Role of Biofilms in Contaminant Bioaccumulation and Trophic Transfer in Aquatic Ecosystems: Current State of Knowledge and Future Challenges

Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 253)


In freshwater environments, microbial assemblages attached to submerged substrates play an essential role in ecosystem processes such as primary production, supported by periphyton, or organic matter decomposition, supported by microbial communities attached to leaf litter or sediments. These microbial assemblages, also called biofilms, are not only involved in nutrients fluxes but also in contaminants dynamics. Biofilms can accumulate metals and organic contaminants transported by the water flow and/or adsorbed onto substrates. Furthermore, due to their high metabolic activity and their role in aquatic food webs, microbial biofilms are also likely to influence contaminant fate in aquatic ecosystems. In this review, we provide (1) a critical overview of the analytical methods currently in use for detecting and quantifying metals and organic micropollutants in microbial biofilms attached to benthic substrata (rocks, sediments, leaf litter); (2) a review of the distribution of those contaminants within aquatic biofilms and the role of these benthic microbial communities in contaminant fate; (3) a set of future challenges concerning the role of biofilms in contaminant accumulation and trophic transfers in the aquatic food web. This literature review highlighted that most knowledge on the interaction between biofilm and contaminants is focused on contaminants dynamics in periphyton while technical limitations are still preventing a thorough estimation of contaminants accumulation in biofilms attached to leaf litter or sediments. In addition, microbial biofilms represent an important food resource in freshwater ecosystems, yet their role in dietary contaminant exposure has been neglected for a long time, and the importance of biofilms in trophic transfer of contaminants is still understudied.


Analytical methods Metals Microbial ecotoxicology Organic micropollutants Periphyton 



Atomic absorption spectrometry


Bioconcentration factor


Biomagnification factor


Confocal laser scanning microscopy




Deoxyribonucleic acid


Dissolved organic matter


Ethylenediaminetetraacetic acid


Extracellular polymeric substances


Gas chromatography-mass spectrometry


Inductively coupled plasma mass spectrometry


Inductively coupled plasma optical emission spectrometry


Octanol-water partition coefficient


Liquid chromatography-mass spectrometry


Limit of quantification


Polycyclic aromatic hydrocarbons


Polychlorinated biphenyls


Scanning transmission X-ray microscopy


Tris(2-butoxyethyl) phosphate


Transmission electron microscopy

Supplementary material

489917_1_En_39_MOESM1_ESM.xlsx (462 kb)
Table S1 Experimental data (from 34 published articles) including chemical concentration in surface water, sediment, and biofilm as well as calculated BCF (L g−1). NA not applicable, n.d. not determined (XLSX 462 kb) (6 kb)
Fig. S1 Bioconcentration factor, expressed as log(BCF) of metals in periphytic biofilms vs. dissolved concentrations of metals in surface water (μg L−1). Data points circled in red are observations from laboratory experiments; all other points are observations from field studies (n = 218; data from 14 published studies) (ZIP 6 kb)


