Skip to main content
Log in

The effect of pyrogallic acid on growth, oxidative stress, and gene expression in Cylindrospermopsis raciborskii (Cyanobacteria)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

In order to investigate the effect of the allelopathic compound pyrogallic acid on Cylindrospermopsis raciborskii F2, the impact on growth, oxidative stress and expression of the psbA, grpE, fabZ, recA, cmpA, ftsZ and cyrJ genes were studied. The results indicated significant decreases in Chl a and cell number following a 24-h incubation with 4 mg L−1 pyrogallic acid. Additionally, malodialdehyde content, superoxide dismutase activity and catalase activity were enhanced following treatment with 2 and 4 mg L−1 pyrogallic acid. Expressions of the genes psbA, grpE, fabZ, recA and cyrJ were significantly up-regulated following exposure to 4 mg L−1 pyrogallic acid, while no changes were observed with concentrations of 1 or 2 mg L−1. Expression of cmpA was significantly down-regulated following treatment with the lowest tested concentration of pyrogallic acid (1 mg L−1), while ftsZ was only significantly down-regulated with concentrations of 2 and 4 mg L−1. These results suggest that photosynthesis inhibition and oxidative damage are important modes of action for the allelopathic effect of pyrogallic acid on C. raciborskii.

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

Access this article

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
Fig. 5

Similar content being viewed by others

References

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 143:113–134

    Google Scholar 

  • Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Bácsi I, Vasas G, Surányi G, M-Hamvas M, Máthé C, Tóth E, Grigorszky I, Gáspár A, Tóth S, Borbely G (2006) Alteration of cylindrospermopsin production in sulfate- or phosphate-starved cyanobacterium Aphanizomenon ovalisporum. FEMS Microbiol Lett 259:303–310

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Belz RG, Hurle K (2004) A novel laboratory screening bioassay for crop seeding allelopathy. J Chem Ecol 30:175–198

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Byth S (1980) Palm Island mystery disease. Med J Aust 2:40–42

    CAS  Google Scholar 

  • Carmichael WW, Beasley V, Bunner DL, Eloff JN, Falconer IR, Gorham P, Harada K-I, Krishnamurthy T, Yu M, Moore RE, Rinehart K, Runnegar M, Skulberg OM, Watanabe M (1988) Naming of cyclic heptapetide toxins of cyanobacteria (blue–green algae). Toxicon 26:971–973

    Article  CAS  Google Scholar 

  • Chang X, Eigemann F, Hilt S (2012) Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae 19:76–84

    Article  CAS  Google Scholar 

  • Choi HJ, Kim BH, Kim JD, Han MS (2005) Streptomyces neyagawaensis as a control for the hazardous biomass of Microcysits aeruginosa (Cyanobacteria) in eutrophic freshwaters. Biol Control 33:335–343

    Article  Google Scholar 

  • Choo KS, Snoeijs P, Pedersén M (2004) Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana. J Exp Mar Bio Ecol 298:111–123

    Article  CAS  Google Scholar 

  • de Oliveira-Filho EC, Lopes RM, Paumagartten FJR (2004) Comparative study on the susceptibility of freshwater species to copper-based pesticides. Chemosphere 56:369–374

    Article  Google Scholar 

  • Duarte CM, Kalff J (1990) Biomass density and the relationship between submerged macrophyte biomass and plant growth form. Hydrobiologia 196:17–23

    Article  Google Scholar 

  • Dziga D, Suda M, Bialczyk J, Urszula CP, Lechowski Z (2007) The alteration of Microcystis aeruginosa biomass and dissolved microcystin-LR concentration following exposure to plant-producing phenols. Environ Toxicol 22:341–346

    Article  CAS  Google Scholar 

  • Gopal B, Goel U (1993) Competition and allelopathy in aquatic plant communities. Bot Rev 59:155–210

    Article  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Hawkins PR, Runnegar MT, Jackson AR, Falconer IR (1985) Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Appl Environ Microbiol 50:1292–1295

    CAS  Google Scholar 

  • Hawkins PR, Putt E, Falconer IR, Humpage A (2001) Phenotypical variation in a toxic strain of the phytoplankter, Cylindrospermopsis raciborskii (nostocales, cyanophyceae) during batch culture. Environ Toxicol 16:460–467

