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Potential role of the cellular matrix of Aphanizomenon strains in the effects of cylindrospermopsin—an experimental study

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Abstract

Some literature data suggest that one of the possible roles of the cyanotoxin cylindrospermopsin (CYN) is forcing other phytoplankton species in the environment to produce alkaline phosphatase, which enables the cyanobacterium to take up the enzymatically liberated phosphate. In this study, cultures of a planktonic green alga, Scenedesmus obtusus (Chlorophyta, Sphaeropleales), were treated with CYN producer Aphanizomenon (Cyanobacteria, Nostocales) crude extract (C+), with non-CYN producer Aphanizomenon crude extract (C−), and with non-CYN producer Aphanizomenon crude extract supplemented with CYN (C−+C). The results showed that C+ treatment induced both acidic and alkaline phosphatases of the studied cosmopolitan green alga, which otherwise was neither sensitive to the relatively high CYN concentration, nor to phosphate limitation. In cases of C− and C−+C treatments, these phenomena were not observed. Several studies suggest that additional compounds may support CYN action. The results presented here suggest in a more direct way that other components present in the cellular matrix of the producer organism itself are involved in the effects of CYN, activation of phosphatases (not only alkaline ones) among them. These other components are absent in C− crude extract or cannot actively contribute to the effects of exogenously added CYN.

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References

  • Aguilera A, Aubriot L, Echenique RO, Salerno GL, Brena BM, Pírez M, Bonilla S (2017) Synergistic effects of nutrients and light favor Nostocales over non-heterocystous cyanobacteria. Hydrobiologia 794:241–255

    Article  CAS  Google Scholar 

  • Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20:1557–1561

    Article  CAS  PubMed  Google Scholar 

  • B-Béres V, Grigorszky I, Vasas G, Borics G, Várbíró G, Nagy SA, Borbély G, Bácsi I (2012) The effects of Microcystis aeruginosa (cyanobacterium) on Cryptomonas ovata (Cryptophyta) in laboratory cultures, why these organisms do no coexist in steady-state assemblages? Hydrobiologia 691:97–107

    Article  CAS  Google Scholar 

  • B-Béres V, Vasas G, Dobronoki D, Gonda S, Nagy SA, Bácsi I (2015) Effects of cylindrospermopsin producing cyanobacterium and its crude extracts on a benthic green alga—competition or allelopathy? Mar Drugs 13:6703–6722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard C, Harvey M, Briand JF, Bire R, Krys S, Fontaine JJ (2003) Toxicological comparison of diverse Cylindrospermopsis raciborskii strains, evidence of liver damage caused by a French C. raciborskii strain. Environ Toxicol 18:176–186

    Article  CAS  PubMed  Google Scholar 

  • Bittencourt-Oliveria MC, Chia MA, Oliveria HSB, Araújo MKC, Molica RJR, Dias CTS (2015) Allelopathic interactions between microcystin-producing and non-microcystin-producing cyanobacteria and green microalgae: implication for microcystins production. J Appl Phycol 27:275–284

    Article  CAS  Google Scholar 

  • Bittencourt-Oliveria MC, Chia MA, Camargo-Santos D, Dias CTS (2016) The effect of saxitoxin and non-saxitoxin extracts of Cylindrospermopsis raciborskii (Cyanobacteria) on cyanobacteria and green microalgae. J Appl Phycol 28:241–250

    Article  CAS  Google Scholar 

  • Bohunická M, Mareš J, Hrouzek P, Urajová P, Lukeš M, Šmarda J, Komárek J, Gaysina LA, Sturnecký O (2015) A combined morphological, ultrastructural, molecular, and biochemical study of the peculiar family Gomontiellaceae (Oscillatoriales) reveals a new cylindrospermopsin-producing clade of cyanobacteria. J Appl Phycol 51:1040–1054

    Article  CAS  Google Scholar 

  • Bonente G, Pippa S, Castellano S, Bassi R, Ballottari M (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J Biol Chem 287:5833–5847

    Article  CAS  PubMed  Google Scholar 

  • Bowen ID, Bryant JA (1978) The fine structural localization of p-nitrophenyl phosphatase activity in the storage cells of pea (Pisum sativum L.) cotyledons. Protoplasma 97:241–250