  1. Aguilera A, Souza-Egipsy V, Martin-Uriz PS, Amils R (2008) Extraction of extracellular polymeric substances from extreme acidic microbial biofilms. Appl Microbiol Biotechnol 78:1079–1088. Scholar
  2. Alvarez M, Peckarsky BL (2005) How do grazers affect periphyton heterogeneity in streams? Oecologia 142:576–587. Scholar
  3. Ancion PY, Lear G, Lewis GD (2010) Three common metal contaminants of urban runoff (Zn, Cu & Pb) accumulate in freshwater biofilm and modify embedded bacterial communities. Environ Pollut 158:2738–2745. Scholar
  4. Ancion PY, Lear G, Dopheide A, Lewis GD (2013) Metal concentrations in stream biofilm and sediments and their potential to explain biofilm microbial community structure. Environ Pollut 173:117–124. Scholar
  5. Arini A, Feurtet-Mazel A, Maury-Brachet R et al (2012) Field translocation of diatom biofilms impacted by Cd and Zn to assess decontamination and community restructuring capacities. Ecol Indic 18:520–531CrossRefGoogle Scholar
  6. Arnot JA, Gobas F (2006) A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ Rev 14:257–297. Scholar
  7. Augustin T, Schlosser D, Baumbach R et al (2006) Biotransformation of 1-naphthol by a strictly aquatic fungus. Curr Microbiol 52:216–220. Scholar
  8. Avery SV, Tobin JM (1993) Mechanism of adsorption of hard and soft metal ions to Saccharomyces cerevisiae and influence of hard and soft anions. Appl Env Microbiol 59:2851–2856CrossRefGoogle Scholar
  9. Avery SV, Codd GA, Gadd GM (1993) Transport kinetics, cation inhibition and intracellular location of accumulated caesium in the green microalga Chlorella salina. Microbiology 139:827–834. Scholar
  10. Barkay T, Schaefer J (2001) Metal and radionuclide bioremediation: issues, considerations and potentials. Curr Opin Microbiol 4:318–323. Scholar
  11. Barral-Fraga L, Morin S, Rovira MDM et al (2016) Short-term arsenic exposure reduces diatom cell size in biofilm communities. Environ Sci Pollut Res 23:4257–4270. Scholar
  12. Battin TJ, Kaplan LA, Newbold JD, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442. Scholar
  13. Battin TJ, Besemer K, Bengtsson MM et al (2016) The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol 14:251–263. Scholar
  14. Behrens S, Kappler A, Obst M (2012) Linking environmental processes to the in situ functioning of microorganisms by high-resolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM). Environ Microbiol 14:2851–2869. Scholar
  15. Berglund O (2003) Periphyton density influences organochlorine accumulation in rivers. Limnol Oceanogr 48:2106–2116CrossRefGoogle Scholar
  16. Berglund O, Nyström P, Larsson P (2005) Persistent organic pollutants in river food webs: influence of trophic position and degree of heterotrophy. Can J Fish Aquat Sci 62:2021–2032. Scholar
  17. Bertini G (2016) Memory effect of aquatic biofilms in the partitioning of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) in water streams. Int J Environ Sci Dev 7:921–927. Scholar
  18. Bradac P, Behra R, Sigg L (2009) Accumulation of cadmium in periphyton under various freshwater speciation conditions. Environ Sci Technol 43:7291–7296. Scholar
  19. Bradac P, Wagner B, Kistler D et al (2010) Cadmium speciation and accumulation in periphyton in a small stream with dynamic concentration variations. Environ Pollut 158:641–648. Scholar
  20. Brown DA, Beveridge TJ, Keevil CW, Sheriff BL (1998) Evaluation of microscopic techniques to observe iron precipitation in a natural microbial biofilm. FEMS Microbiol Ecol 26:297–310. Scholar
  21. Burns A (1997) The role of disturbance in the ecology of biofilms in the River Murray, South Australia. PhD thesis, University of AdelaideGoogle Scholar
  22. Burns A, Ryder DS (2001) Potential for biofilms as biological indicators in Australian riverine systems. Ecol Manag Restor 2:53–64. Scholar
  23. Carles L, Rossi F, Joly M et al (2017) Biotransformation of herbicides by aquatic microbial communities associated to submerged leaves. Environ Sci Pollut Res 24:3664–3674. Scholar
  24. Carles L, Rossi F, Besse-Hoggan P et al (2018) Nicosulfuron degradation by an Ascomycete fungus isolated from submerged Alnus leaf litter. Front Microbiol 9:3167. Scholar
  25. Carles L, Gardon H, Joseph L et al (2019) Meta-analysis of glyphosate contamination in surface waters and dissipation by biofilms. Environ Int 124:284–293. Scholar
  26. Chaumet B, Morin S, Hourtané O et al (2019a) Flow conditions influence diuron toxicokinetics and toxicodynamics in freshwater biofilms. Sci Total Environ 652:1242–1251. Scholar
  27. Chaumet B, Morin S, Boutry S, Mazzella N (2019b) Diuron sorption isotherms in freshwater biofilms. Sci Total Environ 651:1219–1225. Scholar
  28. Chen SJ, Luo XJ, Mai BX et al (2006) Distribution and mass inventories of polycyclic aromatic hydrocarbons and organochlorine pesticides in sediments of the Pearl River estuary and the northern South China Sea. Environ Sci Technol 40:709–714. Scholar
  29. Cleveland D, Long SE, Pennington PL et al (2012) Pilot estuarine mesocosm study on the environmental fate of silver nanomaterials leached from consumer products. Sci Total Environ 421–422:267–272. Scholar
  30. Coat S, Monti D, Legendre P et al (2011) Organochlorine pollution in tropical rivers (Guadeloupe): role of ecological factors in food web bioaccumulation. Environ Pollut 159:1692–1701CrossRefGoogle Scholar
