 https://doi.‍org/10.‍1016/j.‍watres.2011.12.016 . https://do 10.1016/j.watres.2011.12.016 http://dx.doi.org/10.1016/j.watres.2011.12.016

Chaffin J D , Davis T W , Smith D J et al . 2018 . Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production . Harmful Algae , 73 : 84 - 97 , https://doi.org/10.1016/j.hal.2018.02.001 https://doi.org/10.1016/j.hal.2018.02.001 .

Chia M A , Jankowiak J G , Kramer B J et al . 2018 . Succession and toxicity of Microcystis and Anabaena ( Dolichospermum ) blooms are controlled by nutrient-dependent allelopathic interactions . Harmful Algae , 74 : 67 - 77 , https://doi.org/10.1016/j.hal.2018.03.002 https://doi.org/10.1016/j.hal.2018.03.002 .

Codd G A , Meriluoto J , Metcalf J S . 2017 . Introduction: cyanobacteria, cyanotoxins, their human impact and risk management . In: Meriluoto J, Spoof L, Codd G A eds. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis . John Wiley & Sons, Ltd. , Chichester, UK . p. 3 - 8 . https://do 10.1002/9781119068761.ch1 http://dx.doi.org/10.1002/9781119068761.ch1

Davis T W , Bullerjahn G S , Tuttle T et al . 2015 . Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during Planktothrix blooms in Sandusky Bay, Lake Erie . Environmental Science & Technology , 49 ( 12 ): 7197 - 7207 , https://doi.org/10.1021/acs.est.5b00799 https://doi.org/10.1021/acs.est.5b00799 .

Davis T W , Harke M J , Marcoval M A et al . 2010 . Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms . Aquatic Microbial Ecology , 61 ( 2 ): 149 - 162 , https://doi.org/10.3354/ame01445 https://doi.org/10.3354/ame01445 .

De Araujo Torres C , Lürling M , Marinho M M . 2016 . Assessment of the effects of light availability on growth and competition between strains of Planktothrix agardhii and Microcystis aeruginosa . Microbial Ecology , 71 ( 4 ): 802 - 813 , https://doi.org/10.1007/s00248-015-0719-z https://doi.org/10.1007/s00248-015-0719-z .

Du H D , Liu H H , Yuan L et al . 2019 . The diversity of cyanobacterial toxins on structural characterization, distribution and identification: a systematic review . Toxins , 11 ( 9 ): 530 , https://doi.org/10.3390/toxins11090530 https://doi.org/10.3390/toxins11090530 .

Erol A , Randhir T O . 2012 . Climatic change impacts on the ecohydrology of Mediterranean watersheds . Climatic Change , 114 ( 2 ): 319 - 341 , https://doi.‍org/10.‍1007/s10584-012-0406-8 https://doi.‍org/10.‍1007/s10584-012-0406-8 . https://do 10.1007/s10584-012-0406-8 http://dx.doi.org/10.1007/s10584-012-0406-8

Feng B , Wang C , Wu X et al . 2019 . Spatiotemporal dynamics of cell abundance, colony size and intracellular toxin concentrations of pelagic and benthic Microcystis in Lake Caohai, China . Journal of Environmental Sciences , 84 : 184 - 196 , https://doi.org/10.1016/j.jes.2019.05.010 https://doi.org/10.1016/j.jes.2019.05.010 .

Funari E , Testai E . 2008 . Human health risk assessment related to cyanotoxins exposure . Critical Reviews in Toxicology , 38 ( 2 ): 97 - 125 , https://doi.org/10.1080/10408440701749454 https://doi.org/10.1080/10408440701749454 .

