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Toxic effects of erythromycin on photosystem I and II in Microcystis aeruginosa

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Photosynthetica

Abstract

Environmental pollution by antibiotics poses a potential ecological risk to aquatic photosynthetic organisms. In the present study, toxic effects of erythromycin on PSI and PSII were investigated in cyanobacteria culture medium of Microcystis aeruginosa. The activity and electron transport of both photosystems were affected by erythromycin in a concentrationdependent manner. The quantum yield of PSII (YII) was reduced at 0.1 mg L−1 of erythromycin, while the quantum yield of PSI (YI) significantly decreased at concentration of 5–25 mg L−1. The decline of YII was accompanied by an increase of nonregulated energy dissipation (YNO). At 10 mg L−1 of erythromycin, YII decreased by 55%, while YNO increased by 18%. The decrease of YI induced by erythromycin was caused by donor-side limitation of PSI (YND). YND was markedly enhanced with elevated erythromycin concentration. At 10 mg L−1 of erythromycin, YI and YNA (PSI acceptor-side limitation) decreased by 8 and 82%, respectively, while YND rose by 314%. The quantum yield of cyclic electron flow increased significantly at 0.1–1 mg L−1 of erythromycin; it decreased but remained higher than that of the control at 5–25 mg L−1 of erythromycin. The contribution of cyclic electron flow to YI, and to linear electron flow rose significantly with the increasing erythromycin concentration. The maximum values of electron transport rates in PSII and PSI decreased by 71 and 24.3%, respectively, at 25 mg L−1 of erythromycin. Compared with the untreated control, the light saturation of PSII and PSI decreased significantly with increasing erythromycin concentration. We showed that concentrations of erythromycin ≥ 5 mg L−1 could exert acute toxicity to cyanobacteria, whereas the chronic toxicity caused by concentrations of ng or μg L−1 needs further research.

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Abbreviations

CEF:

cyclic electron flow

ETR:

electron transport rate

ETRI :

electron transport rate in PSI

ETRII :

electron transport rate in PSII

ETRmax(I) :

the maximum electron transport rate in PSI

ETRmax(II) :

the maximum electron transport rate in PSII

I k(I) :

the light saturation of PSI

I k(II) :

the light saturation of PSII

LEF:

linear electron flow

NPQ:

nonphotochemical quenching

RLC:

rapid light curves

YCEF :

the quantum yield of cyclic electron flow

YCEF/YI :

the contribution of cyclic electron flow to YI

YCEF/YII :

the ratio of the quantum yield of CEF to LEF

YI :

effective photochemical quantum yield of PSI

YII :

the effective photochemical quantum yield of PSII

YII/YI :

the distribution of quantum yield between two photosystems

YNA :

nonphotochemical energy dissipation due to acceptor-side limitation

YND :

nonphotochemical energy dissipation due to donor-side limitation

YNO :

nonregulated energy dissipation

YNPQ :

regulated energy dissipation

α I :

the initial slope of RLC of ETRI

α II :

the initial slope of RLC of ETRII

References

  • Alder, A.C., McArdell, C.S., Golet, E.M. et al.: Environmental exposure of antibiotics in Switzerland. — In: Kümmerer, K. (ed.): Pharmaceuticals in the Environment: Sources Fate, Effects and Risks. Pp. 63–64. Springer, Freiburg 2004.

    Google Scholar 

  • Aristilde, L., Melis, A., Sposito, G.: Inhibition of photosynthesis by a fluoroquinolone antibiotic. — Environ. Sci. Technol. 41: 1444–1450, 2010.

    Article  Google Scholar 

  • Belatik, A., Hotchandani, S., Tajmir-Riahi, H.A., et al.: Alteration of the structure and function of photosystem I by Pb2+. — J. Photoch. Photobio. B. 123: 41–47, 2013.

    Article  CAS  Google Scholar 

  • Chittum, H.S., Champney, W.S.: Erythromycin inhibits the assembly of the large ribosomal subunit in growing Escherichia coli cells. — Curr. Microbiol. 30: 273–279, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Fick, J., Söderström, H., Lindberg, R.H. et al.: Contamination of surface, ground, and drinking water from pharmaceutical production. — Environ. Toxicol. Chem. 28: 2522–2527, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Gao, S., Wang, G.: The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). — J. Exp. Bot. 63: 4349–4358, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Gao, S., Shen, S.D., Wang, G.C. et al.: PSI-driven cyclic electron flow allows intertidal Macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. — Plant Cell Physiol. 52: 885–893, 2011.

    Article  CAS  PubMed  Google Scholar 

  • González-Pleiter, M., Gonzalo, S., Rodea-Palomares, I. et al.: Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: Implication for environmental risk assessment. — Water Res. 47: 2050–2064, 2013.