  31. Conley JM, Funk DH, Buchwalter DB (2009) Selenium bioaccumulation and maternal transfer in the mayfly Centroptilum triangulifer in a life-cycle, periphyton-biofilm trophic assay. Environ Sci Technol 43:7952–7957. Scholar
  32. Coogan MA, Edziyie RE, La Point TW, Venables BJ (2007) Algal bioaccumulation of triclocarban, triclosan, and methyl-triclosan in a North Texas wastewater treatment plant receiving stream. Chemosphere 67:1911–1918CrossRefGoogle Scholar
  33. Corcoll N, Bonet B, Morin S et al (2012) The effect of metals on photosynthesis processes and diatom metrics of biofilm from a metal-contaminated river: a translocation experiment. Ecol Indic 18:620–631. Scholar
  34. Croteau MN, Luoma SN, Stewart AR (2005) Trophic transfer of metals along freshwater food webs: evidence of cadmium biomagnification in nature. Limnol Oceanogr 50:1511–1519CrossRefGoogle Scholar
  35. Danger M, Lacroix G, Oumarou C et al (2008) Effects of food-web structure on periphyton stoichiometry in eutrophic lakes: a mesocosm study. Freshw Biol 53:2089–2100. Scholar
  36. Danger M, Cornut J, Chauvet E et al (2013) Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect? Ecology 94:1604–1613. Scholar
  37. DeLorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic microorganisms: a review. Environ Toxicol Chem 20:84–98. Scholar
  38. Dimitrov MR, Kosol S, Smidt H et al (2014) Assessing effects of the fungicide tebuconazole to heterotrophic microbes in aquatic microcosms. Sci Total Environ 490:1002–1011. Scholar
  39. Dobor J, Varga M, Záray G (2012) Biofilm controlled sorption of selected acidic drugs on river sediments characterized by different organic carbon content. Chemosphere 87:105–110. Scholar
  40. Domagalski JL, Weston DP, Zhang MH, Hladik M (2010) Pyrethroid insecticide concentrations and toxicity in streambed sediments and loads in surface waters of the San Joaquin valley, California, USA. Environ Toxicol Chem 29:813–823CrossRefGoogle Scholar
  41. Dranguet P, Le Faucheur S, Cosio C, Slaveykova VI (2017) Influence of chemical speciation and biofilm composition on mercury accumulation by freshwater biofilms. Environ Sci Process Impacts 19:38–49. Scholar
  42. Du B, Perez-Hurtado P, Brooks BW, Chambliss CK (2012) Evaluation of an isotope dilution liquid chromatography tandem mass spectrometry method for pharmaceuticals in fish. J Chromatogr A 1253:177–183. Scholar
  43. Du B, Haddad SP, Luek A et al (2014) Bioaccumulation and trophic dilution of human pharmaceuticals across trophic positions of an effluent-dependent wadeable stream. Philos Trans R Soc B Biol Sci 369:20140058. Scholar
  44. Du B, Haddad SP, Scott WC et al (2015) Pharmaceutical bioaccumulation by periphyton and snails in an effluent-dependent stream during an extreme drought. Chemosphere 119:927–934. Scholar
  45. Dynes JJ, Tyliszczak T, Araki T et al (2006a) Speciation and quantitative mapping of metal species in microbial biofilms using scanning transmission X-ray microscopy. Environ Sci Technol 40:1556–1565. Scholar
  46. Dynes JJ, Lawrence JR, Korber DR et al (2006b) Quantitative mapping of chlorhexidine in natural river biofilms. Sci Total Environ 369:369–383. Scholar
  47. 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 97:9909–9921. Scholar
  48. European Commission (2010) Common Implementation Strategy for the Water Framework Directive (2000/60/EC): Guidance Document No. 25 on chemical monitoring of sediment and biota under the Water Framework DirectiveGoogle Scholar
  49. European Commission (2013) Directive 2013/39/EU of the European Parliament and of the Council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Off J L 226Google Scholar
  50. European Commission (2015) Commission Implementing Decision 2015/495 of 20 March 2015 establishing a watch list of substances for union-wide monitoring in the field of water policy pursuant to Directive 2008/105/EC of the European Parliament and of the Council (notified under document C(2015) 1756) text with EEA relevance. Off J L 78Google Scholar
  51. Fabure J, Dufour M, Autret A et al (2015) Impact of an urban multi-metal contamination gradient: metal bioaccumulation and tolerance of river biofilms collected in different seasons. Aquat Toxicol 159:276–289. Scholar
  52. Fan Q, He J, Xue H et al (2007) Competitive adsorption, release and speciation of heavy metals in the Yellow River sediments, China. Environ Geol 53:239–251. Scholar
  53. Farag AM, Woodward DF, Goldstein JN et al (1998) Concentrations of metals associated with mining waste in sediments, biofilm, benthic macroinvertebrates, and fish from the Coeur d’Alene River Basin, Idaho. Arch Environ Contam Toxicol 34:119–127CrossRefGoogle Scholar
  54. Farag AM, Nimick DA, Kimball BA et al (2007) Concentrations of metals in water, sediment, biofilm, benthic macroinvertebrates, and fish in the Boulder River watershed, Montana, and the role of colloids in metal uptake. Arch Environ Contam Toxicol 52:397–409. Scholar
  55. Fechner LC, Gourlay-France C, Tusseau-Vuillemin M-H (2011) Low exposure levels of urban metals induce heterotrophic community tolerance: a microcosm validation. Ecotoxicology 20:793–802. Scholar