Gkelis S , Papadimitriou T , Zaoutsos N et al . 2014 . Anthropogenic and climate-induced change favors toxic cyanobacteria blooms: evidence from monitoring a highly eutrophic, urban Mediterranean lake . Harmful Algae , 39 : 322 - 333 , https://doi.‍org/10.1016/j.‍hal.‍2014.09.002 https://doi.‍org/10.1016/j.‍hal.‍2014.09.002 . https://do 10.1016/j.hal.2014.09.002 http://dx.doi.org/10.1016/j.hal.2014.09.002

Glibert P M , Wilkerson F P , Dugdale R C et al . 2016 . Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen‍‐‍enriched conditions . Limnology and Oceanography , 61 ( 1 ): 165 - 197 , https://doi.‍org/10.‍1002/lno.10203 https://doi.‍org/10.‍1002/lno.10203 . https://do 10.1002/lno.10203 http://dx.doi.org/10.1002/lno.10203

Gobler C J , Burkholder J M , Davis T W et al . 2016 . The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms . Harmful Algae , 54 : 87 - 97 , https://doi.org/10.1016/j.hal.2016.01.010 https://doi.org/10.1016/j.hal.2016.01.010 .

Hamouda S , Tahar A . 2012 . Apport de l'analyse spatiale dans le suivi du couvert végétal du parc national d'El-Kala, (Algérie) . Synthèse , 18 ( 2 ): 5970 . (in French)

Harke M J , Gobler C J . 2013 . Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa , to nitrogen stress, phosphorus stress, and growth on organic matter . PLoS One , 8 ( 7 ): e69834 , https://doi.org/10.1371/journal.pone.0069834 https://doi.org/10.1371/journal.pone.0069834 .

Huang I S , Zimba P V . 2019 . Cyanobacterial bioactive metabolites—a review of their chemistry and biology . Harmful Algae , 86 : 139 - 209 , https://doi.‍org/10.1016/j.‍hal.2019.05.001 https://doi.‍org/10.1016/j.‍hal.2019.05.001 . https://do 10.1016/j.hal.2019.05.001 http://dx.doi.org/10.1016/j.hal.2019.05.001

Humbert J F , Fastner J . 2017 . Ecology of cyanobacteria . In: Meriluoto J, Spoof L, Codd G A eds. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis . John Wiley & Sons, Ltd., West Sussex , UK , https://doi.org/10.1002/9781119068761.ch2 https://doi.org/10.1002/9781119068761.ch2 .

Komárek J , Anagnostidis K . 1999 . Cyanoprokaryota: Part 1: Chroococcales . In: Ettl H, Gärtner G, Heynig H et al eds. Süßwasserflora von Mitteleuropa Begründet von A. PascherBd. 19 / 3 Cyanoprokaryota. 1. Teil Chroococcales. Spektrum, Akademischer Verlag, Heidelberg, Germany .

Komárek J , Anagnostidis K . 2005 . Cyanoprokaryota: Part 2: Oscillatoriales SüBwasserflora von Mittelleuropa freshwater flora of Central Europe . Spektrum Akademischer Verlag Heidelberg, Germany .

Komárek J , Kaštovský J , Mareš J et al . 2014 . Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach . Preslia , 86 ( 4 ): 295 - 335 .

Lee S J , Jang M H , Kim H S et al . 2000 . Variation of microcystin content of Microcystis aeruginosa relative to medium N:P ratio and growth stage . Journal of Applied Microbiology , 89 ( 2 ): 323 - 329 , https://doi.org/10.1046/j.1365-2672.2000.01112.x https://doi.org/10.1046/j.1365-2672.2000.01112.x .

Lee T A , Rollwagen-Bollens G , Bollens S M et al . 2015 . Environmental influence on cyanobacteria abundance and microcystin toxin production in a shallow temperate lake . Ecotoxicology and Environmental Safety , 114 : 318 - 325 , https://doi.org/10.1016/j.ecoenv.2014.05.004 https://doi.org/10.1016/j.ecoenv.2014.05.004 .