    Article  PubMed  Google Scholar 

  • Halling-Sørensen, B.: Algal toxicity of antibacterial agents used in intensive farming. — Chemosphere 40: 731–739, 2000.

    Article  PubMed  Google Scholar 

  • Holten-Lützhøft, H.C., Halling-Sørensen, B., Jørgensen, S.E.: Algal toxicity of antibacterial agents applied in Danish fish farming. — Arch. Environ. Con. Tox. 36: 1–6, 1999.

    Article  Google Scholar 

  • Huang, W., Yang, S.J., Zhang, S.B. et al.: Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. — Planta 235: 819–828, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Huang, W., Zhang, S.B., Cao, K.F.: Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. — Plant Cell Physiol. 51: 1922–1928, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Isidori, M., Lavorgna, M., Nardelli, A. et al.: Toxic and genotoxic evaluation of six antibiotics on non-target organisms. — Sci. Total Environ. 346: 87–98, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Jin, S.H., Wang, D., Zhu, F.Y. et al.: Up-regulation of cyclic electron flow and down regulation of linear electron flow in antisense-rca mutant rice. — Photosynthetica 46: 506–510, 2008.

    Article  CAS  Google Scholar 

  • Klughammer, C., Schreiber, U.: Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. — PAM Appl. Notes 1: 27–35, 2008.

    Google Scholar 

  • Kolpin, D.W., Furlong, E.T., Meyer, M.T. et al.: PharmaceuticalsF hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. — Environ. Sci. Technol. 36: 1202–1211, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Kramer, D.M., Johnson, G., Kiirats, O., Edwards, G.E.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. — Photosynth. Res. 79: 209–218, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Kudoh, H., Sonoike, K.: Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. — Planta 215: 541–548, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Kümmerer, K.: Antibiotics in the aquatic environment. A review. Part I. — Chemosphere 75: 417–434, 2009a.

    Article  PubMed  Google Scholar 

  • Kümmerer, K.: Antibiotics in the aquatic environment. A review. Part II. — Chemosphere 75: 435–441, 2009b.

    Article  PubMed  Google Scholar 

  • Li, X.G., Xu, P.L., Zhao, J.P. et al.: Ferredoxin-quinone reductase benefits cyclic electron flow around photosystem I in tobacco leaves upon exposure to chilling stress under low irradiance. — Photosynthetica 44: 349–354, 2006.

    Article  CAS  Google Scholar 

  • Lin, A.Y.C., Tsai, Y.T.: Occurrence of pharmaceuticals in Taiwan’s surface waters: Impact of waste streams from hospitals and pharmaceutical production facilities. — Sci. Total Environ. 407: 3793–3802, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Liu, B.Y., Nie, X.P., Liu, W.Q. et al.: Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole on photosynthetic apparatus in Selenastrum capricornutum. — Ecotox. Environ. Safe. 74: 1027–1035, 2011.

    Article  CAS  Google Scholar 

  • Lu, K.X., Yang, Y., He, Y., Jiang, D.A.: Induction of cyclic electron flow around photosystem I and state transition are correlated with salt tolerance in soybean. — Photosynthetica 46: 10–16, 2008.

    Article  CAS  Google Scholar 

  • Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence — a practical guide. — J. Exp. Bot. 51: 659–668, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Miyake, C., Horiguchi, S., Makino, A. et al.: Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. — Plant Cell Physiol. 46: 1819–1830, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Munekage, Y., Hojo, M., Meurer, J. et al.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. — Cell 110: 361–371, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Nie, X.P., Liu, B.Y., Yu, H.J. et al.: Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole exposure to the antioxidant system in Pseudokirchneriella subcapitata. — Environ. Pollut. 172: 23–32, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Pan, X.L., Deng, C.N., Zhang, D.Y. et al.: Toxic effects of amoxicillin on the photosystem II of Synechocystis sp. characterized by a variety of in vivo chlorophyll fluorescence tests. — Aquat. Toxicol. 89: 207–213, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Pan, X.L., Zhang, D.Y., Chen, X. et al.: Effects of levofloxacin hydrochlordie on photosystem II activity and heterogeneity of Synechocystis sp. — Chemosphere 77: 413–418, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Park, S.J., Choi, K.H.: Hazard assessment of commonly used agricultural antibiotics on aquatic ecosystems. — Ecotoxicology 17: 526–538, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Pestka, S.: Insights into protein biosynthesis and ribosome function through inhibitiors. — Prog. Nucleic Acid Res. Mol. Biol. 17: 217–245, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Pfündel, E., Klughammer, C., Schreiber, U.: Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. — PAM Appl. Notes 1: 21–24, 2008.

    Google Scholar 

  • Pinckney, J.L., Hagenbuch, I.M., Long, R.A., Lovell, C.R.: Sublethal effects of the antibiotic tylosin on estuarine benthic microalgal communities. — Mar. Pollut. Bull. 68: 8–12, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Platt, T., Gallegos, C.L., Harrison, W.G.: Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. — J. Mar. Res. 38: 687–701, 1980.

