Abstract
Variations of temperature and photoperiod throughout different seasons can affect aquatic communities such as biofilms. Biofilms, generally present at the base of trophic chains in freshwaters, are also subject to organic contamination, and are especially affected by herbicides. Many studies have investigated the effect and interactions of herbicides and environmental factors on biofilms, but never with a toxicokinetic point of view. The objective of this study was to assess structural and functional changes in biofilms exposed to diuron, and to link them with contaminant accumulation, under the influence of temperature and light variations. To this aim, biofilms were exposed to all possible combinations of three concentrations (0, 5 and 50 µg L−1) of diuron, two temperatures (10 and 26 °C), and two light/dark photoperiods (16/8, 10/14), for durations of 0, 1 and 3 days. Diuron accumulation in biofilms was quantified and structural descriptors (protein and polysaccharide contents, dry weight) and functional endpoints (photosynthetic and enzymatic activities) were analyzed. The results obtained mainly highlighted the influence of temperature on diuron bioaccumulation and the associated toxic impact on biofilms. Bioaccumulation in biofilms exposed during three days at 10 °C, at the highest diuron concentration, was in average 1.4 times higher than bioaccumulation on biofilms exposed to 26 °C. Accordingly, the photosynthetic yield was more inhibited at lower than at higher temperatures. Temperature was also the highest impacting factor for metabolism regulation; for example, at 26 °C after three days of exposure, polysaccharide production was boosted under both photoperiods tested.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilera A, Souza-Egipsy V, Martín-Úriz PS, Amils R (2008a) Extraction of extracellular polymeric substances from extreme acidic microbial biofilms. Appl Microbiol Biotechnol 78(6):1079–1088. https://doi.org/10.1007/s00253-008-1390-9
Aguilera A, Souza-Egipsy V, San Martín-Úriz P, Amils R (2008b) Extracellular matrix assembly in extreme acidic eukaryotic biofilms and their possible implications in heavy metal adsorption. Aquat Toxicol 88(4):257–266. https://doi.org/10.1016/j.aquatox.2008.04.014
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 Contamination Toxicol 37(4):472–479. https://doi.org/10.1007/s002449900541
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brown JH, Gilloolly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85(7):1771–1789. https://doi.org/10.2106/JBJS.J.01311
Chalifour A, Arts MT, Kainz MJ, Juneau P (2014) Combined effect of temperature and bleaching herbicides on photosynthesis, pigment and fatty acid composition of Chlamydomonas reinhardtii. Eur J Phycol 49(4):508–515. https://doi.org/10.1080/09670262.2014.977962
Chaumet B, Morin S, Hourtané O, Artigas J, Delest B, Eon M, Mazzella N (2019) Flow conditions influence diuron toxicokinetics and toxicodynamics in freshwater biofilms. Sci Total Environ 652:1242–1251. https://doi.org/10.1016/j.scitotenv.2018.10.265
Dauta A (1982) Conditions de développement du phytoplancton. Etude comparative du comportement de huit espèces en culture. II. Rôle des nutriments: assimilation et stockage intracellulaire. Annales de Limnologie 18(3):263–292. https://doi.org/10.1051/limn/1982014
DeLorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic microorganisms: a review. Environ Toxicol Chem 20(1):84–98. https://doi.org/10.1002/etc.5620200108
Dodds WK, Hutson RE, Eichem AC, Evans MA, Gudder DA, Fritz KM, Gray L (1996) The relationship of floods, drying, flow and light to primary production and producer biomass in a prairie stream. Hydrobiologia 333(3):151–159. https://doi.org/10.1007/BF00013429
Draber W, Tietjen K, Kluth JF, Trebst A (1991) Herbicides in photosynthesis research. Angew Chem Int Ed Engl 30(12):1621–1633. https://doi.org/10.1002/anie.199116211
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017
Duong TT, Morin S, Coste M, Herlory O, Feurtet-Mazel A, Boudou A (2010) Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. Sci Total Environ 408(3):552–562. https://doi.org/10.1016/j.scitotenv.2009.10.015
Edwards SJ, Kjellerup BV (2013) Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl Microbiol Biotechnol 97(23):9909–9921. https://doi.org/10.1007/s00253-013-5216-z
Flemming H-C, Neu TR, Wozniak DJ (2007) The EPS matrix: The “House of Biofilm Cells”. J Bacteriol 189(22):7945–7947. https://doi.org/10.1128/JB.00858-07
Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. https://doi.org/10.1038/nrmicro2415
Gomes MP, Juneau P (2017) Temperature and light modulation of herbicide toxicity on algal and cyanobacterial physiology. Front Environ Sci 5:1–17. https://doi.org/10.3389/fenvs.2017.00050
