SpringerLink
Log in

Effects of Chrysosporum (Aphanizomenon) ovalisporum extracts containing cylindrospermopsin on growth, photosynthetic capacity, and mineral content of carrots (Daucus carota)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Natural toxins produced by freshwater cyanobacteria, such as cylindrospermopsin, have been regarded as an emergent environmental threat. Despite the risks for food safety, the impact of these water contaminants in agriculture is not yet fully understood. Carrots (Daucus carota) are root vegetables, extensively consumed worldwide with great importance for human nourishment and economy. It is, therefore, important to evaluate the possible effects of using water contaminated with cyanotoxins on carrot cultivation. The aim of this work was to investigate cylindrospermopsin effects on D. carota grown in soil and irrigated for 30 days, with a Chrysosporum ovalisporum extract containing environmentally relevant concentrations of cylindrospermopsin (10 and 50 μg/L). The parameters evaluated were plant growth, photosynthetic capacity, and nutritional value (mineral content) in roots of carrots, as these are the edible parts of this plant crop. The results show that, exposure to cylindrospermopsin did not have a clear negative effect on growth or photosynthesis of D. carota, even leading to an increase of both parameters. However, alterations in mineral contents were detected after exposure to crude extracts of C. ovalisporum containing cylindrospermopsin. A general decline was observed for most minerals (Ca, Mg, Na, Fe, Mn, Zn, Mo, and P), although an increase was shown in the case of K and Cu, pointing to a possible interference of the cyanobacterial extract in mineral uptake. This study is the first to evaluate the effects of C. ovalisporum extracts on a root vegetable, however, more research is necessary to understand the effects of this toxin in environmentally relevant scenarios.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Azevedo CC, Azevedo J, Osório H, Vasconcelos V, Campos A (2014) Early physiological and biochemical responses of rice seedlings to low concentration of microcystin-LR. Ecotoxicology 23:107–121

    Article  CAS  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: The hidden part of plant defense. Trends Plant Sci 19:90–98

    Article  CAS  Google Scholar 

  • Banker R, Carmeli S, Hadas O, Teltsh B, Porat R, Sukenik A (1997) Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from lake Kinneret, Israel. J Phycol 33:613–616

    Article  CAS  Google Scholar 

  • Bazin E, Mourot A, Humpage AR, Fessard V (2010) Genotoxicity of a freshwater cyanotoxin, cylindrospermopsin, in two human cell lines: Caco-2 and HepaRG. Environ Mol Mutagen 51:251–259

    CAS  Google Scholar 

  • Berry JP, Gibbs PD, Schmale MC, Saker ML (2009) Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo. Toxicon 53:289–299

    Article  CAS  Google Scholar 

  • Beyer D, Surányi G, Vasas G, Roszik J, Erdodi F, M-Hamvas M, Bácsi I, Bátori R, Serfozo Z, Szigeti ZM, Vereb G, Demeter Z, Gonda S, Máthé C (2009) Cylindrospermopsin induces alterations of root histology and microtubule organization in common reed (Phragmites australis) plantlets cultured in vitro. Toxicon 54:440–449

    Article  CAS  Google Scholar 

  • Bogialli S, Bruno M, Curini R, Di Corcia A, Fanali C, Lagana A (2006) Monitoring algal toxins in lake water by liquid chromatography tandem mass spectrometry. Environ Sci Technol 40:2917–2923

    Article  CAS  Google Scholar 

  • Burns J (2008) Toxic cyanobacteria in Florida waters. Adv Exp Med Biol 619:127–137

    Article  CAS  Google Scholar 

  • Capelo A, Santos C, Loureiro S, Pedrosa MA (2012) Phytotoxicity of lead on Lactuca sativa: effects on growth, mineral nutrition, photosynthetic activity and oxidant metabolism. Fresen Environ Bull 21:450–459

    CAS  Google Scholar 

  • Corbel S, Mougin C, Bouaicha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–5

    Article  CAS  Google Scholar 

  • Dai HP, Wei Y, Yang TX, Sa WQ, Wei AZ (2010) Influence of cadmium stress on chlorophyll fluorescence characteristics in Populus 9 canescens. J Food Agric Environ 10:1281–1283

