The inhibitory effects of the antifouling compound Irgarol 1051 on the marine diatom Skeletonema sp. across a broad range of photosynthetically active radiation.
Inhibition
Irgarol
Photosynthesis
Skeletonema sp.
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
22
12
2020
accepted:
22
04
2021
pubmed:
29
4
2021
medline:
4
9
2021
entrez:
28
4
2021
Statut:
ppublish
Résumé
The release of anthropogenic organic pollutants has resulted in extensive environmental risks to coastal waters. Among pollutants released, the most common antifoulant, Irgarol 1051, is an effective inhibitor of photosystem II of photoautotrophs; thus, the continuous release of this compound into surrounding seawater would potentially threaten marine algae. To investigate this, we grew the model marine diatom Skeletonema sp. at different concentrations of Irgarol 1051 and levels of photosynthetically active radiation (PAR). Irgarol did not affect the photochemical capacity when cells were incubated in the dark, but photochemical yields all significantly decreased, and relative inhibition by Irgarol increased once cells were exposed to even the lowest PAR, with lower photochemical yields observed under increased level of Irgarol. In addition, the rate of decrease in yield increased with Irgarol concentration but was unchanged among PAR treatments. The growth rates showed a similar pattern to photochemical yields, with lower values under higher Irgarol concentrations, but with no significant differences in the effect of Irgarol observed between the light levels employed. The ratio of repair to damage rates of PSII clearly shows that this ratio decreased with light intensity, largely due to increases in damage rates and that the PAR level at which repair balanced damage decreased under a high level of Irgarol. Our results suggest that the inhibitory effects of Irgarol become obvious after PAR exposure even at a relatively low light level, suggesting that Irgarol would affect phytoplankton throughout the daytime, and may therefore have a broad environmental risk, potentially limiting coastal primary production.
Identifiants
pubmed: 33909247
doi: 10.1007/s11356-021-14135-7
pii: 10.1007/s11356-021-14135-7
doi:
Substances chimiques
Triazines
0
Water Pollutants, Chemical
0
irgarol 1051
28159-98-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
48535-48542Subventions
Organisme : National Natural Science Foundation of China
ID : 41876113
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20181314
Organisme : Postgraduate Research & Practice Innovation Program of Jiangsu Province
ID : KYCX19-2285
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abrantes F, Cermeno P, Lopes C, Romero O, Matos L, Van Iperen J, Rufino M, Magalhães V (2016) Diatoms Si uptake capacity drives carbon export in coastal upwelling systems. Biogeosciences 13:4099–4109
doi: 10.5194/bg-13-4099-2016
Babin M, Morel A, Fournier-Sicre V, Fell F, Stramski D (2003) Light scattering properties of marine particles in coastal and open ocean waters as related to the particle mass concentration. Limnol Oceanogr 48:843–859
doi: 10.4319/lo.2003.48.2.0843
Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
doi: 10.1016/0968-0004(92)90503-2
Basheer C, Tan KS, Lee HK (2002) Organotin and Irgarol-1051 contamination in Singapore coastal waters. Mar Pollut Bull 44:697–703
doi: 10.1016/S0025-326X(01)00330-7
Bérard A, Leboulanger C, Pelte T (1999) Tolerance of Oscillatoria limnetica Lemmermann to atrazine in natural phytoplankton populations and in pure culture: influence of season and temperature. Arch Environ Contam Toxicol 37:472–479
doi: 10.1007/s002449900541
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
doi: 10.1016/j.seares.2008.11.007
Campbell DA, Serôdio J (2020) Photoinhibition of photosystem II in phytoplankton: processes and patterns. In: Larkum AWD, Grossmann AR, Raven JA (eds) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Springer International Publishing, Cham, pp 329–365