  56. Fechner LC, Gourlay-France C, Bourgeault A, Tusseau-Vuillemin M-H (2012) Diffuse urban pollution increases metal tolerance of natural heterotrophic biofilms. Environ Pollut 162:311–318. Scholar
  57. Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159. Scholar
  58. Fernandez MA, Alonso C, Gonzalez MJ, Hernandez LM (1999) Occurrence of organochlorine insecticides, PCBs and PCB congeners in waters and sediments of the Ebro River (Spain). Chemosphere 38:33–43. Scholar
  59. Fisk AT, Hobson KA, Norstrom RJ (2001) Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya Marine Food Web. Environ Sci Technol 35:732–738. Scholar
  60. Flemming HC (1995) Sorption sites in biofilms. Water Sci Technol 32:27–33. Scholar
  61. Flemming H-C, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs) – part I: structural and ecological aspects. Water Sci Technol 43:1–8CrossRefGoogle Scholar
  62. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947. Scholar
  63. Friesen V, Doig LE, Markwart BE et al (2017) Genetic characterization of periphyton communities associated with selenium bioconcentration and trophic transfer in a simple food chain. Environ Sci Technol 51:7532–7541. Scholar
  64. Froehner S, Machado KS, Dombroski LF et al (2012) Natural biofilms in freshwater ecosystem: indicators of the presence of polycyclic aromatic hydrocarbons. Water Air Soil Pollut 223:3965–3973. Scholar
  65. García-Ordiales E, Esbrí JM, Covelli S et al (2016) Heavy metal contamination in sediments of an artificial reservoir impacted by long-term mining activity in the Almadén mercury district (Spain). Environ Sci Pollut Res 23:6024–6038. Scholar
  66. Garvin EM, Bridge CF, Garvin MS (2017) Screening level assessment of metal concentrations in streambed sediments and floodplain soils within the Grand Lake Watershed in Northeastern Oklahoma, USA. Arch Environ Contam Toxicol 72:349–363. Scholar
  67. Gascón Díez E, Corella JP, Adatte T et al (2017) High-resolution reconstruction of the 20th century history of trace metals, major elements, and organic matter in sediments in a contaminated area of Lake Geneva, Switzerland. Appl Geochem 78:1–11. Scholar
  68. Golding LA, Borgmann U, Dixon DG (2013) Cadmium bioavailability to Hyalella azteca from a periphyton diet compared to an artificial diet and application of a biokinetic model. Aquat Toxicol 126:291–298. Scholar
  69. Gorga M, Insa S, Petrovic M, Barcelo D (2015) Occurrence and spatial distribution of EDCs and related compounds in waters and sediments of Iberian rivers. Sci Total Environ 503:69–86CrossRefGoogle Scholar
  70. Goulet RR, Krack S, Doyle PJ et al (2007) Dynamic multipathway modeling of Cd bioaccumulation in Daphnia magna using waterborne and dietborne exposures. Aquat Toxicol 81:117–125. Scholar
  71. Guanzon NG Jr, Fukuda M, Nakahara H (1996) Accumulation of agricultural pesticides by three freshwater microalgae. Fish Sci 62:690–697CrossRefGoogle Scholar
  72. Guasch H, Atli G, Bonet B et al (2010) Discharge and the response of biofilms to metal exposure in Mediterranean rivers. Hydrobiologia 657:143–157. Scholar
  73. Guasch H, Ricart M, López-Doval J et al (2016) Influence of grazing on triclosan toxicity to stream periphyton. Freshw Biol 61:2002–2012. Scholar
  74. Hall RO, Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79:1995–2012.[1995:ttsobi];2CrossRefGoogle Scholar
  75. Hamzeh M, Ouddane B, Clérandeau C, Cachot J (2016) Spatial distribution and toxic potency of trace metals in surface sediments of the Seine Estuary (France). Clean (Weinh) 44:544–552. Scholar
  76. Hao L, Li J, Kappler A, Obst M (2013) Mapping of heavy metal ion sorption to cell-extracellular polymeric substance-mineral aggregates by using metal-selective fluorescent probes and confocal laser scanning microscopy. Appl Environ Microbiol 79:6524–6534. Scholar
  77. Hao L, Guo Y, Byrne JM et al (2016) Binding of heavy metal ions in aggregates of microbial cells, EPS and biogenic iron minerals measured in-situ using metal- and glycoconjugates-specific fluorophores. Geochim Cosmochim Acta 180:66–96. Scholar
  78. Headley JV, Peru KM, Lawrence JR, Wolfaardt GM (1995) MS/MS identification of transformation products in degradative biofilms. Anal Chem 67:1831–1837CrossRefGoogle Scholar
  79. Headley JV, Gandrass J, Kuballa J et al (1998) Rates of sorption and partitioning of contaminants in river biofilm. Environ Sci Technol 32:3968–3973. Scholar
  80. Headley JV, Peru KM, Friesen DA, Neu T (2001) Liquid chromatography–mass spectrometry and liquid chromatography–tandem mass spectrometry determination of N-methylpyrrolidinone in riverine biofilms. J Chromatogr A 917:159–165. Scholar
  81. Hepp LU, Pratas JAMS, Graça MAS (2017) Arsenic in stream waters is bioaccumulated but neither biomagnified through food webs nor biodispersed to land. Ecotoxicol Environ Saf 139:132–138. Scholar
  82. Hitchcock AP, Dynes JJ, Johansson G et al (2008) Comparison of NEXAFS microscopy and TEM-EELS for studies of soft matter (vol 39, pg 311, 2008). Micron 39:741–748. Scholar
  83. Hitchcock AP, Dynes JJ, Lawrence JR et al (2009) Soft X-ray spectromicroscopy of nickel sorption in a natural river biofilm. Geobiology 7:432–453. Scholar
  84. Ho HH, Swennen R, Cappuyns V et al (2013) Geogene versus anthropogene origin of trace metals in sediments in Cua Luc Estuary and Ha Long Bay, Vietnam. Estuar Coasts 36:203–219. Scholar