    Google Scholar 

  • De la Cruz AA, Hiskia A, Kaloudis T, Chernoff N, Hill D, Antoniou MG, He X, Loftin K, O’Shea K, Zhao C, Pelaez M, Han C, Lynch TJ, Dionysiou DD (2013) A review on cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ Sci Process Impacts 15:1979–2003

    Article  Google Scholar 

  • El Khalloufi F, Oufdou K, Lahrouni M, El Ghazali I, Saqrane S, Vasconcelos V, Oudra B (2011) Allelopatic effects of cyanobacteria extracts containing microcystins on Medicago sativa-Rhizobia symbiosis. Ecotoxicol Environ Saf 74:431–438

    Article  CAS  Google Scholar 

  • El Khalloufi F, El Ghazali I, Saqrane S, Oufdou K, Vasconcelos V, Oudra B (2012) Phytotoxic effects of a natural bloom extract containing microcystins on Lycopersicon esculentum. Ecotoxicol Environ Saf 79:199–205

    Article  CAS  Google Scholar 

  • Elliott JA (2012) Is the future blue-green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Res 46:1364–1371

    Article  CAS  Google Scholar 

  • Ensafi AA, Khaloo SS (2005) Determination of traces molybdenum by catalytic adsorptive strip** voltammetry. Talanta 65:781–788

    Article  CAS  Google Scholar 

  • Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Article  CAS  Google Scholar 

  • Erofeeva EA (2014) Hormesis and paradoxical effects of wheat seedling (Triticum Aestivum L.) parameters upon exposure to different pollutants in a wide range of doses. Dose Response 12:121–135

    Article  Google Scholar 

  • Freitas M, Azevedo J, Pinto E, Neves J, Campos A, Vasconcelos V (2015) Effects of microcystin-LR, cylindrospermopsin and a microcystin-LR/cylindrospermopsin mixture on growth, oxidative stress and mineral content in lettuce plants (Lactuca sativa L.). Ecotoxicol Environ Saf 116:59–67

    Article  CAS  Google Scholar 

  • Froscio SM, Humpage AR, Wickramasinghe W, Shaw G, Falconer IR (2008) Interaction of the cyanobacterial toxin cylindrospermopsin with the eukaryotic protein synthesis system. Toxicon 5:191–198

    Article  Google Scholar 

  • Garda T, Riba M, Vasas G, Beyer D, M-Hamvas M, Hajdu G, Tándor I, Máthé C (2015) Cytotoxic effects of cylindrospermopsin in mitotic and non-mitotic Vicia faba cells. Chemosphere 120:145–153

    Article  CAS  Google Scholar 

  • Gutiérrez-Praena D, Jos A, Pichardo S, Moreno IM, Cameán AM (2013) Presence and bioaccumulation of microcystins and cylindrospermopsin in food and the effectiveness of some cooking techniques at decreasing their concentrations: a review. Food Chem Toxicol 53:136–152

    Article  Google Scholar 

  • Gutiérrez-Praena D, Campos A, Azevedo J, Neves J, Freitas M, Guzmán-Guillén R, Vasconcelos V (2014) Exposure of Lycopersicon Esculentum to microcystin-LR: Effects in the leaf proteome and toxin translocation from water to leaves and fruits. Toxins 6:1837–1854

    Article  Google Scholar 

  • Guzmán-Guillén R, Prieto AI, González AG, Soria-Díaz ME, Cameán AM (2012) Cylindrospermopsin determination in water by LC–MS/MS: Optimization and validation of the method and application to real samples. Environ Toxicol Chem 31:2233–2238

    Article  Google Scholar 

  • Guzmán-Guillén R, Prieto AI, Moreno I, Rios V, Vasconcelos VM, Camean AM (2014) Effects of depuration on oxidative biomarkers in Tilapia (Oreochromis niloticus) after subchronic exposure to cyanobacterium producing cylindrospermopsin. Aquat Toxicol 149:40–49

