Abstract
The impact of long-term exposure (6 months) to highly or slightly polluted sediments on the energy metabolism of an ecosystem engineer (the oligochaete Limnodrilus hoffmeisteri) was investigated in laboratory conditions. We evaluated some mitochondrial parameters (respiratory chain activity and ATP production rate) and the accumulation of anaerobic end-products (lactate, alanine, succinate, and propionate). The sediments were collected from stormwater infiltration basins and presented high levels of heavy metals and polycyclic aromatic hydrocarbons (PAHs). These compounds had been drained by the runoff water on impervious surfaces of urban areas during rainfall events. A decrease in the activity of the mitochondrial electron transport chain was observed in worms exposed to the most polluted sediment. Urban contaminants disrupted both aerobic metabolism and mitochondrial functioning, forcing organisms to shift from aerobic to anaerobic metabolism (which is characteristic of a situation of functional hypoxia). Although L. hoffmeisteri is very tolerant to urban pollutants, long-term exposure to high concentrations can cause disruption in mitochondrial activity and therefore energy production. Finally, this study demonstrated that anaerobic end-products could be used as biomarkers to evaluate the impact of a mixture of urban pollutants on invertebrates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barret J (1991) Parasitic helmints. In: Bryant C (ed) Metazoan life without oxygen. Chapman and Hall, London, pp 146–164
Bergmeyer HU (1985) Methods of enzymatic analysis, vols Vl-VIII (ed HU Bergmeyer). Verlag Chemie, Weinheim, Basel
Cannino G, Ferruggia E, Luparello C, Rinaldi AM (2009) Cadmium and mitochondria. Mitochondrion 9:377–384. https://doi.org/10.1016/j.mito.2009.08.009
Carvalho CS, Fernandes MN (2008) Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilodus lineatus. Comp Biochem Physiol C 151:437–442. https://doi.org/10.1016/j.cbpa.2007.04.016
Colinet H, Renault D, Roussel D (2017) Cold acclimation allows Drosophila flies to maintain mitochondrial functioning under cold stress. Insect Biochem Mol Biol 80:52–60. https://doi.org/10.1016/j.ibmb.2016.11.007
Ciutat A, Weber O, Gérino M, Boudou A (2006) Stratigraphic effects of tubificids in freshwater sediments: a kinetic study based on X-ray images and grain-size analysis. Acta Oecol 30(2):228–237
Datry T, Hervant F, Malard F, Vitry L, Gibert J (2003) Dynamics and adaptive responses of invertebrates to suboxia in contaminated sediments of a stormwater infiltration basin. Arch Hydrobiol 156:339–359. https://doi.org/10.1127/0003-9136/2003/0156-0339
De Coen WM, Janssen CR, Segner H (2001) The use of biomarkers in Daphnia magna toxicity testing V. In vivo alterations in the carbohydrate metabolism of Daphnia magna exposed to sublethal concentrations of mercury and lindane. Ecotoxicol Environ Saf 48:223–234. https://doi.org/10.1006/eesa.2000.2009
Gagnon MM, Holdway DA (1999) Metabolic enzyme activities in fish gills as biomarkers of exposure to petroleum hydrocarbons. Ecotoxicol Environ Saf 44:92–99. https://doi.org/10.1006/eesa.1999.1804
Gauthier PT, Norwood WP, Prepas EE, Pyle GG (2014) Metal-PAH mixtures in the aquatic environment: a review of co-toxic mechanisms leading to more-than-additive outcomes. Aquat Toxicol 154:253–269. https://doi.org/10.1016/j.aquatox.2014.05.026
Gette-Bouvarot M, Mermillod-Blondin F, Angullo-Jaramillo R, Delolme C, Lemoine D, Lassabatere L, Volatier L (2014) Coupling hydraulic and biological measurements highlights the key influence of algal biofilm on infiltration basin performance. Ecohydrology 7:950–964. https://doi.org/10.1016/j.scitotenv.2016.05.174
Giacomin M, Jorge MB, Bianchini A (2014) Effects of copper exposure on the energy metabolism in juveniles of the marine clam Mesodesma mactroides. Aquat Toxicol 152:30–37. https://doi.org/10.1016/j.aquatox.2014.03.025