  85. Holding KL, Gill RA, Carter J (2003) The relationship between epilithic periphyton (biofilm) bound metals and metals bound to sediments in freshwater systems. Environ Geochem Health 25:87–93. Scholar
  86. Hudson ML, Costello DM, Daley JM, Burton GA (2019) Species-specific (Hyalella azteca and Lymnea stagnalis) dietary accumulation of gold nano-particles associated with periphyton. Bull Environ Contam Toxicol 103:255–260. Scholar
  87. Huerta B, Rodriguez-Mozaz S, Nannou C et al (2016) Determination of a broad spectrum of pharmaceuticals and endocrine disruptors in biofilm from a waste water treatment plant-impacted river. Sci Total Environ 540:241–249. Scholar
  88. Hunter RC, Hitchcock AP, Dynes JJ et al (2008) Mapping the speciation of iron in Pseudomonas aeruginosa biofilms using scanning transmission X-ray microscopy. Environ Sci Technol 42:8766–8772. Scholar
  89. INERIS (2010) Qualité chimique des sédiments fluviaux en France. Synthèse des bases de données disponibles. Rapport d’étude. N° INERIS-DRC-10-105335-04971A, 99 ppGoogle Scholar
  90. Ivorra N, Hettelaar J, Tubbing GMJ et al (1999) Translocation of microbenthic algal assemblages used for in situ analysis of metal pollution in rivers. Arch Environ Contam Toxicol 37:19–28. Scholar
  91. Jardine TD, Kidd KA, Rasmussen JB (2012) Aquatic and terrestrial organic matter in the diet of stream consumers: implications for mercury bioaccumulation. Ecol Appl 22:843–855CrossRefGoogle Scholar
  92. Jardine TD, Kidd KA, O’Driscoll N (2013) Food web analysis reveals effects of pH on mercury bioaccumulation at multiple trophic levels in streams. Aquat Toxicol 132:46–52. Scholar
  93. Kilunga PI, Sivalingam P, Laffite A et al (2017) Accumulation of toxic metals and organic micro-pollutants in sediments from tropical urban rivers, Kinshasa, Democratic Republic of the Congo. Chemosphere 179:37–48. Scholar
  94. Kim KS, Funk DH, Buchwalter DB (2012) Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer. Ecotoxicology 21:2288–2296. Scholar
  95. Kim JI, Park HG, Chang KH et al (2016) Trophic transfer of nano-TiO2 in a paddy microcosm: a comparison of single-dose versus sequential multi-dose exposures. Environ Pollut 212:316–324. Scholar
  96. Kohušová K, Havel L, Vlasák 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 174:555–572. Scholar
  97. Komjarova I, Blust R (2009) Application of a stable isotope technique to determine the simultaneous uptake of cadmium, copper, nickel, lead and zinc by the water flea Daphnia magna from water and the green algae Pseudokirchneriella subcapitata. Environ Toxicol Chem 28:1739–1748CrossRefGoogle Scholar
  98. Krumins JA, van Oevelen D, Bezemer TM et al (2013) Soil and freshwater and marine sediment food webs: their structure and function. Bioscience 63:35–42. Scholar
  99. Laabs V, Wehrhan A, Pinto A et al (2007) Pesticide fate in tropical wetlands of Brazil: an aquatic microcosm study under semi-field conditions. Chemosphere 67:975–989. Scholar
  100. Labadie P, Hill EM (2007) Analysis of estrogens in river sediments by liquid chromatography-electrospray ionisation mass spectrometry – comparison of tandem mass spectrometry and time-of-flight mass spectrometry. J Chromatogr A 1141:174–181. Scholar
  101. Lambert AS, Morin S, Artigas J et al (2012) Structural and functional recovery of microbial biofilms after a decrease in copper exposure: influence of the presence of pristine communities. Aquat Toxicol 109:118–126. Scholar
  102. Lambert AS, Dabrin A, Morin S et al (2016) Temperature modulates phototrophic periphyton response to chronic copper exposure. Environ Pollut 208:821–829. Scholar
  103. Lavoie I, Lavoie M, Fortin C (2012) A mine of information: benthic algal communities as biomonitors of metal contamination from abandoned tailings. Sci Total Environ 425:231–241. Scholar
  104. Lawrence JR, Kopf G, Headley JV, Neu TR (2001) Sorption and metabolism of selected herbicides in river biofilm communities. Can J Microbiol 47:634–641. Scholar
  105. Lawrence JR, Swerhone GDW, Leppard GG et al (2003) Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl Environ Microbiol 69:5543–5554. Scholar
  106. Lawrence JR, Dynes JJ, Korber DR et al (2012) Monitoring the fate of copper nanoparticles in river biofilms using scanning transmission X-ray microscopy (STXM). Chem Geol 329:18–25. Scholar
  107. Lawrence JR, Swerhone GDW, Dynes JJ et al (2016) Soft X-ray spectromicroscopy for speciation, quantitation and nano-eco-toxicology of nanomaterials. J Microsc 261:130–147. Scholar
  108. Lawrence JR, Swerhone GDW, Neu TR (2019) Visualization of the sorption of nickel within exopolymer microdomains of bacterial microcolonies using confocal and scanning electraon microscopy. Microbes Environ 34:76–82. Scholar
  109. Leguay S, Lavoie I, Levy JL, Fortin C (2016) Using biofilms for monitoring metal contamination in lotic ecosystems: the protective effects of hardness and ph on metal bioaccumulation. Environ Toxicol Chem 35:1489–1501. Scholar
  110. Lei BL, Huang SB, Zhou YQ et al (2009) Levels of six estrogens in water and sediment from three rivers in Tianjin area, China. Chemosphere 76:36–42CrossRefGoogle Scholar