    Article  Google Scholar 

  • Havens KE (2008) Cyanobacteria blooms: effects on aquatic ecosystems. Adv Exp Med Biol 619:733–747

    Article  Google Scholar 

  • Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133

    Article  CAS  Google Scholar 

  • Hoeger SJ, Shaw G, Hitzfeld BC, Dietrich DR (2004) Occurrence and elimination of cyanobacterial toxins in two Australian drinking water treatment plants. Toxicon 43:639–649

    Article  CAS  Google Scholar 

  • Humpage A (2008) Toxin types, toxicokinetics and toxicodynamics. In: Hudnel HK (ed) Cyanobacterial harmful algal blooms state of the science and research needs. Springer Press, New York, pp 383–415

    Chapter  Google Scholar 

  • Humpage AR, Falconer IR (2003) Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male Swiss albino mice: determination of no observed adverse effect level for deriving a drinking water guideline value. Environ Toxicol 18:94–103

    Article  CAS  Google Scholar 

  • Ibelings BW, Chorus I (2007) Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–192

    Article  CAS  Google Scholar 

  • Jia L, Liu Z, Chen W, Ye Y, Yu S, He X (2015) Hormesis effects induced by cadmium on growth and phtotosynthetic performance in a hyperaccumulator Lonicera japonica thunb. J Plant Growth Regul 34:13–21

    Article  CAS  Google Scholar 

  • Kinnear S, Fabbro L, Duivenvoorden L (2008) Variable growth responses of water thyme (Hydrilla verticillata); To whole-cell extracts of Cylindrospermopsis raciborskii. Arch Environ Contam Toxicol 54:187–194

    Article  CAS  Google Scholar 

  • Kinnear S (2010) Cylindrospermopsin: a decade of progress on bioaccumulation research. Mar Drugs 8:542–564

    Article  CAS  Google Scholar 

  • Kirkby EA, Römheld V (2007) Micronutrients in Plant Physiology: Functions, Uptake and Mobility. Proceedings 543. The International Fertilizer Society, York, United Kingdom.

  • Kittler K, Schreiner M, Krumbein A, Manzei S, Koch M, Rohn S, Maul R (2012) Uptake of the cyanobacterial toxin cylindrospermopsin in Brassica vegetables. Food Chem 133:875–879

    Article  CAS  Google Scholar 

  • Kosma DK, Rice A, Pollard M (2015) Analysis of aliphatic waxes associated with root periderm or exodermis from eleven plant species. Phytochemistry 117:351–362

    Article  CAS  Google Scholar 

  • Lahrouni M, Oufdou K, El Khalloufi F, Baz M, Lafuente A, Dary M, Pajuelo E, Oudra B (2013) Physiological and biochemical defense reactions of Vicia faba L.-Rhizobium symbiosis face to chronic exposure to cyanobacterial bloom extract containing microcystins. Environ Sci Pollut Res 20:5405–5415

    Article  CAS  Google Scholar 

  • Li TQ, Tao Q, Di ZZ, Lu F, Yang XE (2014) Effect of elevated CO2 concentration on photosynthetic characteristics of hyperaccumulator Sedum alfredii under cadmium stress. J Integr Plant Biol 57:653–660

    Article  Google Scholar 

  • M-Hamvas M, Máthé C, Vasas G, Jámbrik K, Papp M, Beyer D, Mészáros I, Borbély G (2010) Cylindrospermopsin and microcystin-LR alter the growth, development and peroxidase enzyme activity of white mustard (Sinapis alba L.) seedlings, a comparative analysis. Acta Biol Hung 61:35–48

    Article  CAS  Google Scholar 

  • Machado JFF (2014) Implicações do Uso de Água Contaminada com Microcistina na Qualidade de Daucus Carota (Cenoura). Dissertação de Mestrado. Universidade do Porto, Portugal

    Google Scholar 

  • Madhana Sekhar K, Rachapudi VS, Mudalkar S, Reddy AR (2014) Persistent stimulation of photosynthesis in short rotation coppice mulberry under elevated CO2 atmosphere. J Photochem Photobiol B: Biol 137:21–30

