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Solar UV radiation exacerbates photoinhibition of a diatom by antifouling agents Irgarol 1051 and diuron

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Abstract

Marine diatoms are ubiquitously distributed in both coastal and open oceans, playing an important role in global primary productivity. In coastal waters, they are exposed to various pollutants in addition to multiple environmental stressors. Here, we show the pennate diatom Nitzschia sp. isolated from the East China Sea decreased its photosynthetic performance under the combined influences of two typical marine organic pollutants (Irgarol 1051 and diuron), that are frequently used as biocides to prevent biofouling, and solar UV radiation (UVR). Nitzschia sp. was sensitive to both pollutants under visible light (PAR) without UVR, even at the lowest concentration (0.5 μg L−1) tested; higher levels led to greater reductions in its photochemical yield. When additionally exposed to UVR (280–400 nm), the inhibition of the quantum yields by the antifouling pollutants was exacerbated, reflecting a synergistic impact of the pollutants and UVR. Exposure to UVR brought about 5–20% reduction at different levels of Irgarol 1051, diuron, and their mixture, with a higher reduction percentage due to UVR observed at lower concentrations of the pollutants. Our results indicate that even low levels of antifouling agents can result in significant impacts on diatoms in the presence of solar UVR, implying that combinations of UVR and organic pollutants could be a potential method to control-target algal biofouling.

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References

  • Ali HR, Arifin MM, Sheikh MA, Mohamed Shazili NA, Bachok Z (2013) Occurrence and distribution of antifouling biocide Irgarol-1051 in coastal waters of peninsular Malaysia. Mar Pollut Bull 70:253–257

    Article  CAS  Google Scholar 

  • Ansanelli G, Manzo S, Parrella L, Massanisso P, Chiavarini S, Di Landa G, Ubaldi C, Cannarsa S, Cremisini C (2017) Antifouling biocides (Irgarol, Diuron and dichlofluanid) along the Italian Tyrrhenian coast: temporal, seasonal and spatial threats. Reg Stud Mar Sci 16:254–266

    Article  Google Scholar 

  • Barnes PW, Williamson CE, Lucas RM, Robinson SA, Madronich S, Paul ND, Bornman JF, Bais AF, Sulzberger B, Wilson SR, Andrady AL, McKenzie RL, Neale PJ, Austin AT, Bernhard GH, Solomon KR, Neale RE, Young PJ, Norval M, Rhodes LE, Hylander S, Rose KC, Longstreth J, Aucamp PJ, Ballaré CL, Cory RM, Flint SD, de Gruijl FR, Häder D-P, Heikkilä AM, Jansen MAK, Pandey KK, Robson TM, Sinclair CA, Wängberg S-Å, Worrest RC, Yazar S, Young AR, Zepp RG (2019) Ozone depletion, ultraviolet radiation, climate change and prospects for a sustainable future. Nature Sustainability 2:569–579

    Article  Google Scholar 

  • Barnett A, Meleder V, Blommaert L, Lepetit B, Gaudin P, Vyverman W, Sabbe K, Dupuy C, Lavaud J (2015) Growth form defines physiological photoprotective capacity in intertidal benthic diatoms. ISME J 9:32–45

    Article  CAS  Google Scholar 

  • Basheer C, Tan KS, Lee HK (2002) Organotin and Irgarol-1051 contamination in Singapore coastal waters. Mar Pollut Bull 44:697–703

    Article  CAS  Google Scholar 

  • Bates SS, Hubbard KA, Lundholm N, Montresor M, Leaw CP (2018) Pseudo-nitzschia, Nitzschia, and domoic acid: new research since 2011. Harmful Algae 79:3–43

    Article  Google Scholar 

  • Bonnineau C, Sague IG, Urrea G, Guasch H (2012) Light history modulates antioxidant and photosynthetic responses of biofilms to both natural (light) and chemical (herbicides) stressors. Ecotoxicology 21:1208–1224

    Article  CAS  Google Scholar 

  • Buma AGJ, Sjollema SB, van de Poll WH, Klamer HJC, Bakker JF (2009) Impact of the antifouling agent Irgarol 1051 on marine phytoplankton species. J Sea Res 61:133–139

    Article  CAS  Google Scholar 

  • Carstensen J, Klais R, Cloern JE (2015) Phytoplankton blooms in estuarine and coastal waters: seasonal patterns and key species. Estuar Coast Shelf Sci 162:98–109

  • Cerino F, Orsini L, Sarno D, Dell’Aversano C, Tartaglione L, Zingone A (2005) The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae. Harmful Algae 4:33–48

    Article  CAS  Google Scholar 

  • Chesworth JC, Donkin ME, Brown MT (2004) The interactive effects of the antifouling herbicides Irgarol 1051 and Diuron on the seagrass Zostera marina (L.). Aquat Toxicol 66:293–305