Guasch H, Artigas J, Bonet B, Bonnineau C, Canals O, Corcoll N, Foulquier A, López-Doval J, Kim-Tiam S, Morin S, Navarro E, Pesce S, Proia L, Salvadó H, Serra A (2016) The use of biofilms to assess the effects of chemicals on freshwater ecosystems. In: Romaní AM, Guasch H, Balaguer D (eds), Aquatic biofilms: ecology, water quality and wastewater treatment. Vol 53. Caister Academic Press, UK. p 160. https://doi.org/10.1017/CBO9781107415324.004
Herzig R, Dubinsky Z (1992) Photoacclimation, photosynthesis, and growth in phytoplankton. Isr J Bot 41(4–6):199–212. https://doi.org/10.1080/0021213X.1992.10677227
Kim Tiam S, Fauvelle V, Morin S, Mazzella N (2016) Improving toxicity assessment of pesticide mixtures: the use of polar passive sampling devices extracts in microalgae toxicity tests. Front Microbiol 7:1388. https://doi.org/10.3389/fmicb.2016.01388
Kim Tiam S, Laviale M, Feurtet-Mazel A, Jan G, Gonzalez P, Mazzella N, Morin S (2015) Herbicide toxicity on river biofilms assessed by pulse amplitude modulated (PAM) fluorometry. Aquat Toxicol 165:160–171. https://doi.org/10.1016/j.aquatox.2015.05.001
Kohusova K, Havel L, Vlasak P, Tonika J (2011) A long-term survey of heavy metals and specific organic compounds in biofilms, sediments, and surface water in a heavily affected river in the Czech Republic. Environ Monit Assess 174(1–4):555–572. https://doi.org/10.1007/s10661-010-1478-4
Larras F, Lambert A, Pesce S, Rimet F, Bouchez A, Montuelle B (2013) The effect of temperature and a herbicide mixture on freshwater periphytic algae. Ecotoxicol Environ Saf 98:162–170. https://doi.org/10.1016/j.ecoenv.2013.09.007
Lurling M, Eshetu F, Faassen E, Kosten S, Huszar, V (2012) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol. https://doi.org/10.1111/j.1365-2427.2012.02866.x
Pesce S, Bouchez A, Montuelle B (2011) Effects of organic herbicides on phototrophic microbial communities in freshwater ecosystems. Rev Environ Contamination Toxicol 214:87–124. https://doi.org/10.1007/978-1-4614-0668-6
Proia L, Cassió F, Pascoal C, Tlili A, Romaní AM (2012) The use of attached microbial communities to assess ecological risks of pollutants in river ecosystems: the role of heterotrophs. Handb Environ Chem 19:55–83
Proia L, Morin S, Peipoch M, Romaní AM, Sabater S (2011) Resistance and recovery of river biofilms receiving short pulses of triclosan and diuron. Sci Total Environ 409(17):3129–3137. https://doi.org/10.1016/j.scitotenv.2011.05.013
Romaní AM, Fund K, Artigas J, Schwartz T, Sabater S, Obst U (2008) Relevance of polymeric matrix enzymes during biofilm formation. Microb Ecol 56(3):427–436. https://doi.org/10.1007/s00248-007-9361-8
Romanı A, Giorgi A, Acuna V, Sabater S (2004) The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnol Oceanogr 49(5):1713–1721
Staehr P, Sand-Jensen K (2006) Seasonal changes in temperature and nutrient control of photosynthesis, respiration and growth of natural phytoplankton communities. Freshw Biol 51(2):249–262. https://doi.org/10.1111/j.1365-2427.2005.01490.x
Tasmin R, Shimasaki Y, Tsuyama M, Qiu X, Khalil F, Okino N, Yamada N, Fukuda S, Kang IJ, 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 Res 21(2):1064–1070. https://doi.org/10.1007/s11356-013-1989-y
Tlili A, Dorigo U, Montuelle B, Margoum C, Carluer N, Gouy V, Bouchez A, Bérard A (2008) Responses of chronically contaminated biofilms to short pulses of diuron. An experimental study simulating flooding events in a small river. Aquat Toxicol 87(4):252–263. https://doi.org/10.1016/j.aquatox.2008.02.004
Villeneuve A, Bouchez A, Montuelle B (2011) In situ interactions between the effects of season, current velocity and pollution on a river biofilm. Freshw Biol 2245–2259. https://doi.org/10.1111/j.1365-2427.2011.02649.x
Villeneuve A, Montuelle B, Bouchez A (2010) Influence of slight differences in environmental conditions (light, hydrodynamics) on the structure and function of periphyton. Aquat Sci 33–44. https://doi.org/10.1007/s00027-009-0108-0
Wolfstein K, Stal LJ (2002) Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar Ecol Prog Ser 236:13–22. https://doi.org/10.3354/meps236013
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(2):75–104. https://doi.org/10.1016/j.porgcoat.2003.06.001
Acknowledgements
This study was carried out with financial support from the French National Research Agency (ANR) in the framework of the Investments for the future Programme, within the Cluster of Excellence COTE (ANR-10-LABX-45).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Chaumet, B., Mazzella, N., Neury-Ormanni, J. et al. Light and temperature influence on diuron bioaccumulation and toxicity in biofilms. Ecotoxicology 29, 185–195 (2020). https://doi.org/10.1007/s10646-020-02166-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-020-02166-8