Ma Z L , Fang T X , Thring R W et al . 2015 . Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris . Harmful Algae , 48 : 21 - 29 , https://doi.org/10.1016/j.hal.2015.07.002 https://doi.org/10.1016/j.hal.2015.07.002 .

Mathe C , M-Hamvas M , Garda T et al . 2017 . Cellular effects of cylindrospermopsin (cyanobacterial alkaloid toxin) and its potential medical consequences . Current Medicinal Chemistry , 24 ( 1 ): 91 - 109 , https://doi.‍org/10.2174/0929867323666161028153814 https://doi.‍org/10.2174/0929867323666161028153814 . https://do 10.2174/0929867323666161028153814 http://dx.doi.org/10.2174/0929867323666161028153814

Mehnert G , Leunert F , Cirés S et al . 2010 . Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions . Journal of Plankton Research , 32 ( 7 ): 1009 - 1021 . https://doi.org/10.1093/plankt/fbq033 https://doi.org/10.1093/plankt/fbq033 .

Nasri A B , Bouaïcha N , Fastner J . 2004 . First report of a microcystin-containing bloom of the cyanobacteria Microcystis spp. in Oubeira Lake, Eastern Algeria . Archives of Environmental Contamination and Toxicology , 46 ( 2 ): 197 - 202 , https://doi.org/10.1007/s00244-003-2283-7 https://doi.org/10.1007/s00244-003-2283-7 .

Özen A , Karapınar B , Kucuk I et al . 2010 . Drought-induced changes in nutrient concentrations and retention in two shallow Mediterranean lakes subjected to different degrees of management . Hydrobiologia , 646 ( 1 ): 61 - 72 , https://doi.org/10.1007/s10750-010-0179-x https://doi.org/10.1007/s10750-010-0179-x .

Paerl H W , Huisman J . 2008 . Blooms like it hot . Science , 320 ( 5872 ): 57 - 58 , https://doi.org/10.1126/science.1155398 https://doi.org/10.1126/science.1155398 .

Paerl H W , Otten T G . 2013 . Harmful cyanobacterial blooms: causes, consequences, and controls . Microbial Ecology , 65 ( 4 ): 995 - 1010 , http://doi.‍org/10.‍1007/s00248-012-0159-y http://doi.‍org/10.‍1007/s00248-012-0159-y . https://do 10.1007/s00248-012-0159-y http://dx.doi.org/10.1007/s00248-012-0159-y

Reynolds C S , Huszar V , Kruk C et al . 2002 . Towards a functional classification of the freshwater phytoplankton . Journal of Plankton Research , 24 ( 5 ): 417 - 428 , https://doi.org/10.1093/plankt/24.5.417 https://doi.org/10.1093/plankt/24.5.417 .

Romo S , Soria J , Fernández F et al . 2013 . Water residence time and the dynamics of toxic cyanobacteria . Freshwater Biology , 58 ( 3 ): 513 - 522 , https://doi.‍org/10.1111/j.‍1365-2427.2012.02734.x https://doi.‍org/10.1111/j.‍1365-2427.2012.02734.x . https:// do 10.1111/j.1365-2427.2012.02734.x http://dx.doi.org/10.1111/j.1365-2427.2012.02734.x

Søndergaard M , Jensen J P , Jeppesen E . 2003 . Role of sediment and internal loading of phosphorus in shallow lakes . Hydrobiologia , 506 ( 1 ): 135 - 145 , https://doi.‍org/10.1023/B:HYDR.0000008611.12704.dd https://doi.‍org/10.1023/B:HYDR.0000008611.12704.dd .