    Article  CAS  Google Scholar 

  • Connelly DP, Readman JW, Knap AH, Davies J (2001) Contamination of the coastal waters of Bermuda by organotins and the triazine herbicide Irgarol 1051. Mar Pollut Bull 42:409–414

    Article  CAS  Google Scholar 

  • Diepens NJ, Buffan-Dubau E, Budzinski H, Kallerhoff J, Merlina G, Silvestre J, Auby I, Nathalie T, Elger A (2017) Toxicity effects of an environmental realistic herbicide mixture on the seagrass Zostera noltei. Environ Pollut 222:393–403

    Article  CAS  Google Scholar 

  • Eriksson KM, Clarke AK, Franzen LG, Kuylenstierna M, Martinez K, Blanck H (2009) Community-level analysis of psbA gene sequences and Irgarol tolerance in marine periphyton. Appl Environ Microbiol 75:897–906

    Article  CAS  Google Scholar 

  • Evans SM, Birchenough AC, Brancatoà MS (2000) The TBT ban: out of the frying pan into the fire? Mar Pollut Bull 40:204–211

    Article  CAS  Google Scholar 

  • Fernández-Alba AR, Hernando MD, Piedra L, Chisti Y (2002) Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal Chim Acta:303–312

  • Gallucci F, Castro IB, Perina FC, Souza Abessa DM, Paula Teixeira A (2015) Ecological effects of Irgarol 1051 and Diuron on a coastal meiobenthic community: a laboratory microcosm experiment. Ecol Indic 58:21–31

    Article  Google Scholar 

  • Gao X, Song J (2005) Phytoplankton distributions and their relationship with the environment in the Changjiang Estuary, China. Mar Pollut Bull 50:327–335

    Article  CAS  Google Scholar 

  • Gao X, Song J (2006) Main geochemical characteristics and key biogeochemical carbon processes in the East China Sea. J Coast Res 226:1330–1339

    Article  Google Scholar 

  • Gao K, Beardall J, Häder D-P, Hall-Spencer JM, Gao G, Hutchins DA (2019) Effects of ocean acidification on marine photosynthetic organisms under the concurrent influences of warming, UV radiation, and deoxygenation. Front Mar Sci 6

  • Gatidou G, Thomaidis NS (2007) Evaluation of single and joint toxic effects of two antifouling biocides, their main metabolites and copper using phytoplankton bioassays. Aquat Toxicol 85:184–191

    Article  CAS  Google Scholar 

  • Heraud P, Beardall J (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth Res 63:123–134

  • Hirayama K, Takayama K, Haruta S, Ishibashi H, Takeuchi I (2017) Effect of low concentrations of Irgarol 1051 on RGB (R, red; G, green; B, blue) colour values of the hard-coral Acropora tenuis. Mar Pollut Bull 124:678–686

    Article  CAS  Google Scholar 

  • Jones RJ, Kerswell AP (2003) Phytotoxicity of photosystem II (PSII) herbicides to coral. Mar Ecol Prog Ser 261:149–159

    Article  CAS  Google Scholar 

  • Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12:95–104

    Article  CAS  Google Scholar 

  • Klais R, Cloern JE, Harrison PJ (2015) Resolving variability of phytoplankton species composition and blooms in coastal ecosystems. Estuar Coast Shelf S 162:4–6

    Article  Google Scholar 

  • Kottuparambil S, Brown MT, Park J, Choi S, Lee H, Choi H-G, Depuydt S, Han T (2017) Comparative assessment of single and joint effects of diuron and Irgarol 1051 on Arctic and temperate microalgae using chlorophyll a fluorescence imaging. Ecol Indic 76:304–316

    Article  CAS  Google Scholar 

  • Lambert SJ, Thomas KV, Davy AJ (2006) Assessment of the risk posed by the antifouling booster biocides Irgarol 1051 and diuron to freshwater macrophytes. Chemosphere 63:734–743

    Article  CAS  Google Scholar 

  • Landoulsi J, Cooksey KE, Dupres V (2011) Review – interactions between diatoms and stainless steel: focus on biofouling and biocorrosion. Biofouling 27:1105–1124

    Article  CAS  Google Scholar 

  • Larras F, Montuelle B, Bouchez A (2013) Assessment of toxicity thresholds in aquatic environments: does benthic growth of diatoms affect their exposure and sensitivity to herbicides? Sci Total Environ 463-464:469–477

    Article  CAS  Google Scholar 

  • Laviale M, Prygiel J, Créach A (2010) Light modulated toxicity of isoproturon toward natural stream periphyton photosynthesis: a comparison between constant and dynamic light conditions. Aquat Toxicol 97:334–342