doi: 10.1007/978-3-030-33397-3_13
Campbell DA, Tyystjarvi E (2012) Parameterization of photosystem II photoinactivation and repair. BBA-Bioenergetics 1817:258–265
doi: 10.1016/j.bbabio.2011.04.010
Campbell DA, Hossain Z, Cockshutt AM, Zhaxybayeva O, Wu HY, Li G (2013) Photosystem II protein clearance and FtsH function in the diatom Thalassiosira pseudonana. Photosynth Res 115:43–54
doi: 10.1007/s11120-013-9809-2
Chaffin JD, Davis TW, Smith DJ, Baer MM, Dick GJ (2018) Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production. Harmful Algae 73:84–97
doi: 10.1016/j.hal.2018.02.001
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
doi: 10.1016/j.aquatox.2003.10.002
Edwards KF, Thomas MK, Klausmeier CA, Litchman E (2015) Light and growth in marine phytoplankton: allometric, taxonomic, and environmental variation. Limnol Oceanogr 60:540–552
doi: 10.1002/lno.10033
Edwards KF, Thomas MK, Klausmeier CA, Litchman E (2016) Phytoplankton growth and the interaction of light and temperature: a synthesis at the species and community level. Limnol Oceanogr 61:1232–1244
doi: 10.1002/lno.10282
Falkowski PG, Raven JA (2013) Aquatic photosynthesis. Princeton University Press, New York
doi: 10.1515/9781400849727
Fernandez MV, Gardinali PR (2016) Risk assessment of triazine herbicides in surface waters and bioaccumulation of Irgarol and M1 by submerged aquatic vegetation in Southeast Florida. Sci Total Environ 541:1556–1571
doi: 10.1016/j.scitotenv.2015.09.035
Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877
doi: 10.4319/lo.1999.44.3_part_2.0864
Gallo M, Morse D, Hollnagel HC, Barros MP (2020) Oxidative stress and toxicology of Cu
doi: 10.1016/j.aquatox.2020.105450
Gatley-Montross CM, Finlay JA, Aldred N, Cassady H, Destino JF, Orihuela B, Hickner MA, Clare AS, Rittschof D, Holm ER, Detty MR (2017) Multivariate analysis of attachment of biofouling organisms in response to material surface characteristics. Biointerphases 12:12
doi: 10.1116/1.5008988
Guan WC, Gao KS (2010) Impacts of UV radiation on photosynthesis and growth of the coccolithophore Emiliania huxleyi (Haptophyceae). Environ Exp Bot 67:502–508
doi: 10.1016/j.envexpbot.2009.08.003
Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239
doi: 10.1139/m62-029
Haynes D, Christie C, Marshall P, Dobbs K (2002) Antifoulant concentrations at the site of the Bunga Teratai Satu grounding, Great Barrier Reef, Australia. Mar Pollut Bull 44:968–972
doi: 10.1016/S0025-326X(02)00114-5
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
doi: 10.1023/A:1006319802047
Hou R, Wu YP, Xu JT, Gao KS (2020) Solar UV radiation exacerbates photoinhibition of a diatom by antifouling agents Irgarol 1051 and diuron. J Appl Phycol 32:1243–1251
doi: 10.1007/s10811-020-02048-w
Jimbo H, Izuhara T, Hihara Y, Hisabori T, Nishiyama Y (2019) Light-inducible expression of translation factor EF-Tu during acclimation to strong light enhances the repair of photosystem II. Proc Natl Acad Sci 116:21268–21273
doi: 10.1073/pnas.1909520116
Kaiser E, Galvis VC, Armbruster U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast’s perspective. Biochem J 476:2725–2741
doi: 10.1042/BCJ20190134
Kamei M, Takayama K, Ishibashi H, Takeuchi I (2020) Effects of ecologically relevant concentrations of Irgarol 1051 in tropical to subtropical coastal seawater on hermatypic coral Acropora tenuis and its symbiotic dinoflagellates. Mar Pollut Bull 150:110734
doi: 10.1016/j.marpolbul.2019.110734
Knauert S, Escher B, Singer H, Hollender J, Knauer K (2008) Mixture toxicity of three photosystem II inhibitors (atrazine, isoproturon, and diuron) toward photosynthesis of freshwater phytoplankton studied in outdoor mesocosms. Environ Sci Technol 42:6424–6430
doi: 10.1021/es072037q
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
doi: 10.1016/j.ecolind.2017.01.024
