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Physiological and structural responses of the seagrass Cymodocea nodosa to titanium dioxide nanoparticle exposure

  • Zoi Mylona

    Zoi Mylona has a BSc degree in environmental sciences (A.U.Th.) and has completed her postgraduate studies at the Interdisciplinary Postgraduate Study Program “Ecological Water Quality and Management at a River Basin Level” (A.U.Th.). She is a PhD student at the School of Biology, Department of Botany (A.U.Th.) and she is currently working at iSea, Environmental Organization for the Preservation of Aquatic Ecosystems. Her research interests focus on seagrass ecophysiology and ecotoxicology.

         , Emmanuel Panteris

    Emmanuel Panteris is an associate professor of botany in Aristotle University of Thessaloniki. He received a diploma in biology (1989) and a Ph.D. in biology (1995) from University of Athens, Greece. His research focuses on plant cell biology, with emphasis on the cytoskeleton, expanding from the molecular factors that regulate cytoskeletal organization to the responses of cytoskeletal elements to environmental challenges. He applies microscopy, as well as genetic and biochemical approaches.

         , Theodoros Kevrekidis

    Theodoros Kevrekidis is a professor at the Democritus University of Thrace (DUTH), Greece. At present, Prof. Kevrekidis is the dean of the School of Education Sciences and head of the Laboratory of Environmental Research and Education of the DUTH. His current research focus areas are the biology of marine macroinvertebrates, the structure and dynamics of marine macrozoobenthos, and the ecology and ecophysiology of marine angiosperms and macroalgae. His research also focuses on ocean literacy.

         and Paraskevi Malea

    Paraskevi Malea is an associate professor at the School of Biology, Aristotle University of Thessaloniki, Greece. Her specialist research field is the ecology and ecophysiology of seagrasses and seaweeds. Current research focuses on metal accumulation and bioindication in marine macrophytes, as well as on morphological, physiological and cellular responses of these organisms to stress induced by anthropogenic chemicals and the detection of biomarkers for the evaluation of environmental quality.

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Published/Copyright: October 21, 2020
Botanica Marina
From the journal Botanica Marina Volume 63 Issue 6

Abstract

The extensive application of titanium dioxide nanoparticles (TiO2 NPs) has raised concern about its environmental risks. The present study aims to elucidate TiO2 NP ecotoxicity, by assessing effects on seagrasses at environmentally relevant concentrations. Changes in physiological and structural cell traits of Cymodocea nodosa leaves, treated with TiO2 NPs at 0.0015–1.5 mg l−1 for eight consecutive days, were investigated. Intracellular levels of hydrogen peroxide (H2O2) increased significantly, even early during the lowest exposure, despite an up-regulation of H2O2-scavenging enzyme activity. Actin filaments (AFs) and endoplasmic reticulum (ER) were affected in a concentration- and time-dependent pattern, while no changes in microtubule organization and cell ultrastructure were detected. The lowest effect concentrations for AF and ER impairment were 0.15 and 1.5 mg l−1, respectively; for cell death, these were 0.15–1.5 mg l−1, depending on leaf age, and for leaf elongation inhibition 0.15 mg l−1. Thus, elevated H2O2 level can be considered as an early warning biomarker for TiO2 NPs, while leaf elongation, AF and ER impairment are also reliable indicators. A risk quotient greater than 1 was estimated; thus, TiO2 NPs might present a significant potential environmental risk. Our findings can be utilized for monitoring pollution levels in coastal environments.

Keywords: biomarker; Cymodocea nodosa; cytotoxicity; physiological response; risk assessment
Corresponding author: Paraskevi Malea, Department of Botany, School of Biology, Aristotle University of Thessaloniki, GR-54124Thessaloniki, Greece, E-mail:

About the authors

Zoi Mylona

Zoi Mylona has a BSc degree in environmental sciences (A.U.Th.) and has completed her postgraduate studies at the Interdisciplinary Postgraduate Study Program “Ecological Water Quality and Management at a River Basin Level” (A.U.Th.). She is a PhD student at the School of Biology, Department of Botany (A.U.Th.) and she is currently working at iSea, Environmental Organization for the Preservation of Aquatic Ecosystems. Her research interests focus on seagrass ecophysiology and ecotoxicology.

