Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii.

The effect of core-shell copper oxide nanoparticles with sizes smaller than 100 nm on cellular systems is still not well understood. Documenting these effects is pressing since core-shell copper oxide nanoparticles are currently components of pigments used frequently as antifouling paint protecting boats from crustacean, weed and slime fouling. However, the use of such paints may induce strong deteriorative effects on different aquatic trophic levels that are not the intended targets. Here, the toxic effect of core-shell copper oxide nanoparticles on the green alga, Chlamydomonas reinhardtii was investigated with regards to the change of algal cellular population structure, primary photochemistry of photosystem II and reactive oxygen species formation. Algal cultures were exposed to 0.004, 0.01 and 0.02 g/l of core-shell copper oxide nanoparticles for 6h and a change in algal population structure was observed, while the formation of reactive oxygen species was determined using the 2',7'-dichlorodihydrofluorescein diacetate marker measured by flow cytometry. For the study of the photosystem II primary photochemistry we investigated the change in chlorophyll a rapid rise of fluorescence. We found that core-shell copper oxide nanoparticles induced cellular aggregation processes and had a deteriorative effect on chlorophyll by inducing the photoinhibition of photosystem II. The inhibition of photosynthetic electron transport induced a strong energy dissipation process via non-photochemical pathways. The deterioration of photosynthesis was interpreted as being caused by the formation of reactive oxygen species induced by core-shell copper oxide nanoparticles. However, no formation of reactive oxygen species was observed when C. reinhardtii was exposed to the core without the shell or to the shell only.

[1]  Mohammad Yunus,et al.  Probing photosynthesis : mechanisms, regulation, and adaptation , 2000 .

[2]  N. Sueoka,et al.  Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi. I. Isotopic transfer experiments with a strain producing eight zoospores. , 1967, Journal of molecular biology.

[3]  Pedro J J Alvarez,et al.  Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. , 2006, Water research.

[4]  H. Nalwa,et al.  Nanotoxicology: Interactions of Nanomaterials with Biological Systems , 2007 .

[5]  Lazăr,et al.  Chlorophyll a fluorescence induction1 , 1999, Biochimica et biophysica acta.

[6]  D. Morse,et al.  HEAVY METAL–INDUCED OXIDATIVE STRESS IN ALGAE 1 , 2003 .

[7]  C. Critchley,et al.  New fluorescence parameters for monitoring photosynthesis in plants , 2004, Photosynthesis Research.

[8]  A. Turner,et al.  Leaching of copper and zinc from spent antifouling paint particles. , 2009, Environmental pollution.

[9]  R. Strasser,et al.  Measuring fast fluorescence transients to address environmental questions: the JIP-test , 1995 .

[10]  Partial Photooxidation of Ethylene with Water as Oxidant over Copper Oxide Supported on Silica , 2001 .

[11]  P. Bowen,et al.  Photocatalytic storing of O2 as H2O2 mediated by high surface area CuO. Evidence for a reductive-oxidative interfacial mechanism. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[12]  R. Strasser,et al.  Analysis of the Chlorophyll a Fluorescence Transient , 2004 .

[13]  G. Vernet,et al.  Determination of photosynthetic and enzymatic biomarkers sensitivity used to evaluate toxic effects of copper and fludioxonil in alga Scenedesmus obliquus. , 2005, Aquatic toxicology.

[14]  Peter M.A. Toivonen,et al.  Practical Applications of Chlorophyll Fluorescence in Plant Biology , 2003, Springer US.

[15]  John Moncrieff,et al.  Photosynthesis: from Light to Biosphere , 1995 .

[16]  J. Breton,et al.  Methodological principles of measurement of light emitted by photosynthetic systems. , 1986 .

[17]  M. Greger,et al.  Aggregation effects due to aluminum adsorption to cell walls of the unicellular green alga Scenedesmus obtusiusculus , 2004 .

[18]  P. Mathis,et al.  Primary Processes of Photosynthesis , 1981 .

[19]  Z. Mohamed.  Polysaccharides as a protective response against microcystin-induced oxidative stress in Chlorella vulgaris and Scenedesmus quadricauda and their possible significance in the aquatic ecosystem , 2008, Ecotoxicology.

[20]  P. Juneau,et al.  Applications of Chlorophyll Fluorescence in Ecotoxicology: Heavy Metals, Herbicides, and Air Pollutants , 2003 .

[21]  H. Lichtenthaler.  CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[22]  Hong-Ying Hu,et al.  Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. , 2009, Aquatic toxicology.

[23]  B. Behrends,et al.  A methodology for evaluating biocide release rate, surface roughness and leach layer formation in a TBT-free, self-polishing antifouling coating , 2006, Biofouling.

[24]  Govindjee,et al.  Light Emission by Plants and Bacteria , 1986 .

[25]  Nanna B. Hartmann,et al.  Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi , 2008, Ecotoxicology.

[26]  H. Karlsson,et al.  Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. , 2008, Chemical research in toxicology.

[27]  B. Strasser,et al.  Comparison of light induced and cell cycle dependent changes in the photosynthetic apparatus: A fluorescence induction study on the green alga Scenedesmus obliquus , 1999, Photosynthesis Research.

[28]  Jean-Christophe Daigle,et al.  A Simple Method for Forming Hybrid Core-Shell Nanoparticles Suspended in Water , 2008 .

[29]  I. Dubery,et al.  Fluorescence microplate assay for the detection of oxidative burst products in tobacco cell suspensions using 2',7'-dichlorofluorescein. , 2003, Methods in cell science : an official journal of the Society for In Vitro Biology.

[30]  G. Samson,et al.  Use of algal fluorescence for determination of phytotoxicity of heavy metals and pesticides as environmental pollutants. , 1988, Ecotoxicology and environmental safety.

[31]  M. Moore,et al.  Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? , 2006, Environment international.

[32]  Milton Sommerfeld,et al.  Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. , 2008, Chemosphere.

[33]  T. Diamantino,et al.  Marine paints: The particular case of antifouling paints , 2007 .

[34]  A. K. Tyagi,et al.  Physics and chemistry of photocatalytic titanium dioxide: visualization of bactericidal activity using atomic force microscopy , 2006 .

[35]  C. Leygraf,et al.  Release and chemical speciation of copper from anti‐fouling paints with different active copper compounds in artificial seawater , 2007 .

[36]  Brad M. Angel,et al.  Uptake and internalisation of copper by three marine microalgae: comparison of copper-sensitive and copper-tolerant species. , 2008, Aquatic toxicology.

[37]  K. Knauer,et al.  THE ROLE OF REACTIVE OXYGEN SPECIES IN COPPER TOXICITY TO TWO FRESHWATER GREEN ALGAE 1 , 2008, Journal of phycology.