    Article  CAS  Google Scholar 

  • Burford MA, Beardall J, Willis A, Orr PT, Magalhaes VF, Rangel LM, Azevedo SMFOE, Neilan BA (2016) Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 54:44–53

    Article  PubMed  Google Scholar 

  • Campos A, Araújó P, Pinheiro C, Azvedo J, Osório H, Vasconcelos V (2013) Effects on growth, antioxidant enzyme activity and levels of extracellular proteins in the green alga Chlorella vulgaris exposed to crude cyanobacterial extracts and pure microcystin and cylindrospermopsin. Ecotoxicol Environ Saf 94:45–53

    Article  CAS  PubMed  Google Scholar 

  • Carvalho AP, Monteiro CM, Malcata FX (2009) Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavlova lutheri. J Appl Phycol 21:543–552

    Article  Google Scholar 

  • CCAP Media Recipes (n.d.) Available online: http://www.ccap.ac.uk/media/documents/JM.pdf (Accessed on 3 June 2018)

  • Cembella AD, Antia NJ, Harrison PJ (1984) The utilization of inorganic and organic phosphorus-compounds as nutrients by eukaryotic microalgae—a multidisciplinary perspective. Crit Rev Microbiol 11:13–81

    Article  CAS  PubMed  Google Scholar 

  • DuBois JD, Roberts KR, Kapustka LA (1984) Polyphosphate body and acid phosphatase localization in Nostoc sp. Can J Microbiol 30:8–15

    Article  CAS  Google Scholar 

  • Fastner J, Heinze R, Humpage AR, Mischke U, Eaglesham GK, Chorus I (2003) Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. Toxicon 42:313–321

    Article  CAS  PubMed  Google Scholar 

  • Felföldy L (1987) Ecological status assessment. (In Hungarian: A biológiai vízminősítés.) In: Vízügyi Hidrobiológia 16. VGI, Budapest. pp 258

  • Ferreira VS, Pinto RF, Sant’Anna C (2016) Low light intensity and nitrogen starvation modulate the chlorophyll content of Scenedesmus dimorphus. J Appl Microbiol 120:661–670

    Article  CAS  PubMed  Google Scholar 

  • Freitas M, Campos A, Azevedo J, Barreiro A, Planchon S, Renaut J, Vasconcelos V (2015) Lettuce (Lactuca sativa L.) leaf-proteome profiles after exposure to cylindrospermopsin and a microcystin-LR/cylindrospermopsin mixture: a concentration-dependent response. Phytochemistry 110:91–103

    Article  CAS  PubMed  Google Scholar 

  • Froscio SM, Humpage AR, Burcham PC, Falconer IR (2001) Cell-free protein synthesis inhibition assay for the cyanobacterial toxin cylindrospermopsin. Environ Toxicol 16:408–412

    Article  CAS  PubMed  Google Scholar 

  • Froscio SM, Humpage AR, Burcham PC, Falconer IR (2003) Cylindrospermopsin induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environ Toxicol 18:243–251

    Article  CAS  PubMed  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 51:191–198

    Article  CAS  PubMed  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaentol Electron 4(1) Unpaginated

  • He Q, Yang H, Wua L, Hua C (2015) Effect of light intensity on physiological changes, carbon allocation and neutral lipid accumulation in oleaginous microalgae. Bioresour Technol 191:219–228

    Article  CAS  PubMed  Google Scholar 

  • Hindák F (1990) Studies on the chlorococcal algae (Chlorophyceae). V, VEDA Publishing House of the Slovak Academy of Sciences, Bratislava

    Google Scholar 

  • Humpage AR, Fenech M, Thomas P, Falconer IR (2000) Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin. Mutat Res 472:155–161

    Article  CAS  PubMed  Google Scholar 

  • Hussain A, Krischke M, Roitsch T, Hasnain S (2010) Rapid determination of cytokinins and auxin in cyanobacteria. Curr Microbiol 61:361–369

    Article  CAS  PubMed  Google Scholar 

  • Ihlenfeldt MJ, Gibson J (1975) Phosphate utilization and alkaline phosphatase activity in Anacystis nidulans (Synechococcus). Arch Microbiol 102:23–28