Emmanuel Panteris

Emmanuel Panteris is an associate professor of botany in Aristotle University of Thessaloniki. He received a diploma in biology (1989) and a Ph.D. in biology (1995) from University of Athens, Greece. His research focuses on plant cell biology, with emphasis on the cytoskeleton, expanding from the molecular factors that regulate cytoskeletal organization to the responses of cytoskeletal elements to environmental challenges. He applies microscopy, as well as genetic and biochemical approaches.

Theodoros Kevrekidis

Theodoros Kevrekidis is a professor at the Democritus University of Thrace (DUTH), Greece. At present, Prof. Kevrekidis is the dean of the School of Education Sciences and head of the Laboratory of Environmental Research and Education of the DUTH. His current research focus areas are the biology of marine macroinvertebrates, the structure and dynamics of marine macrozoobenthos, and the ecology and ecophysiology of marine angiosperms and macroalgae. His research also focuses on ocean literacy.

Paraskevi Malea

Paraskevi Malea is an associate professor at the School of Biology, Aristotle University of Thessaloniki, Greece. Her specialist research field is the ecology and ecophysiology of seagrasses and seaweeds. Current research focuses on metal accumulation and bioindication in marine macrophytes, as well as on morphological, physiological and cellular responses of these organisms to stress induced by anthropogenic chemicals and the detection of biomarkers for the evaluation of environmental quality.

Acknowledgments

The authors are grateful to Assoc. Prof. D. Fatouros (School of Pharmacy, AUTH, Greece), and Prof. T. Kechagias and Assoc. Prof. G. Vourlias (School of Physics, AUTH, Greece) for their support with TiO2 NP characterization. Thanks are due to the anonymous referees for thoughtful critiques and comments.

  1. Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Adamakis, I.-D.S., Malea, P., and Panteris, E. (2018). The effects of bisphenol A on the seagrass Cymodocea nodosa: leaf elongation impairment and cytoskeleton disturbance. Ecotoxicol. Environ. Saf. 157: 431–440, https://doi.org/10.1016/j.ecoenv.2018.04.005.Search in Google Scholar

Baluska, F., Jasik, J., Edelman, H.G., Salajova, T., and Volkmann, D. (2001). Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin dependent. Dev. Biol. 231: 113–124, https://doi.org/10.1006/dbio.2000.0115.Search in Google Scholar

Baskin, T.I. and Bivens, N.J. (1995). Stimulation of radial expansion in Arabidopsis roots by inhibitors of actomyosin and vesicle secretion but not by various inhibitors of metabolism. Planta 197: 514–521, https://doi.org/10.1007/BF00196673.Search in Google Scholar

Beyer, W.F.J.R. and Fridovich, I. (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 161: 559–566, https://doi.org/10.1016/0003-2697(87)90489-1.Search in Google Scholar

Blancaflor, E.B. (2000). Cortical actin filaments potentially interact with cortical microtubules in regulating polarity of cell expansion in primary roots of maize (Zea mays L.). J. Plant Growth Regul. 19: 406–414, https://doi.org/10.1007/s003440000044.Search in Google Scholar PubMed

Bradford, M.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, https://doi.org/10.1006/abio.1976.9999.Search in Google Scholar PubMed

Bundschuh, M., Filser, J., Lüderwald, S., McKee, M.S., Metreveli, G., Scaumann, G.E., Schulz, R., and Wagner, S. (2018). Nanoparticles in the environment: where do we come from, where do we go to?. Environ. Sci. Eur. 30: 6, https://doi.org/10.1186/s12302-018-0132-6.Search in Google Scholar PubMed PubMed Central

Clément, L., Charlotte, H., and Marmier, N. (2013). Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and plants – effects of size and crystalline structure. Chemosphere 90: 1083–1089. https://doi.org/10.1016/j.chemospher.2012.09.013.Search in Google Scholar