    Article  CAS  Google Scholar 

  • Liu K-K, Chao S-Y, Lee H-J, Gong G-C, Teng Y-C (2010) Seasonal variation of primary productivity in the East China Sea: a numerical study based on coupled physical-biogeochemical model. Deep-Sea Res II 57:1762–1782

    Article  CAS  Google Scholar 

  • Magnusson M, Heimann K, Ridd M, Negri AP (2012) Chronic herbicide exposures affect the sensitivity and community structure of tropical benthic microalgae. Mar Pollut Bull 65:363–372

    Article  CAS  Google Scholar 

  • McCarthy A, Rogers SP, Duffy SJ, Campbell DA (2012) Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta). J Phycol 48:635–646

  • Montzka SA, Dutton GS, Yu P, Ray E, Portmann RW, Daniel JS, Kuijpers L, Hall BD, Mondeel D, Siso C, Nance JD, Rigby M, Manning AJ, Hu L, Moore F, Miller BR, Elkins JW (2018) An unexpected and persistent increase in global emissions of ozone-depleting CFC-11. Nature 557:413–417

    Article  CAS  Google Scholar 

  • Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL (2000) Fate and ecotoxicity of the new antifouling compound Irgarol 1051 in the aquatic environment. Water Res 34:3523–3530

  • Owen R, Knap A, Toaspern M, Carbery K (2002) Inhibition of coral photosynthesis by the antifouling herbicide Irgarol 1051. Mar Pollut Bull 44:623–632

    Article  CAS  Google Scholar 

  • Soroldoni S, Abreu F, Castro ÍB, Duarte FA, Pinho GLL (2017) Are antifouling paint particles a continuous source of toxic chemicals to the marine environment? J Hazard Mater 330:76–82

    Article  CAS  Google Scholar 

  • Turner A (2010) Marine pollution from antifouling paint particles. Mar Pollut Bull 60:159–171

    Article  CAS  Google Scholar 

  • Underwood GJC, Phillips J, Saunders K (1998) Distribution of estuarine benthic diatom species along salinity and nutrient gradients. Eur J Phycol 33:173–183

    Article  Google Scholar 

  • Wang L, Wang Y, Xu C, An Z, Wang S (2011) Analysis and evaluation of the source of heavy metals in water of the river Changjiang. Environ Monit Assess 173:301–313

    Article  CAS  Google Scholar 

  • Wang B, Chen J, Jin H, Li H, Huang D, Cai W-J (2017) Diatom bloom-derived bottom water hypoxia off the Changjiang Estuary, with and without typhoon influence. Limnol Oceanogr 62:1552–1569

    Article  CAS  Google Scholar 

  • Wu Y, Zhu Y, Xu J (2017) High salinity and UVR synergistically reduce the photosynthetic performance of an intertidal benthic diatom. Mar Environ Res 130:258–263

    Article  CAS  Google Scholar 

  • Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104

    Article  CAS  Google Scholar 

  • Zamora-Ley IM, Gardinali PR, Jochem FJ (2006) Assessing the effects of Irgarol 1051 on marine phytoplankton populations in Key Largo Harbor, Florida. Mar Pollut Bull 52:935–941

    Article  CAS  Google Scholar 

  • Zhu Z-Y, Ng W-M, Liu S-M, Zhang J, Chen J-C, Wu Y (2009) Estuarine phytoplankton dynamics and shift of limiting factors: a study in the Changjiang (Yangtze River) estuary and adjacent area. Estuar Coast Shelf Sci 84:393-401

  • Zhu Z, Wu Y, Xu J, Beardall J (2019) High copper and UVR synergistically reduce the photochemical activity in the marine diatom Skeletonema costatum. J Photochem Photobiol B 192:97–102

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Professor John Beardall for his linguistic assistance.

Funding

This research was funded by Natural Science Foundation of Jiangsu Province of China (BK20181314), Natural Science Foundation of China (41876113). and the Fundamental Research Funds for the Central Universities (2019B18614).

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Authors and Affiliations

  1. Institute of Marine Biology, College of Oceanography, Hohai University, Nanjing, 210098, China

    Rui Hou & Yaping Wu

  2. College of Marine Life and Fisheries, Jiangsu Ocean University, Lianyungang, 222005, China

    Yaping Wu & Juntian Xu

  3. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361005, China

    Kunshan Gao

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  1. Rui Hou
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  2. Yaping Wu
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Correspondence to Yaping Wu.

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Hou, R., Wu, Y., Xu, J. et al. Solar UV radiation exacerbates photoinhibition of a diatom by antifouling agents Irgarol 1051 and diuron. J Appl Phycol 32, 1243–1251 (2020). https://doi.org/10.1007/s10811-020-02048-w

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  • DOI: https://doi.org/10.1007/s10811-020-02048-w

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