    Article  CAS  PubMed  Google Scholar 

  • Karadžić V, Simić GS, Natić DR, Ržaničanin A, Cirić M, Gačić Z (2013) Changes in the phytoplankton community and dominance of Cylindrospermopsis raciborskii (Wolosz.) Subba Raju in a temperate lowland river (Ponjavica, Serbia). Hydrobiologia 711:43–60

    Article  CAS  Google Scholar 

  • Komárek J (2013) Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota 3. Teil/3rd part: Heterocytous Genera. Springer Spektrum, Heidelberg

  • Kruskopf MM, Du Plessis S (2004) Induction of both acid and alkaline phosphatase activity in two green-algae (Chlorophyceae) in low N and P concentrations. Hydrobiologia 513:59–70

    Article  CAS  Google Scholar 

  • Kuenzler EJ (1965) Glucose-6-phosphate utilization by marine algae. J Phycol 1:156–164

    Article  Google Scholar 

  • Kuenzler EJ, Perras JP (1965) Phosphatases of marine algae. Biol Bull 128:271–284

    Article  Google Scholar 

  • Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282

    Article  CAS  PubMed  Google Scholar 

  • Leflaive J, Ten-Hage L (2007) Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 52:199–214

    Article  CAS  Google Scholar 

  • MSZ EN ISO 6878 (2004) Water quality. Determination of phosphorus. Ammonium molybdate spectrometric method (ISO 6878:2004)

  • Omidi A, Esterhuizen-Londt M, Pflugmacher S (2018) Still challenging: the ecological function of the cyanobacterial toxin microcystin—what we know so far. Toxin Rev 37:87–105

    Article  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  PubMed  PubMed Central  Google Scholar 

  • Pinheiro C, Azvedo J, Campos A, Loureiro S, Vasconcelos V (2013) Absence of negative allelopathic effects of cylindrospermopsin and microcystin-LR on selected marine and freshwater phytoplankton species. Hydrobiologia 705:27–42

    Article  CAS  Google Scholar 

  • Poniedziałek B, Rzymski P, Kokociński M (2012a) Cylindrospermopsin: water-linked potential threat to human health in Europe. Environ Toxicol Pharmacol 34:651–660

    Article  CAS  PubMed  Google Scholar 

  • Poniedziałek B, Rzymski P, Wiktorowicz K (2012b) First report of cylindrospermopsin effect on human peripheral blood lymphocytes proliferation in vitro. Cent Eur J Immunol 37:314–317

    Article  CAS  Google Scholar 

  • Poniedziałek B, Rzymski P, Wiktorowicz K (2014a) Toxicity of cylindrospermopsin in human lymphocytes: proliferation, viability and cell cycle studies. Toxicol in Vitro 28:968–974

    Article  CAS  PubMed  Google Scholar 

  • Poniedziałek B, Rzymski P, Karczewski J (2014b) Cylindrospermopsin decreases the oxidative burst capacity of human neutrophils. Toxicon 87:113–199

    Article  CAS  PubMed  Google Scholar 

  • Poniedziałek B, Rzymski P, Karczewski J (2015) The role of the enzymatic antioxidant system in cylindrospermopsin-induced toxicity in human lymphocytes. Toxicol in Vitro 29:926–932

    Article  CAS  PubMed  Google Scholar 

  • Rhee G (1973) A continuous culture study of phosphate uptake, growth rate and polyphosphate in Scenedesmus sp. J Phycol 9:495–506

    CAS  Google Scholar 

  • Runnegar MT, Kong SM, Zhong YZ, Lu SC (1995) Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem Pharmacol 49:219–225

    Article  CAS  PubMed  Google Scholar 

  • Rymuszka A, Sieroslawska A (2014) Cylindrospermopsin induces oxidative stress and genotoxic effects in the fish CLC cell line. J Appl Toxicol 35:426–433

    PubMed  Google Scholar 

  • Rzymski P, Poniedziałek B (2014) In search of environmental role of cylindrospermopsin: a review on global distribution and ecology of its producers. Water Res 66:320–337

    Article  CAS  PubMed  Google Scholar 

  • Rzymski P, Poniedziałek B, Kokociński M, Jurczak T, Lipski D, Wiktorowicz K (2014) Interspecific allelopathy in cyanobacteria: cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 35:1–8

    Article  CAS  Google Scholar 

  • Saker ML, Nogueira ICG, Vasconcelos VM, Neilan BA, Eaglesham GH, Pereira P (2003) First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotoxicol Environ Saf 55:243–250