Dolenc Koce, J. (2017). Effects of exposure to nano and bulk sized TiO2 and CuO in Lemna minor. Plant Physiol. Biochem. 119: 43–49, https://doi.org/10.1016/j.plaphy.2017.08.014.Search in Google Scholar PubMed

ECB. (2003). Technical guidance document on risk assessment. European Chemicals Bureau, Institute for Health and Consumer Protection, Part II, European Commission, Dublin.Search in Google Scholar

Gottschalk, F., Sun, T.Y., and Nowack, B. (2013). Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies. Environ. Pollut. 181: 287–300, https://doi.org/10.1016/j.envpol.2013.06.003.Search in Google Scholar PubMed

Heath, R.L. and Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125: 189–198, https://doi.org/10.1016/0003-9861(68)90654-1.Search in Google Scholar

Idrees, S., Shabir, S., Ilyas, N., Batool, N., and Kanwal, S. (2015). Assessment of cadmium on wheat (Triticum aestivum L.) in hydroponics medium. Agrociencia 49: 917–929, https://www.redalyc.org/articulo.oa?id=30243055008.Search in Google Scholar

Jiang, H.S., Qiu, X.N., Li, G.B., Li, W., and Yin, L.Y. (2014). Silver nanoparticles induced accumulation of reactive oxygen species and alteration of antioxidant systems in the aquatic plant Spirodela polyrhiza. Environ. Toxicol. Chem. 33: 1394–1405, https://doi.org/10.1002/etc.2577.Search in Google Scholar PubMed

Khosravi, K., Hoque, M.E., Dimock, B., Hintelmann, H., and Metcalfe, C.D. (2012). A novel approach for determining total titanium from titanium dioxide nanoparticles suspended in water and biosolids by digestion with ammonium persulfate. Anal. Chim. Acta 713: 86–91, https://doi.org/10.1016/j.aca.2011.11.048.Search in Google Scholar PubMed

Kourtidou, D., Chaliampalias, D., Vogiatzis, C., Tarani, E., Kamou, A., Pavlidou, E., Skolianos, S., Chrissafis, K., and Vourlias, G. (2019). Deposition of Ni-Al coatings by pack cementation and corrosion resistance in high temperature and marine environments. Corrosion Sci. 148: 12–23, https://doi.org/10.1016/j.corsci.2018.11.003.Search in Google Scholar

Kurepa, J., Paunesku, T., Vogt, S., Arora, H., Rabatic, B.M., Lu, J., Wanzer, M.B., Woloschak, G.E., and Smalle, J.A. (2010). Uptake and distribution of ultrasmall anatase TiO2 alizarin red S nanoconjugates in Arabidopsis thalliana. Nano Lett. 10: 2296–2302, https://doi.org/10.1021/nl903518f.Search in Google Scholar PubMed PubMed Central

Llagostera, I., Dervantes, C., Nanmartí, S., Romero, J., and Pérez, M. (2016). Effects of copper exposure on photosynthesis and growth of the seagrass Cymodocea nodosa: an experimental assessment. Bull. Environ. Contam. Toxicol. 97: 374–379, https://doi.org/10.1007/s00128-016-1863-y.Search in Google Scholar PubMed

Malea, P., Adamakis, I.-D.S., and Kevrekidis, T. (2013). Microtubule integrity and cell viability under metal (Cu, Ni, Cr) stress in the seagrass Cymodocea nodosa. Chemosphere 93: 1035–1042, https://doi.org/10.1016/j.chemosphere.2013.05.074.Search in Google Scholar PubMed

Malea, P., Adamakis, I.-D.S., and Kevrekidis, T. (2014). Effects of lead uptake on microtubule cytoskeleton organization and cell viability in the seagrass Cymodocea nodosa. Ecotoxicol. Environ. Saf. 104: 175–181, https://doi.org/10.1016/j.ecoenv.2014.03.005.Search in Google Scholar PubMed