Li H, Xu T, Ma J, Li F, Xu J (2021) Physiological responses of Skeletonema costatum to the interactions of seawater acidification and the combination of photoperiod and temperature. Biogeosciences 18:1439–1449
doi: 10.5194/bg-18-1439-2021
Luhtala H, Kulha N, Tolvanen H, Kalliola R (2016) The effect of underwater light availability dynamics on benthic macrophyte communities in a Baltic Sea archipelago coast. Hydrobiologia 776:277–291
doi: 10.1007/s10750-016-2759-x
McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483
doi: 10.1021/cr0204294
Mohr S, Schröder H, Feibicke M, Berghahn R, Arp W, Nicklisch A (2008) Long-term effects of the antifouling booster biocide Irgarol 1051 on periphyton, plankton and ecosystem function in freshwater pond mesocosms. Aquat Toxicol 90:109–120
doi: 10.1016/j.aquatox.2008.08.004
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
doi: 10.1016/S0043-1354(00)00095-6
Ross JJ, Ailsa PK (2003) Phytotoxicity of photosystem II (PSII) herbicides to coral. Mar Ecol Prog Ser 261:149–159
doi: 10.3354/meps261149
Sabbah S, Shashar N (2007) Light polarization under water near sunrise. J Opt Soc Am A 24:2049–2056
doi: 10.1364/JOSAA.24.002049
Sapozhnikova Y, Wirth E, Schiff K, Fulton M (2013) Antifouling biocides in water and sediments from California marinas. Mar Pollut Bull 69:189–194
doi: 10.1016/j.marpolbul.2013.01.039
Smedbol E, Lucotte M, Labrecque M, Lepage L, Juneau P (2017) Phytoplankton growth and PSII efficiency sensitivity to a glyphosate-based herbicide (Factor 540 (R)). Aquat Toxicol 192:265–273
doi: 10.1016/j.aquatox.2017.09.021
Sun HW, Dai SG, Huang GL (2001) Bioaccumulation of butyltins via an estuarine food chain. Water Air Soil Pollut 125:55–68
doi: 10.1023/A:1005255713030
Tasmin R, Shimasaki Y, Tsuyama M, Qiu X, Khalil F, Okino N, Yamada N, Fukuda S, Kang I-J, Oshima Y (2014) Elevated water temperature reduces the acute toxicity of the widely used herbicide diuron to a green alga, Pseudokirchneriella subcapitata. Environ Sci Pollut R 21:1064–1070
doi: 10.1007/s11356-013-1989-y
van de Poll WH, Buma AGJ, Visser RJW, Janknegt PJ, Villafane VE, Helbling EW (2010) Xanthophyll cycle activity and photosynthesis of Dunaliella tertiolecta (Chlorophyceae) and Thalassiosira weissflogii (Bacillariophyceae) during fluctuating solar radiation. Phycologia 49:249–259
doi: 10.2216/PH-08-83.1
Van de Waal DB, Litchman E (2020) Multiple global change stressor effects on phytoplankton nutrient acquisition in a future ocean. Philos Trans R Soc B Biol Sci 375:8
Wagner H, Jakob T, Lavaud J, Wilhelm C (2016) Photosystem II cycle activity and alternative electron transport in the diatom Phaeodactylum tricornutum under dynamic light conditions and nitrogen limitation. Photosynth Res 128:151–161
doi: 10.1007/s11120-015-0209-7
Wang N, Wang YP, Duan XY, Wan JQ, Xie YQ, Dong C, Gao JH, Yin P (2020) Controlling factors for the distribution of typical organic pollutants in the surface sediment of a macrotidal bay. Environ Sci Pollut R: 27:28276–28287
doi: 10.1007/s11356-020-09199-w
Wu Y, Yue F, Xu J, Beardall J (2017) Differential photosynthetic response of marine planktonic and benthic diatoms to ultraviolet radiation under various temperature regimes. Biogeosciences 14:5029–5037
doi: 10.5194/bg-14-5029-2017
Wu Y, Zhang M, Li Z, Xu J, Beardall J (2020) Differential responses of growth and photochemical performance of marine diatoms to ocean warming and high light irradiance. Photochem Photobiol 96:1074–1082
doi: 10.1111/php.13268
Yang L, Li H, Zhang Y, Jiao N (2019) Environmental risk assessment of triazine herbicides in the Bohai Sea and the Yellow Sea and their toxicity to phytoplankton at environmental concentrations. Environ Int 133:105175
doi: 10.1016/j.envint.2019.105175
Zhang AQ, Zhou G-J, Lam MHW, Leung KMY (2019) Toxicities of the degraded mixture of Irgarol 1051 to marine organisms. Chemosphere 225:565–573
doi: 10.1016/j.chemosphere.2019.03.038
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 Biol 192:97–102
doi: 10.1016/j.jphotobiol.2019.01.016