Grajeda y Ortega MDLA, Ortiz Ordoñez E, Favari L, Shibayama M, Silva Olivares A, López López E (2011) Biochemical and mitochondrial changes induced by cd, Fe and Zn in Limnodrillus hoffmeisteri. Int J Morphol 29:412–419. https://doi.org/10.4067/S0717-95022011000200018
Guderley H, Kraffe W, Bureau D, Bureau P (2008) Dietary fatty acid composition changes mitochondrial phospholipids and oxidative capacities in rainbow trout red muscle. J Comp Physiol B 178(3):385–399
Hervant F, Mathieu J, Garin D, Fréminet A (1995) Behavioral, ventilatory, and metabolic responses to severe hypoxia and subsequent recovery of the hypogean Niphargus rhenorhodanensis and the epigean Gammarus fossarum (Crustacea: Amphipoda). Physiol Zool 68:223–244. https://doi.org/10.1086/physzool.68.2.30166501
Hervant F, Mathieu J, Barré H, Simon K, Pinon C (1997) Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comp Biochem Physiol A 118:1277–1283. https://doi.org/10.1016/S0300-9629(97)00047-9
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford
Ji X, Li Y, He J, Shah W, Xue X, Feng G, Zhang H, Gao M (2016) Depletion of mitochondrial enzyme system in liver, lung, brain, stomach and kidney induced by benzo(a)pyrene. Environ Toxicol Pharmacol 43:83–93. https://doi.org/10.1016/j.etap.2016.03.001
Ku HFH, Hagelin NW, Buxton HT (1992) Effects of urban storm-runoff control on ground-water recharge in Nassau country, New York. Ground Water 30(5):07–514. https://doi.org/10.1111/j.1745-6584.1992.tb01526.x
Kurochkin IO, Etzkorn M, Buchwalter D, Leamy L, Sokolova IM (2011) Top-down control analysis of the cadmium effects on molluscan mitochondria and the mechanisms of cadmium-induced mitochondrial dysfunction. Am J Physiol Regul Integr Comp Physiol 300:R21–R31. https://doi.org/10.1152/ajpregu.00279.2010
Lauer MM, De Oliveira CB, Yano NLI, Bianchini A (2012) Copper effects on key metabolic enzymes and mitochondrial membrane potential in gills of the estuarine crab Neohelice granulata at different salinities. Comp Biochem Physiol Part C 156:140–147. https://doi.org/10.1016/j.cbpc.2012.08.001
Li N, Sioutas C, Cho A, Schmitz D, Misra C, Sempf J, Wang M, Oberley T, Froines J, Nel A (2003) Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ Health Perspect 111:455–460. https://doi.org/10.1289/ehp.6000
Lotufo GR, Fleeger JW (1996) Toxicity of sediment –associated pyrene and phenanthrene to Limnodrilus hoffmeisteri (Oligochaeta: Tubificidae). Environ Toxicol Chem 15:1508–1516. https://doi.org/10.1002/etc.5620150912
Marmonier P, Maazouzi C, Foulquier A, Navel S, François C, Hervant F, Mermillod-Blondin F, Vienney A, Barraud S, Togola A, Piscart C (2013) The use of crustaceans as sentinel organisms to evaluate groundwater ecological quality. Ecol Eng 57:118–132. https://doi.org/10.1016/j.ecoleng.2013.04.009
Marsalek J, Chocat B (2002) International report: Stormwater management. Water Sci Technol 46:1–17
Marsalek J, Marsalek P (1997) Characteristics of sediments from a stormwater management pond. Water Sci Technol 36:117–122. https://doi.org/10.1016/S0273-1223(97)00610-0
McCall PL, Tevesz MJS (1982) The effects of benthos on physical properties of freshwater sediments. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations: the biogenic alteration of sediments. Springer US, Boston, pp 105–176
Mermillod-Blondin F, Lemoine D (2010) Ecosystem engineering by tubificid worms stimulates macrophyte growth in poorly oxygenated wetland sediments. Funct Ecol 24:444–453. https://doi.org/10.1111/j.1365-2435.2009.01624.x
Mermillod-Blondin F, Rosenberg R (2006) Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquat Sci Across Boundaries 68:434–442. https://doi.org/10.1007/s00027-006-0858-x
Mermillod-Blondin F, Gérino M, Degrange V, Lensi R, Chassé JL, Rard M, Creuzé d, Châtellier M (2001) Testing the functional redundancy of Limnodrilus and Tubifex (Oligochaeta, Tubificidae) in hyporheic sediments: an experimental study in microcosms. Can J Fish Aquat Sci 58:1747–1759. https://doi.org/10.1139/cjfas-58-9-1747