Malea, P., Kokkinidi, D., Kevrekidou, A., and Adamakis, I.-D.S. (2020). Environmentally relevant bisphenol A concentrations effects on the seagrass Cymodocea nodosa different part elongation: perceptive assessors of toxicity. Environ. Sci. Pollut. Res. 27: 7267–7279, https://doi.org/10.1007/s11356-019-07443-6.Search in Google Scholar PubMed

Morelli, E., Gabelliere, E., Bornomini, A., Tognotti, D., Grassi, G., and Corsi, I. (2018). TiO2 nanoparticles in seawater: aggregation and interactions with the green alga Dunaliella tertiolecta. Ecotoxicol. Environ. Saf. 148: 184–193, https://doi.org/10.1016/j.ecoenv.2017.10.024.Search in Google Scholar PubMed

Movafeghi, A., Khataee, A., Abedi, M., Tarrahi, R., Dadpour, M., and Vafaei, F. (2018). Effects of TiO2 nanoparticles on the aquatic plant Spirodela polyrrhiza: evaluation of growth parameters, pigment contents and antioxidant enzyme activities. J. Environ. Sci. 64: 130–138, https://doi.org/10.1016/j.jes.2016.12.020.Search in Google Scholar PubMed

Mylona, Z., Panteris, E., Kevrekidis, T., and Malea, P. (2020a). Silver nanoparticle toxicity effect on the seagrass Halophila stipulacea. Ecotoxicol. Environ. Saf. 189: 109925, https://doi.org/10.1016/j.ecoenv.2019.109925.Search in Google Scholar PubMed

Mylona, Z., Panteris, E., Kevrekidis, T., and Malea, P. (2020b). Effects of titanium dioxide nanoparticles on leaf cell structure and viability, and leaf elongation in the seagrass Halophila stipulacea. Sci. Total Environ. 719: 137378, https://doi.org/10.1016/j.scitotenv.2020.137378.Search in Google Scholar PubMed

Mylona, Z., Panteris, E., Moustakas, M., Kevrekidis, T., and Malea, P. (2020c). Physiological, structural and ultrastructural impacts of silver nanoparticles on the seagrass Cymodocea nodosa. Chemosphere 248: 126066, https://doi.org/10.1016/j.chemosphere.2020.126066.Search in Google Scholar PubMed

Nakano, Y. and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22: 867–880, https://doi.org/10.1093/oxfordjournals.pcp.a076232.Search in Google Scholar

Navarro, E., Baun, A., Behra, R., Hartmann, N.B., Filser, J., Miao, A.-J., Quigg, A., Santschi, P.H., and Sigg, L. (2008). Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17: 372–386, https://doi.org/10.1007/s10646-008-0214-0.Search in Google Scholar PubMed

Okupnik, A. and Pflugmacher, S. (2016). Oxidative stress response of the aquatic macrophyte Hydrilla verticillate exposed to TiO2 nanoparticles. Environ. Toxicol. Chem. 35: 2859–2866, https://doi.org/10.1002/etc.3469.Search in Google Scholar PubMed

Orlando-Bonaca, M., Francé, J., Mavrič, B., Grego, M., Lipej, L., Flander-Putrle, V., Šiško, M., and Falace, A. (2015). A new index (MediSkew) for the assessment of the Cymodocea nodosa (Ucria) Ascherson meadow’s status. Mar. Environ. Res. 110: 132–141, https://doi.org/10.1016/j.marenvres.2015.08.009.Search in Google Scholar PubMed

Panteris, E., Diannelidis, B.-E., and Adamakis, I.-D.S. (2018). Cortical microtubule orientation in Arabidopsis thaliana root meristematic zone depends on cell division and requires severing by katanin. J. Biol. Res. 25: 12, https://doi.org/10.1186/s40709-018-0082-6.Search in Google Scholar PubMed PubMed Central