    Article  CAS  Google Scholar 

  • Hilt S, Ghobrial MGN, Gross EM (2006) In situ allelopathic potential of Myriophyllum verticillatum (haloragaceae) against selected phytoplankton species. J Phycol 42:1189–1198

    Article  Google Scholar 

  • Hong Y, Hu H, Xie X, Sakoda A, Sagehashi M, Li F (2009) Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. Aquat Toxicol 91:262–269

    Article  CAS  Google Scholar 

  • Hrudey S, Burch S, Burch M, Drikas M, Greorgy R (1999) Remedial measures. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Routledge, London, pp 275–312

    Google Scholar 

  • Huisman JM, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. Springer aquatic ecology series 3. Springer, Dordrecht

    Book  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  Google Scholar 

  • Ichimura T (1979) Isolation and culture methods of algae (Sôrui no bunri to baiyôhô. 2.5.B. Tansui sôrui). In: Nishizawa K, Chihara M (eds) Methods in phycological studies (Sôrui Kenkyûhô). Kyoritu Shuppan, Tokyo, pp 294–305 (in Japanese without English title)

    Google Scholar 

  • Inderjit S, Dakshini KMM (1994) Algal allelopathy. Bot Rev 60:182–196

    Article  Google Scholar 

  • Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539

    Article  CAS  Google Scholar 

  • Khil PP, Camerini-Otero RD (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microb 44:89–105

    Article  CAS  Google Scholar 

  • Klint J, Rasmussen U, Bergman B (2007) FtsZ may have dual roles in the filamentous cyanobacterium Nostoc/Anabaena sp. strain PCC 7120. J Plant Physiol 164:11–18

    Article  CAS  Google Scholar 

  • Körner S, Nicklisch A (2000) Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. J Phycol 38:862–871

    Article  Google Scholar 

  • Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo SMFQ, Oshima Y (1999) The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37:1359–1373

    Article  CAS  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 

  • Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, Noparatnaraporn AMN, Yongmanitchai W, Kaya K, Watanabe MM (2001) Detection of cylindrospermopsin from a strain of Cylindrospermopsis raciborskii (Cyanobacteria) isolated from Thailand. Toxicon 39:973–980

    Article  CAS  Google Scholar 

  • Lipinska B, King J, Ang D, Georgopoulos C (1988) Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein. Nucleic Acids Res 16:7545–7562

    Article  CAS  Google Scholar 

  • Liu B, Zhou P, Tian J, Jiang S (2007) Effect of pyrogallol on the growth and pigment content of cyanobacteria-blooming toxic and nontoxic Microcystis aeruinosa. Bull Environ Contam Toxicol 78:499–502

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and 2−ΔΔCt the method. Method 25:402–408

    Article  CAS  Google Scholar 

  • Maeda S, Price GD, Badger MR, Enomoto C, Omata T (2000) Bicarbonate binding activity of the cmpA protein of the cyanobacterium Synechococcus PCC7942 is involved in active transport of bicarbonate. J Biol Chem 275:20551–20555

    Google Scholar 

  • McGregor GB, Sendall BC, Hunt LT, Eaglesham GK (2011) Report of the cyanotoxins cylindrospermopsin and deoxy-cylindrospermopsin from Raphidiopsis mediterranea Skuja (Cyanobacteria/Nostocales). Harmful Algae 10:402–410

    Article  CAS  Google Scholar 

  • Mihali TK, Kellmann R, Muenchhoff J, Barrow KD, Neilan BA (2008) Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl Environ Microbiol 74:716–722

    Article  CAS  Google Scholar 

  • Mulderij G, Mooij WM, Smolders AJP, Van Donk E (2005) Allelopathic inhibition of phytoplankton by exudates from Stratiotes aloides. Aquat Bot 82:284–296

    Article  Google Scholar 

  • Nakai S, Inoue Y, Hosomi M, Murakami A (1999) Growth inhibition of blue-green algae by allelopathic effects of macrophytes. Water Sci Technol 39:47–53

    Google Scholar 

  • Nakai S, Inoue Y, Hosomi M, Murakami A (2000) Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Res 34:3026–3032