Mermillod-Blondin F, Foulquier A, Gilbert F, Navel S, Montuelle B, Bellvert F, Comte G, Grossi V, Fourel F, Lecuyer C, Simon L (2013) Benzo(a)pyrene inhibits the role of the bioturbator Tubifex tubifex in river sediment biogeochemistry. Sci Total Environ 450–451:230–241. https://doi.org/10.1016/j.scitotenv.2013.02.013
Meyer JN, Leung MCK, Rooney JP, Sendoel A, Hengartner MO, Kisby GE, Bess AS (2013) Mitochondria as a target of environmental toxicants. Toxicol Sci 134:1–17. https://doi.org/10.1093/toxsci/kft102
Millward RN, Fleeger JW, Reible DD, Keteles AK, Cunningham BP, Zhang L (2001) Pyrene bioaccumulation, effects of pyrene exposure on particle-size selection, and fecal pyrene content in the oligochaete Limnodrilus hoffmeisteri (Tubificidae, Oligochaeta). Environ Toxicol Chem 20:1359–1366. https://doi.org/10.1002/etc.5620200627
Nelson DL, Cox MM (2017) In: WH Freeman (ed) Lehninger principles of biochemistry, 7th edn. 1328 pp
Niemczynowicz J (1999) Urban hydrology and water management – present and future challenges. Urban Water 1:1–14. https://doi.org/10.1016/S1462-0758(99)00009-6
Pigneret M, Mermillod-Blondin F, Volatier L, Romestaing C, Maire E, Adrien J, Guillard L, Roussel D, Hervant F (2016) Urban pollution of sediments: impact on the physiology and burrowing activity of tubificid worms and consequences on biogeochemical processes. Sci Total Environ 568:196–207. https://doi.org/10.1016/j.scitotenv.2016.05.174
Plenet S, Hervant F, Joly P (2000) Ecology of the Hybridogenetic Rana esculenta Complex: Differential Oxygen Requirements of Tadpoles. Evol Ecol 14(1):13–23
Renault D, Hervant F, Vernon P (2002) Comparative study of the metabolic responses during food shortage and subsequent recovery at different temperatures in the adult lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Physiol Entomol 27:291–301. https://doi.org/10.1046/j.1365-3032.2002.00299.x
Roussel D, Salin K, Dumet A, Romestaing C, Rey B, Voituron Y (2015) Oxidative phosphorylation efficiency, proton conductance and reactive oxygen species production of liver mitochondria correlates with body mass in frogs. J Exp Biol 218:3222–3228. https://doi.org/10.1242/jeb.126086
Salin K, Luquet E, Rey B, Roussel D, Voituron Y (2012) Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles. J Exp Biol 215:863–869. https://doi.org/10.1242/jeb.062745
Schaller J, Brackhage C, Mkandawire M, Dudel EG (2011) Metal/metalloid accumulation/remobilization during aquatic litter decomposition in freshwater: a review. Sci Total Environ 409:4891–4898. https://doi.org/10.1016/j.scitotenv.2011.08.006
Schöttler U, Bennet EM (1991) Annelids. In: Bryant C (ed) Metazoan life without oxygen. Chapman and Hall, London, pp 165–185
Shang J, Liao Q, Zhang L, Fan C (2014) The influence of different benthic fauna on inorganic nitrogen flux and denitrification in a large shallow hyper-eutrophic lake. Fundam Appl Limnol 184:101–108. https://doi.org/10.1127/1863-9135/2014/0431
US EPA (1991) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. 4th ed. Report EPA/600/4–90/2, Environmental Protection Agency, Washington
Wang Y, Fang J, Leonard SS, Rao KMK (2004) Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443. https://doi.org/10.1016/j.freeradbiomed.2004.03.01
Acknowledgments
The authors thank Prof. Eric Pattee (Université Lyon 1) for his assistance in correcting a first version of the manuscript.
Funding
This study was conducted and funded within the framework of the Experimental Observatory for Urban Hydrology (OTHU; http://www.graie.org/othu/).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Pigneret, M., Roussel, D. & Hervant, F. Anaerobic end-products and mitochondrial parameters as physiological biomarkers to assess the impact of urban pollutants on a key bioturbator. Environ Sci Pollut Res 25, 27225–27234 (2018). https://doi.org/10.1007/s11356-018-2756-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-2756-x