Rastogi, A., Zivcak, M., Sytar, Q., Kalaji, H.M., He, X., Mbarki, S., and Brestic, M. (2017). Impact of metal and metal oxide nanoparticles on plant: a critical review. Front. Chem. 5, Article 78, https://doi.org/10.3389/fchem.2017.00078.Search in Google Scholar PubMed PubMed Central

Schmidt, R., Kunkowska, A.B., and Schippers, J.H. (2016). Role of reactive oxygen species during cell expansion in leaves. Plant Physiol. 172: 2098–2106, https://doi.org/10.1104/pp.16.00426.Search in Google Scholar

Scown, T.M., Santos, E.M., Johnston, B.D., Gaiser, B., Baalousha, M., Mitov, S., Lead, J.R., Stone, V., Fernandes, T.F., Jepson, M., . (2010). Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol. Sci. 115: 521–535, https://doi.org/10.1093/toxsci/kfq076.Search in Google Scholar

Song, G., Gao, Y., Wu, H., Hou, W., Zhang, C., and Ma, H. (2012). Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environ. Toxicol. Chem. 31: 2147–2152, https://doi.org/10.1002/etc.1933.Search in Google Scholar

Sosan, A., Svistunenko, D., Straltsova, D., Tsiurkina, K., Smolich, I., Lawson, T., Subramaniam, S., Golovko, V., Anderson, D., Sokolik, A., . (2016). Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify the physiology of Arabidopsis thaliana plants. Plant J. 85: 245–257, https://doi.org/10.1111/tpj.13105.Search in Google Scholar

Spalding, M., Taylor, M., Ravilious, C., Short, F., and Green, E. (2003). The distribution and status of seagrasses. In: Green, E.P. and Short, F. (Eds.). World atlas of seagrasses. University California Press, London, pp. 5–26.Search in Google Scholar

Spengler, A., Wanninger, L., and Pflugmacher, S. (2017). Oxidative stress mediated toxicity of TiO2 nanoparticles after a concentration and time dependent exposure of the aquatic macrophyte Hydrilla verticillata. Aquat. Toxicol. 190: 32–39, https://doi.org/10.1016/j.aquatox.2017.06.006.Search in Google Scholar

Sun, T.Y., Bornhöft, N., Hungerbühler, K., and Nowack, B. (2016). Dynamic probabilistic modeling of environmental emissions of engineered nanomaterials. Environ. Sci. Technol. 50: 4701–4711, https://doi.org/10.1021/acs.est.5b05828.Search in Google Scholar

Thwala, M., Klaine, S.J., and Musee, N. (2016). Interactions of metal-based engineered nanoparticles with aquatic higher plants: a review of the state of current knowledge. Environ. Toxicol. Chem. 35: 1677–1694, https://doi.org/10.1002/etc.3364.Search in Google Scholar

Vale, G., Mehennaoui, K., Cambier, S., Libralato, G., Jomini, S., and Domingos, R.F. (2016). Manufactured nanoparticles in the aquatic environment-biochemical responses on freshwater organisms: a critical overview. Aquat. Toxicol. 170: 162–174, https://doi.org/10.1016/j.aquatox.2015.11.019.Search in Google Scholar

Volkmann, D. and Baluška, F. (1999). Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc. Res. Tech. 47: 135–154.10.1002/(SICI)1097-0029(19991015)47:2<135::AID-JEMT6>3.0.CO;2-1Search in Google Scholar

Wan, L. and Zhang, H. (2012). Cadmium toxicity: effects on cytoskeleton, vesicular trafficking and cell wall construction. Plant Signal. Behav. 7: 345–348, https://doi.org/10.4161/psb.18992.Search in Google Scholar

Wang, S., Kurepa, J., and Smalle, J.A. (2011). Ultra-small TiO2 nanoparticles disrupt microtubular networks in Arabidopsis thaliana. Plant Cell Environ. 34: 811–820, https://doi.org/10.1111/j.1365-3040.2011.02284.x.Search in Google Scholar PubMed