Souissi M , Chaibi R , Melizi M et al . 2004 . Les cyanobactéries d'un plan d'eau douce (le lac Oubeira-El Kala). Inventaire et répartition spatiale. Sciences & Technologie . C, Biotechnologies , 38 - 42 . (in French)

Spoof L , Catherine A . 2017 . Appendix 3: tables of microcystins and nodularins . In: Meriluoto J, Spoof L, Codd G A eds. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis . John Wiley & Sons, Ltd., West Sussex , UK , https://doi.‍org/10.1002/9781119068761.app3 https://doi.‍org/10.1002/9781119068761.app3 . https://do 10.1002/9781119068761.app3 http://dx.doi.org/10.1002/9781119068761.app3

Sukenik A , Hadas O , Kaplan A et al . 2012 . Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes-physiological, regional, and global driving forces . Frontiers in Microbiology , 3 : 86 , https://doi.org/10.3389/fmicb.2012.00086 https://doi.org/10.3389/fmicb.2012.00086 .

Sun J , Liu D Y . 2003 . Geometric models for calculating cell biovolume and surface area for phytoplankton . Journal of Plankton Research , 25 ( 11 ): 1331 - 1346 , https://doi.org/10.1093/plankt/fbg096 https://doi.org/10.1093/plankt/fbg096 .

Taranu Z E , Gregory‐Eaves I , Steele R J et al . 2017 . Predicting microcystin concentrations in lakes and reservoirs at a continental scale: a new framework for modelling an important health risk factor . Global Ecology and Biogeography , 26 ( 6 ): 625 - 637 , https://doi.org/10.1111/geb.12569 https://doi.org/10.1111/geb.12569 .

Touati H , Guellati F Z , Arif S et al . 2019 . Cyanobacteria dynamics in a mediterranean reservoir of the north east of Algeria: vertical and seasonal variability . Journal of Ecological Engineering , 201 : 93 - 107 , https://doi.‍org/10.12911/22998993/94606 https://doi.‍org/10.12911/22998993/94606 . https://do 10.12911/22998993/94606 http://dx.doi.org/10.12911/22998993/94606

Uvëges V , Tapolczai K , Krienitz L et al . 2012 . Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos - aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligo-mesotrophic lake (Lake Stechlin, Germany) . Hydrobiologia , 698 ( 1 ): 263 - 272 , https://doi.org/10.1007/s10750-012-1103-3 https://doi.org/10.1007/s10750-012-1103-3 .

Van de Waal D B , Ferreruela G , Tonk L et al . 2010 . Pulsed nitrogen supply induces dynamic changes in the amino acid composition and microcystin production of the harmful cyanobacterium Planktothrix agardhii . FEMS Microbiology Ecology , 74 ( 2 ): 430 - 438 , https://doi.‍org/10.‍1111/j.‍1574-6941.2010.00958.x https://doi.‍org/10.‍1111/j.‍1574-6941.2010.00958.x . https://do 10.1111/j.1574-6941.2010.00958.x http://dx.doi.org/10.1111/j.1574-6941.2010.00958.x

Wu S , Wang S , Yang H et al . 2008 . Field studies on the environmental factors in controlling microcystin production in the subtropical shallow lakes of the Yangtze River . Bulletin of Environmental Contamination and Toxicology , 80 ( 4 ): 329 - 334 , https://doi.org/10.1007/s00128-008-9378-9 https://doi.org/10.1007/s00128-008-9378-9 .

Zhao H J , Wang Y , Yang L L et al . 2015 . Relationship between phytoplankton and environmental factors in landscape water supplemented with reclaimed water . Ecological Indicators , 58 : 113 - 121 , https://doi.‍org/10.1016/j.ecolind.2015.03.033 https://doi.‍org/10.1016/j.ecolind.2015.03.033 . https://do 10.1016/j.ecolind.2015.03.033 http://dx.doi.org/10.1016/j.ecolind.2015.03.033

Zidane B , Akila A , Ounissi M et al . 2013 . Dynamic densities and specific cyanobacteria biomass of Oubeira Lake (National Parc of Elkala, Algeria) . Environmental Research Journal , 7 ( 1 ): 9 - 14 , https://doi.‍org/10.36478/erj.2013.9.14 https://doi.‍org/10.36478/erj.2013.9.14 .

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