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson N (2000) Cholorophyll fluorescence – A practical guide. J Exp Bot 51:659–668

    Article  CAS  Google Scholar 

  • Metcalf JS, Barakate A, Codd GA (2004) Inhibition of plant protein synthesis by the cyanobacterial hepatotoxin, cylindrospermopsin. FEMS Microbiol Lett 235:125–129

    Article  CAS  Google Scholar 

  • Mitrovic SM, Allis O, Furey A, James KJ (2005) Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Chladophorafracta. Ecotoxicol Environ Saf 61:345–352

    Article  CAS  Google Scholar 

  • Moreira C, Azevedo J, Antunes A, Vasconcelos V (2012) Cylindrospermopsin: occurrence, methods of detection and toxicology. J Appl Microbiol 114:605–620

    Article  Google Scholar 

  • Nicolle C, Simon G, Rock E, Amouroux P, Rémésy C (2004) Genetic variability influences carotenoid, vitamin, phenolic, and mineral content in white, yellow, purple, orange and dark orange carrot cultivars. J Am Soc Hortic Sci 129:523–529

    CAS  Google Scholar 

  • Pearson L, Mihali T, Moffitt M, Kellmann R, Neilan B (2010) On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar Drugs 8:1650–1680

    Article  CAS  Google Scholar 

  • Pflugmacher S, Jung K, Lundvall L, Neumann S, Peuthert A (2006) Effects of cyanobacterial toxins and cyanobacterial cell-free crude extract on germination of alfalfa (Medicago sativa) and induction of oxidative stress. Environ Toxicol Chem 25:2381–2387

    Article  CAS  Google Scholar 

  • Pinto E, Almeida AA, Aguiar AA, Ferreira IM (2014a) Changes in macrominerals, trace elements and pigments content during lettuce (Lactuca sativa L.) growth: influence of soil composition. Food Chem 152:603–611

    Article  CAS  Google Scholar 

  • Pinto E, Aguiar AA, Ferreira IM (2014b) Influence of soil chemistry and plant physiology in the phytoremediation of Cu, Mn, and Zn. Crit Rev Plant Sci 33:351–373

    Article  CAS  Google Scholar 

  • Pinto E, Ferreira IMPLVO (2015) Cation transporters/channels in plants: tools for nutrient biofortification. J Plant Physiol 179:64–82

    Article  CAS  Google Scholar 

  • Prieto A, Campos A, Cameán A, Vasconcelos V (2011) Effects on growth and oxidative stress status of rice plants (Oryza sativa) exposed to two extracts of toxin-producing cyanobacteria (Aphanizomenon ovalisporum and Microcystis aeruginosa). Ecotoxicol Environ Safe 74:1973–1980

    Article  CAS  Google Scholar 

  • Quesada A, Moreno E, Carrasco D, Paniagua T, Wörmer L, De Hoyos C, Sukenik A (2006) Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir. Eur J Phycol 41:39–45

    Article  CAS  Google Scholar 

  • Quiblier C, Susanna W, Isidora ES, Mark H, Aurélie V, Jean-François H (2013) A review of current knowledge on toxic benthic freshwater cyanobacteria - Ecology, toxin production and risk management. Water Res 47:5464–5479

    Article  Google Scholar 

  • Rücker J, Stüken A, Nixdorf B, Fastner J, Chorus I, Wiedne C (2007) Concentrations of particulate and disolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50:800–809

    Article  Google Scholar 

  • Saker ML, Eaglesham GK (1999) The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus. Toxicon 37:1065–1077

    Article  CAS  Google Scholar 

  • Saker ML, Metcalf JS, Codd GA, Vasconcelos VM (2004) Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. Toxicon 43:185–194

    Article  CAS  Google Scholar 

  • Saqrane S, Ouahid Y, El Ghazali I, Oudra B, Bouarab L, del Campo FF (2009) Physiological changes in Triticum durum, Zea mays, Pisum sativum and Lens esculenta cultivars, caused by irrigation with water contaminated with microcystins: a laboratory experimental approach. Toxicon 53:786–796