  111. Li M, Costello DM, Allen Burton G (2012) Interactive effects of phosphorus and copper on Hyalella azteca via periphyton in aquatic ecosystems. Ecotoxicol Environ Saf 83:41–46. Scholar
  112. Li H, Shi A, Li M, Zhang X (2013) Effect of pH, temperature, dissolved oxygen, and flow rate of overlying water on heavy metals release from storm sewer sediments. J Chem. Accessed 2 May 2019
  113. Liang XM, Chen BW, Nie XP et al (2013) The distribution and partitioning of common antibiotics in water and sediment of the Pearl River Estuary, South China. Chemosphere 92:1410–1416CrossRefGoogle Scholar
  114. Liao J, Chen J, Ru X et al (2017) Heavy metals in river surface sediments affected with multiple pollution sources, South China: distribution, enrichment and source apportionment. J Geochem Explor 176:9–19. Scholar
  115. Lin J-G, Chen S-Y (1998) The relationship between adsorption of heavy metal and organic matter in river sediments. Environ Int 24:345–352. Scholar
  116. Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425. Scholar
  117. Lundqvist A, Bertilsson S, Goedkoop W (2012) Interactions with DOM and biofilms affect the fate and bioavailability of insecticides to invertebrate grazers. Ecotoxicology 21:2398–2408. Scholar
  118. Lünsdorf H, Brümmer I, Timmis KN, Wagner-Döbler I (1997) Metal selectivity of in situ microcolonies in biofilms of the Elbe river. J Bacteriol 179:31–40CrossRefGoogle Scholar
  119. Magellan K, Barral-Fraga L, Rovira M et al (2014) Behavioural and physical effects of arsenic exposure in fish are aggravated by aquatic algae. Aquat Toxicol 156:116–124. Scholar
  120. Margoum C, Malessard C, Gouy V (2006) Investigation of various physicochemical and environmental parameter influence on pesticide sorption to ditch bed substratum by means of experimental design. Chemosphere 63:1835–1841. Scholar
  121. Mattila K, Carpen L, Hakkarainen T, Salkinoja-Salonen MS (1997) Biofilm development during ennoblement of stainless steel in Baltic Sea water: a microscopic study. Int Biodeterior Biodegrad 40:1–10CrossRefGoogle Scholar
  122. Métivier R, Bourven I, Labanowski J, Guibaud G (2013) Interaction of erythromycin ethylsuccinate and acetaminophen with protein fraction of extracellular polymeric substances (EPS) from various bacterial aggregates. Environ Sci Pollut Res 20:7275–7285. Scholar
  123. Meylan S, Behra R, Sigg L (2003) Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater. Environ Sci Technol 37:5204–5212. Scholar
  124. Meylan S, Behra R, Sigg L (2004) Influence of metal speciation in natural freshwater on bioaccumulation of copper and zinc in periphyton: a microcosm study. Environ Sci Technol 38:3104–3111. Scholar
  125. Miller AZ, Dionisio A, Braga MAS et al (2012) Biogenic Mn oxide minerals coating in a subsurface granite environment. Chem Geol 322:181–191. Scholar
  126. Morin S, Duong TT, Herlory O et al (2008) Cadmium toxicity and bioaccumulation in freshwater biofilms. Arch Environ Contam Toxicol 54:173–186CrossRefGoogle Scholar
  127. Munoz G, Fechner LC, Geneste E et al (2016) Spatio-temporal dynamics of per and polyfluoroalkyl substances (PFASs) and transfer to periphytic biofilm in an urban river: case-study on the River Seine. Environ Sci Pollut Res 25:23574–23582. Scholar
  128. Murray KE, Thomas SM, Bodour AA (2010) Prioritizing research for trace pollutants and emerging contaminants in the freshwater environment. Environ Pollut 158:3462–3471. Scholar
  129. Neu TR, Manz B, Volke F et al (2010) Advanced imaging techniques for assessment of structure, composition and function in biofilm systems. FEMS Microbiol Ecol 72:1–21. Scholar
  130. Neury-Ormanni J, Vedrenne J, Morin S (2016) Who eats who in biofilms? Exploring the drivers of microalgal and micro-meiofaunal abundance. Bot Lett 163:83–92CrossRefGoogle Scholar
  131. Pal A, Gin KY-H, Lin AY-C, Reinhard M (2010) Impacts of emerging organic contaminants on freshwater resources: review of recent occurrences, sources, fate and effects. Sci Total Environ 408:6062–6069. Scholar
  132. Park HG, Kim JI, Chang KH et al (2018) Trophic transfer of citrate, PVP coated silver nanomaterials, and silver ions in a paddy microcosm. Environ Pollut 235:435–445. Scholar
  133. Passeport E, Benoit P, Bergheaud V et al (2011) Selected pesticides adsorption and desorption in substrates from artificial wetland and forest buffer. Environ Toxicol Chem 30:1669–1676. Scholar
  134. Passeport E, Tournebize J, Chaumont C et al (2013) Pesticide contamination interception strategy and removal efficiency in forest buffer and artificial wetland in a tile-drained agricultural watershed. Chemosphere 91:1289–1296CrossRefGoogle Scholar
  135. Passeport E, Richard B, Chaumont C et al (2014) Dynamics and mitigation of six pesticides in a “Wet” forest buffer zone. Environ Sci Pollut Res 21:4883–4894. Scholar
  136. Pereira WE, Domagalski JL, Hostettler FD et al (1996) Occurrence and accumulation of pesticides and organic contaminants in river sediment, water and clam tissues from the San Joaquin River and tributaries, California. Environ Toxicol Chem 15:172–180.<0172:oaaopa>;2CrossRefGoogle Scholar
  137. Perrier F, Baudrimont M, Mornet S et al (2018) Gold nanoparticle trophic transfer from natural biofilm to grazer fish. Gold Bull 51:163–173. Scholar