Wang, N., Hsu, C., Zhu, L., Tseng, S., and Hsu, J.-P. (2013). Influence of metal oxide nanoparticles concentration on their zeta potential. J. Colloid Influence Sci. 407: 22–28, https://doi.org/10.1016/j.jcis.2013.05.058.Search in Google Scholar PubMed

Xia, B., Chen, B., Sun, X., Qu, K., Ma, F., and Du, M. (2015). Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci. Total Environ. 508: 525–533, https://doi.org/10.1016/j.scitotenv.2014.11.066.Search in Google Scholar PubMed

Xu, F. (2018). Review of analytical studies on TiO2 nanoparticles and particle aggregation, coagulation, flocculation, sedimentation, stabilization. Chemosphere 212: 662–677, https://doi.org/10.1016/j.chemosphere.2018.08.108.Search in Google Scholar PubMed

Yan, A. and Chen, Z. (2019). Impacts of silver nanoparticles on plants: a focus on the phytotoxicity and underlying mechanism. Int. J. Mol. Sci. 20: 1003, https://doi.org/10.3390/ijms20051003.Search in Google Scholar PubMed PubMed Central

Zachariadis, M., Quader, H., Galatis, B., and Apostolakos, P. (2001). Endoplasmic reticulum preprophase band in dividing root-tip cells of Pinus brutia. Planta 213: 824–827, https://doi.org/10.1007/s004250100563.Search in Google Scholar PubMed

Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0047).

Received: 2020-07-18
Accepted: 2020-10-06
Published Online: 2020-10-21
Published in Print: 2020-12-16

© 2020 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. In this issue
  3. Physiology and ecology
  4. Physiological and structural responses of the seagrass Cymodocea nodosa to titanium dioxide nanoparticle exposure
  5. Iodine and fluorine concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes
  6. The influence of migratory birds on the distribution of the seagrass Zostera japonica
  7. Taxonomy/phylogeny and biogeography
  8. Molecular analysis confirms Laurenciella marilzae (Rhodophyta, Rhodomelaceae) in the Mediterranean Sea, a species often misidentified as Laurencia dendroidea
  9. Inconclusive evidence of sexual reproduction of invasive Halophila stipulacea: a new field guide to encourage investigation of flower and fruit production throughout its invasive range
  10. Genomics
  11. Superoxide dismutase and ascorbate peroxidase genes in Antarctic endemic brown alga Ascoseira mirabilis (Ascoseirales, Phaeophyceae): data mining of a de novo transcriptome
  12. Chemistry and applications
  13. Monitoring environmental risk of the exotic species Kappaphycus alvarezii (Rhodophyta), after two decades of introduction in southeastern Brazil
  14. Photo-bleached agar extracts from Gracilariopsis heteroclada
https://doi.org/10.1515/bot-2020-0047
Keywords for this article
biomarker; Cymodocea nodosa; cytotoxicity; physiological response; risk assessment

Articles in the same Issue

  1. Frontmatter
  2. In this issue
  3. Physiology and ecology
  4. Physiological and structural responses of the seagrass Cymodocea nodosa to titanium dioxide nanoparticle exposure
  5. Iodine and fluorine concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes
  6. The influence of migratory birds on the distribution of the seagrass Zostera japonica
  7. Taxonomy/phylogeny and biogeography
  8. Molecular analysis confirms Laurenciella marilzae (Rhodophyta, Rhodomelaceae) in the Mediterranean Sea, a species often misidentified as Laurencia dendroidea
  9. Inconclusive evidence of sexual reproduction of invasive Halophila stipulacea: a new field guide to encourage investigation of flower and fruit production throughout its invasive range
  10. Genomics
  11. Superoxide dismutase and ascorbate peroxidase genes in Antarctic endemic brown alga Ascoseira mirabilis (Ascoseirales, Phaeophyceae): data mining of a de novo transcriptome
  12. Chemistry and applications
  13. Monitoring environmental risk of the exotic species Kappaphycus alvarezii (Rhodophyta), after two decades of introduction in southeastern Brazil
  14. Photo-bleached agar extracts from Gracilariopsis heteroclada
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