    Article  CAS  Google Scholar 

  • Scherz H, Kirchhoff E (2006) Trace elements in foods: zinc contents of raw foods—A comparison of data originating from different geographical regions of the world. Critical Review. J Food Compos Anal 19:420–433

    Article  CAS  Google Scholar 

  • Shaw GR, Seawright AA, Moore MR, Lam PKS (2009) Cylindrospermopsin, a cyanobacterial alkaloid: evaluation of its toxicologic activity. Ther Drug Monit 22:89–92

    Article  Google Scholar 

  • Van Apeldoorn ME, Van Egmond HP, Speijers GJA, Bakker GJI (2007) Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60

    Article  Google Scholar 

  • Vasas G, Gáspár A, Surányi G, Batta G, Gyémánt G, M-Hamvas M, Máthé C, Grigorszky I, Molnaár E, Borbeély G (2002) Capillary electrophoretic assay and purification of cylindrospermopsin, a cyanobacterial toxin from Aphanizomenon ovalisporum, by plant test (blue-green sinapis test). Anal Biochem 302:95–103

    Article  CAS  Google Scholar 

  • Warman PR, Havard KA (1997) Yield, vitamin and mineral contents of organically and conventionally grown carrots and cabbage. Agr Ecosyst Environ 61:155–162

    Article  CAS  Google Scholar 

  • White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080

    Article  CAS  Google Scholar 

  • Zaccari F, Cabrera MC, Ramos A, Saadoun A (2015) In vitro bioaccessibility of β-carotene, Ca, Mg and Zn in landrace carrots (Daucus carota, L.). Food Chem 166:365–371

    Article  CAS  Google Scholar 

  • Žegura B, Gajski G, Štraser A, Garaj-Vrhovac V (2011) Cylindrospermopsin induced DNA damage and alteration in the expression of genes involved in the response to DNA damage, apoptosis and oxidative stress. Toxicon 58:471–479

    Article  Google Scholar 

Download references

Funding

This work was partially funded by Fundação para a Ciência e Tecnologia (FCT), under the framework of the project UID/Multi/04423/2013, by Ministerio de Ciencia e Innovación of Spain under the project AGL2009-10026, and by Junta de Andalucía under the project P09-AGR-4672. Remedios Guzmán’s work is supported by the Spanish Ministerio de Educación fellowship. Alexandre Campos work is supported by a post-doctoral grant (SFRH/BPD/103683/2014) from FCT.

Author information

Authors and Affiliations

  1. Area of Toxicology, Department of Pharmacy, University of Sevilla, Sevilla, Spain

    Remedios Guzmán-Guillén & Ana M. Cameán

  2. Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), Porto, 4050-123, Portugal

    Alexandre Campos, Joana Machado, Marisa Freitas, Joana Azevedo & Vitor Vasconcelos

  3. LAQV/REQUIMTE, Department of Chemical Sciences, Laboratory of Applied Chemistry, Department of Pharmacy, University of Porto, Rua de Jorge Viterbo Ferreira 228, Porto, 4050-313, Portugal

    Edgar Pinto & Agostinho Almeida

  4. Department of Environmental Health, Escola Superior de Tecnologia da Saúde do Porto, Polytechnic Institute of Porto, CISA/Research Center in Environment and Health, Rua de Valente Perfeito, 322, Gaia, 4400-330, Portugal

    Marisa Freitas & Edgar Pinto

  5. Department of Biology, Department of Sciences of the University of Porto, Porto, 4169-007, Portugal

    Vitor Vasconcelos

Authors
  1. Remedios Guzmán-Guillén
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandre Campos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joana Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marisa Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joana Azevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edgar Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Agostinho Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana M. Cameán
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Vitor Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandre Campos.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guzmán-Guillén, R., Campos, A., Machado, J. et al. Effects of Chrysosporum (Aphanizomenon) ovalisporum extracts containing cylindrospermopsin on growth, photosynthetic capacity, and mineral content of carrots (Daucus carota). Ecotoxicology 26, 22–31 (2017). https://doi.org/10.1007/s10646-016-1737-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1737-4

Keywords

Search

Navigation