  138. Pesce S, Fabrice ML, Rouard N, Montuelle B (2009) Potential for microbial diuronmineralisation in a small wine-growing watershed: from treated plots to lotic receiver hydrosystem. Pest Manag Sci 65:651–657. Scholar
  139. Pesce S, Margoum C, Rouard N et al (2013) Freshwater sediment pesticide biodegradation potential as an ecological indicator of microbial recovery following a decrease in chronic pesticide exposure: a case study with the herbicide diuron. Ecol Indic 29:18–25. Scholar
  140. Pesce S, Lyautey E, Foulquier A (2017) Réponse structurelle et fonctionnelle des communautés microbiennes hétérotrophes benthiques aux contaminants: quelle conséquence pour le fonctionnement de l’écosystème? In Bernard C, Mougin C, Péry A (eds) Ecotoxicologie, des communautés au fonctionnement des écosystèmes. ISTE Editions, pp 31–54Google Scholar
  141. Pesce S, Lambert AS, Morin S et al (2018) Experimental warming differentially influences the vulnerability of phototrophic and heterotrophic periphytic communities to copper toxicity. Front Microbiol 9.
  142. Pinder JE, Hinton TG, Taylor BE, Whicker FW (2011) Cesium accumulation by aquatic organisms at different trophic levels following an experimental release into a small reservoir. J Environ Radioact 102:283–293. Scholar
  143. Proia L, Lupini G, Osorio V et al (2013a) Response of biofilm bacterial communities to antibiotic pollutants in a Mediterranean River. Chemosphere 92:1126–1135. Scholar
  144. Proia L, Osorio V, Soley S et al (2013b) Effects of pesticides and pharmaceuticals on biofilms in a highly impacted river. Environ Pollut 178:220–228. Scholar
  145. Prokes R, Vrana B, Klanova J (2012) Levels and distribution of dissolved hydrophobic organic contaminants in the Morava River in Zlin District, Czech Republic as derived from their accumulation in silicone rubber passive samplers. Environ Pollut 166:157–166CrossRefGoogle Scholar
  146. Quesada S, Tena A, Guillen D et al (2014) Dynamics of suspended sediment borne persistent organic pollutants in a large regulated Mediterranean River (Ebro, NE Spain). Sci Total Environ 473:381–390CrossRefGoogle Scholar
  147. Robson BJ, Barmuta LA (1998) The effect of two scales of habitat architecture on benthic grazing in a river. Freshw Biol 39:207–220. Scholar
  148. Rodrigues MLK, Formoso MLL (2006) Geochemical distribution of selected heavy metals in stream sediments affected by tannery activities. Water Air Soil Pollut 169:167–184. Scholar
  149. Roeselers G, van Loosdrecht MCM, Muyzer G (2008) Phototrophic biofilms and their potential applications. J Appl Phycol 20:227–235. Scholar
  150. Roessink I, Moermond CTA, Gillissen F, Koelmans AA (2010) Impacts of manipulated regime shifts in shallow lake model ecosystems on the fate of hydrophobic organic compounds. Water Res 44:6153–6163. Scholar
  151. Romani AM, Sabater S (2001) Structure and activity of rock and sand biofilms in a Mediterranean stream. Ecology 82:3232–3245CrossRefGoogle Scholar
  152. Romani AM, Guasch H, Munoz I et al (2004) Biofilm structure and function and possible implications for riverine DOC dynamics. Microb Ecol 47:316–328. Scholar
  153. Rossi F, Pesce S, Mallet C et al (2018) Interactive effects of pesticides and nutrients on microbial communities responsible of litter decomposition in streams. Front Microbiol 9.
  154. Ruhí A, Acuña V, Barceló D et al (2016) Bioaccumulation and trophic magnification of pharmaceuticals and endocrine disruptors in a Mediterranean river food web. Sci Total Environ 540:250–259. Scholar
  155. Sabater S, Guasch H, Munoz I, Romani A (2006) Hydrology, light and the use of organic and inorganic materials as structuring factors of biological communities in Mediterranean streams. Limnetica 25:335–348Google Scholar
  156. Saeedi M, Hosseinzadeh M, Rajabzadeh M (2011) Competitive heavy metals adsorption on natural bed sediments of Jajrood River, Iran. Environ Earth Sci 62:519–527. Scholar
  157. 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. Scholar
  158. Schmitt J, Nivens D, White DC, Flemming H-C (1995) Changes of biofilm properties in response to sorbed substances – an FTIR-ATR study. Water Sci Technol 32:149–155. Scholar
  159. Schneck F, Schwarzbold A, Melo AS (2013) Substrate roughness, fish grazers, and mesohabitat type interact to determine algal biomass and sediment accrual in a high-altitude subtropical stream. Hydrobiologia 711:165–173. Scholar
  160. Schorer M, Eisele M (1997) Accumulation of inorganic and organic pollutants by biofilms in the aquatic environment. Water Air Soil Pollut 99:651–659. Scholar
  161. Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397. Scholar
  162. Smolders AJP, Lock RAC, Van der Velde G et al (2003) Effects of mining activities on heavy metal concentrations in water, sediment, and macroinvertebrates in different reaches of the Pilcomayo River, South America. Arch Environ Contam Toxicol 44:0314–0323. Scholar
  163. Sole M, Kellner H, Brock S et al (2008) Extracellular laccase activity and transcript levels of putative laccase genes during removal of the xenoestrogen technical nonylphenol by the aquatic hyphomycete Clavariopsis aquatica. FEMS Microbiol Lett 288:47–54. Scholar
  164. Sridhar KR, Krauss G, Barlocher F et al (2001) Decomposition of alder leaves in two heavy metal-polluted streams in Central Germany. Aquat Microb Ecol 26:73–80. Scholar