    Article  CAS  Google Scholar 

  • Nakai S, Inoue Y, Hosomi M (2001) Algal growth inhibition effects and inducement modes by plant-producing phenols. Water Res 35:1855–1859

    Article  CAS  Google Scholar 

  • Nor YM (1987) Ecotoxicology of copper to aquatic biota: a review. Environ Res 43:274–282

    Article  CAS  Google Scholar 

  • Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigment determination. Archiv Hydrobiol Beiheft Ergebnisse Limnol 14:14–36

    CAS  Google Scholar 

  • Ohta H, Shibata Y, Haseyama Y, Yoshino Y, Suzuki T, Kagasawa T, Kamei A, Ikeuchi M, Enami I (2005) Identification of genes expressed in response to acid stress in Synechocystis sp. PCC 6803 using DNA microarrays. Photosynth Res 84:225–230

    Article  CAS  Google Scholar 

  • Ohtani I, Moore RE, Runnegar MTC (1992) Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J Am Chem Soci 114:7941–7942

    Article  CAS  Google Scholar 

  • Padisák J (1997) Cylindrospermopsis raciborskii (Woloszaynska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol 107:563–593

    Google Scholar 

  • Paerl HW (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. Adv Exp Med Biol 619:216–241

    Google Scholar 

  • Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37

    Article  CAS  Google Scholar 

  • Preußel K, Stuken A, Wiedner C, Chorus I, Fastner J (2006) First report on cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) isolated from two German lakes. Toxicon 47:156–162

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Saito K, Matsumoto M, Sekine T, Murakoshi I (1989) Inhibitory substances from Myriophyllum brasiliense on growth of blue–green algae. J Nat Prod 52:1221–1226

    Article  CAS  Google Scholar 

  • Saker M (2000) Cyanobacterial blooms in tropical North Queensland water bodies. PhD thesis. James Cook University, Townsville, Australia

  • Saker ML, Griffiths DJ (2000) The effect of temperature on growth and cylindrospermopsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia 39:349–354

    Article  Google Scholar 

  • Schembri MA, Neilan BA, Saint CP (2001) Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Toxicol 16:413–421

    Article  CAS  Google Scholar 

  • Shao J, Wu Z, Yu G, Peng X, Li R (2009) Allelopathic mechanism of pyrogallol to Microcystis aeruginosa PCC 7806 (Cyanobacteria): from views of gene expression and antioxidant system. Chemosphere 75:924–928

    Article  CAS  Google Scholar 

  • Shapiro J (1997) The role of carbon dioxide in the initiation and maintenance of blue–green dominance in lakes. Freshw Biol 37:307–323

    Article  Google Scholar 

  • Sinha R, Pearson LA, Davis TW, Burford MA, Orr PT, Neilan BA (2012) Increased incidence of Cylindrospermopsis raciborskii in temperate zones—is climate change responsible? Water Res 46:1408–1419

    Article  CAS  Google Scholar 

  • Spencer CM, Cai Y, Martin R, Gaffney SH, Goulding PN, Magnolato D, Lilley TH, Haslam E (1988) Polyphenol complexation—some thoughts and observations. Phytochemistry 27:2397–2409

    Article  CAS  Google Scholar 

  • Spoof L, Berg KA, Rapala J, Lahti K, Lepisto L, Metcalf JS, Codd GA, Meriluoto J (2006) First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21:552–560

    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 blue–green alga Umezakia natans. Toxicon 32:833–843

    Article  CAS  Google Scholar 

  • Uchimaya M, Mihara M (1978) Determination of malonadehyde precursor in tissues by thiobarbituric acid test. Analyt Biochem 86:271–278

    Article  Google Scholar 

  • Wu Z, Gan N, Huang Q, Song L (2007) Response of Microcystis to copper stress—do phenotypes of Microcystis make a difference in stress tolerance? Environ Pollut 147:324–330

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study was supported by the National Natural Science Foundation of China (31170372) and Doctoral Found Project of China SWU (SWU110065).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhongxing Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, Z., Shi, J. & Yang, S. The effect of pyrogallic acid on growth, oxidative stress, and gene expression in Cylindrospermopsis raciborskii (Cyanobacteria). Ecotoxicology 22, 271–278 (2013). https://doi.org/10.1007/s10646-012-1023-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-012-1023-z

Keywords

Navigation