    Google Scholar 

  • Richardson, B.J., Lam, P.K.S., Martin, M.: Emerging chemicals of concern: pharmaceuticals and personal care products (PPCPs) in Asia, with particular reference to Southern China. — Mar. Pollut. Bull. 50: 913–920, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Santos, L.H., Araújo, A.N., Fachini, A., et al.: Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. — J. Hazard. Mater. 175: 45–95, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Sarmah, A.K., Meyer, M.T., Boxall, A.B.A.: A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. — Chemosphere 65: 725–759, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Saroussi, S., Beer, S.: Alpha and quantum yield of aquatic plants derived from PAM fluorometry: Uses and misuses. — Aquat. Bot. 86: 89–92, 2007.

    Article  Google Scholar 

  • Schreiber, U., Muller, J.F., Haugg, A., Gademann, R.: New type of dual-channel PAM chlorophyll fluorometer for highly sensitive water toxicity biotests. — Photosynth. Res. 74: 317–330, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Scribner, E.A., Dietze, J.E., Meyer, M.T., Kolpin, D.W.: Occurrence of antibiotics in water from fish hatcheries [abs.]. — In: 21st Annual Water and Future of Kansas Conference. Pp. 68. Water Resources Research Institute, New York 2004.

    Google Scholar 

  • Singh, R., Dubey, G., Singh, V.P. et al.: High light intensity augments mercury toxicity in cyanobacterium Nostoc muscorum. — Biol. Trace Elem. Res. 149: 262–272, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G.: Purification and properties of unicellular blue-green algae (order Chroococcales). — Bacteriol. Rev. 35: 171–205, 1971.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stoichev, T., Baptista, M.S., Basto, M.C.P. et al.: Effects of minocycline and its degradation products on the growth of Microcystis aeruginosa. — Ecotox. Environ. Safe. 74: 219–224, 2011.

    Article  CAS  Google Scholar 

  • Strasser, B.J.: Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. — Photosynth. Res. 52: 147–155, 1997.

    Article  CAS  Google Scholar 

  • Suzuki, K., Ohmori, Y., Ratel, E.: High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings. — Plant Cell Physiol. 52: 1697–1707, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, S., Milward, S.E., Fan, D.Y. et al.: How does cyclic electron flow alleviate photoinhibition in Arabidopsis? — Plant Physiol. 149: 1560–1567, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang, S.Z., Chen, F.L., Mu, S.Y. et al.: Simutaneous analysis of photosystem responses of Microcystis aeruginoga under chromium stress. — Ecotox. Environ. Safe. 88: 163–168, 2013.

    Article  CAS  Google Scholar 

  • Wang, S.Z., Zhang, D.Y., Pan, X.L.: Effects of arsenic on growth and photosystem II (PSII) activity of Microcystis aeruginosa. — Ecotox. Environ. Safe. 84: 104–111, 2012.

    Article  CAS  Google Scholar 

  • White, S., Anandraj, A., Bux, F.: PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. — Bioresource Technol. 102: 1675–1682, 2011.

    Article  CAS  Google Scholar 

  • Wise, R.: Antimicrobial resistance: priorities for action. — J. Antimicrob. Chemoth. 49: 585–586, 2002.

    Article  CAS  Google Scholar 

  • Wodala, B., Eitel, G., Gyula, T.N. et al.: Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P700 absorbance in pea leaves. — Photosynthetica 50: 380–386, 2012.

    Article  CAS  Google Scholar 

  • Yang, W.W., Tang, Z.P., Zhou, F.Q. et al.: Toxicity studies of tetracycline on Microcystis aeruginosa and Selenasrum capricornutum. — Environ.Toxicol. Phar. 35: 320–324, 2013.

    Article  CAS  Google Scholar 

  • Zuccato, E., Calamari, D., Natangelo, M., Fanelli, R..: Presence of therapeutic drugs in the environment. — Lancet 355: 1789–1790, 2000.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to X. -L. Pan.

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Acknowledgements: This work was supported by Program of 100 Distinguished Young Scientists of the Chinese Academy of Sciences (U1120302), National Natural Science Foundation of China (21177127, 21467031) and Specialized Research Fund for the Doctoral Program of Higher Education (20125303120003). We are grateful to the editor and the anonymous reviewers for their valuable comments and suggestions.

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Deng, C.N., Zhang, D.Y. & Pan, X.L. Toxic effects of erythromycin on photosystem I and II in Microcystis aeruginosa . Photosynthetica 52, 574–580 (2014). https://doi.org/10.1007/s11099-014-0063-4

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  • DOI: https://doi.org/10.1007/s11099-014-0063-4

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