    Article  CAS  PubMed  Google Scholar 

  • Sergeeva E, Liaaimer A, Bergman B (2002) Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215:229–238

    Article  CAS  PubMed  Google Scholar 

  • Shen X, Lam PKS, Shaw GR, Wickramasinghe W (2002) Genotoxicity investigation of a cyanobacterial toxin, cylindrospermopsin. Toxicon 40:1499–1501

    Article  CAS  PubMed  Google Scholar 

  • Soares MC, Lürling M, Panosso R, Huszar V (2009) Effects of the cyanobacterium Cylindrospermopsis raciborskii on feeding and life-history characteristics of the grazer Daphnia magna. Ecotoxicol Environ Saf 72:1183–1189

    Article  CAS  PubMed  Google Scholar 

  • Stirk WA, Ördög V, Van Staden J, Jäger K (2002) Cytokinin- and auxin-like activity in Cyanophyta and microalgae. J Appl Phycol 14:215–221

    Article  CAS  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Terao K, Ohmori S, Igarashi K, Ohtani I, Watanabe MF, Harada KI, Ito E, Watanabe M (1994) Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from the blue-green alga Umezakia natans. Toxicon 32:833–844

    Article  CAS  PubMed  Google Scholar 

  • Tsavkelova EA, Klimova SY, Cherdyntsteva TA, Netrosov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microl 42:117–126

    Article  CAS  Google Scholar 

  • Vasas G, Gáspár A, Surányi G, Batta G, Gyémánt G, M-Hamvas M, Máthé M, Grigorszky I, Molnár E, Borbély 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  PubMed  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3th edn. Prentice-Hall International, New York

    Google Scholar 

  • Zhang W, Jeppensen E, Wang M, Xu Z, Wang L (2016) Allelopathic effect boots Chrysosporum ovalisporum dominance in summer at the expense of Microcystis panniformis in a shallow coastal water body. Environ Sci Pollut Res 24:4666–4675

    Article  CAS  Google Scholar 

  • Zhang W, Jeppesen E, Wang M, Xu X, Wang L (2017) Allelopathic effect boosts Chrysosporum ovalisporum dominance in summer at the expense of Microcystis panniformis in a shallow coastal water body

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Acknowledgements

The research was financed by the Higher Education Institutional Excellence Programme of the Ministry of Human Capacities in Hungary, within the framework of the fourth thematic program of the University of Debrecen. The work was supported by the ÚNKP-18-3 New National Excellence Program of the Ministry of Human Capacities (D.D.)

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Authors and Affiliations

  1. Department of Hydrobiology, University of Debrecen, Egyetem sqr. 1, Debrecen, 4032, Hungary

    Dalma Dobronoki, Sándor Alex Nagy & István Bácsi

  2. MTA Centre for Ecological Research, GINOP Sustainable Ecosystems Group, Klebelsberg Kuno str. 3, Tihany, 8237, Hungary

    Viktória B-Béres

  3. MTA-DE Lendület Functional and Restoration Ecology Research Group, Egyetem sqr. 1, Debrecen, 4032, Hungary

    Viktória B-Béres

  4. Department of Botany, University of Debrecen, Egyetem sqr. 1, Debrecen, 4032, Hungary

    Gábor Vasas & Sándor Gonda

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  1. Dalma Dobronoki
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  2. Viktória B-Béres
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  3. Gábor Vasas
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  4. Sándor Gonda
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  5. Sándor Alex Nagy
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  6. István Bácsi
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Contributions

Experiments were performed by D.D. and V.B-B. (Figs. 1, 2, 3, 4, and 5). S.G. and G.V. provided the purified CYN and contributed to the preparation of crude extracts and instrumental analytical measurements. S.A.N. provided additional financial support for the experiments. D.D., G.V., and I.B. related to conception and design of the study, acquisition of data, analysis and interpretation of data, and drafting the article. I.B. supervised the whole work and finalized the manuscript.

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Correspondence to István Bácsi.

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Dobronoki, D., B-Béres, V., Vasas, G. et al. Potential role of the cellular matrix of Aphanizomenon strains in the effects of cylindrospermopsin—an experimental study. J Appl Phycol 31, 1805–1817 (2019). https://doi.org/10.1007/s10811-018-1699-4

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