  165. Sridhar KR, Barlocher F, Wennrich R et al (2008) Fungal biomass and diversity in sediments and on leaf litter in heavy metal contaminated waters of Central Germany. Fundam Appl Limnol 171:63–74. Scholar
  166. Tao F, Jiantong L, Bangding X et al (2005) Mobilization potential of heavy metals: a comparison between river and lake sediments. Water Air Soil Pollut 161:209–225. Scholar
  167. Thevenon F, Graham ND, Chiaradia M et al (2011) Local to regional scale industrial heavy metal pollution recorded in sediments of large freshwater lakes in Central Europe (lakes Geneva and Lucerne) over the last centuries. Sci Total Environ 412–413:239–247. Scholar
  168. Trinh SB, Hiscock KM, Reid BJ (2012) Mechanistic insights into the role of river sediment in the attenuation of the herbicide isoproturon. Environ Pollut 170:95–101. Scholar
  169. Vallée R, Dousset S, Billet D, Benoit M (2014) Sorption of selected pesticides on soils, sediment and straw from a constructed agricultural drainage ditch or pond. Environ Sci Pollut Res 21:4895–4905. Scholar
  170. van Hullebusch ED, Zandvoort MH, Lens PNL (2003) Metal immobilisation by biofilms: mechanisms and analytical tools. Rev Environ Sci Biotechnol 2:9–33. Scholar
  171. Vila-Costa M, Gioia R, Aceña J et al (2017) Degradation of sulfonamides as a microbial resistance mechanism. Water Res 115:309–317. Scholar
  172. Vilchez R, Gomez-Silvan C, Purswani J et al (2011) Characterization of bacterial communities exposed to Cr(III) and Pb(II) in submerged fixed-bed biofilms for groundwater treatment. Ecotoxicology 20:779–792. Scholar
  173. Vinot I, Pihan JC (2005) Circulation of copper in the biotic compartments of a freshwater dammed reservoir. Environ Pollut 133:169–182. Scholar
  174. Walters DM, Fritz KM, Johnson BR et al (2008) Influence of trophic position and spatial location on polychlorinated biphenyl (PCB) bioaccumulation in a stream food web. Env Sci Technol 42:2316–2322CrossRefGoogle Scholar
  175. Walters DM, Mills MA, Cade BS, Burkard LP (2011) Trophic magnification of PCBs and its relationship to the octanol-water partition coefficient. Environ Sci Technol 45:3917–3924. Scholar
  176. Walters DM, Rosi-Marshall E, Kennedy TA et al (2015) Mercury and selenium accumulation in the Colorado River food web, Grand Canyon, USA. Env Toxicol Chem 34:2385–2394. Scholar
  177. Wang H, Kostel JA, St. Amand AL, Gray KA (1999) 2. The response of a laboratory stream system to PCB exposure: study of periphytic and sediment accumulation patterns. Water Res 33:3749–3761. Scholar
  178. Wang W, Wang W, Zhang X, Wang D (2002) Adsorption of p-chlorophenol by biofilm components. Water Res 36:551–560. Scholar
  179. Wang Z, Yang YY, Sun WM et al (2014) Nonylphenol biodegradation in river sediment and associated shifts in community structures of bacteria and ammonia-oxidizing microorganisms. Ecotoxicol Environ Saf 106:1–5CrossRefGoogle Scholar
  180. Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182:2675–2679. Scholar
  181. White C, Gadd GM (1987) The uptake and cellular distribution of zinc in Saccharomyces cerevisiae. Microbiology 133:727–737. Scholar
  182. White C, Gadd GM (1995) Determination of metals and metal fluxes in algae and fungi. Sci Total Environ 176:107–115. Scholar
  183. Wolfaardt GM, Lawrence JR, Headley JV et al (1994) Microbial exopolymers provide a mechanism for bioaccumulation of contaminants. Microb Ecol 27:279–291. Scholar
  184. Wolfaardt GM, Lawrence JR, Robarts RD, Caldwell DE (1998) In situ characterization of biofilm exopolymers involved in the accumulation of chlorinated organics. Microb Ecol 35:213–223. Scholar
  185. Writer JH, Ryan JN, Barber LB (2011) Role of biofilms in sorptive removal of steroidal hormones and 4-nonylphenol compounds from streams. Environ Sci Technol 45:7275–7283. Scholar
  186. Wuertz S, Müller E, Spaeth R et al (2000) Detection of heavy metals in bacterial biofilms and microbial flocs with the fluorescent complexing agent Newport Green. J Ind Microbiol Biotechnol 24:116–123. Scholar
  187. Wunder DB, Bosscher VA, Cok RC, Hozalski RM (2011) Sorption of antibiotics to biofilm. Water Res 45:2270–2280. Scholar
  188. Xie L, Funk DH, Buchwalter DB (2010) Trophic transfer of Cd from natural periphyton to the grazing mayfly Centroptilum triangulifer in a life cycle test. Environ Pollut 158:272–277. Scholar
  189. Yang SI, George GN, Lawrence JR et al (2016) Multispecies biofilms transform selenium oxyanions into elemental selenium particles: studies using combined synchrotron X-ray fluorescence imaging and scanning transmission X-ray microscopy. Environ Sci Technol 50:10343–10350. Scholar
  190. Ylla I, Borrego C, Romani AM, Sabater S (2009) Availability of glucose and light modulates the structure and function of a microbial biofilm. FEMS Microbiol Ecol 69:27–42. Scholar
  191. Zou K, Thebault E, Lacroix G, Barot S (2016) Interactions between the green and brown food web determine ecosystem functioning. Funct Ecol.

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.INRAE, UR RiverLyVilleurbanneFrance
  2. 2.Université Clermont Auvergne, CNRS, Laboratoire Microorganismes: Génome et Environnement (LMGE)Clermont-FerrandFrance
  3. 3.INRAE, UR EABXCestasFrance
  4. 4.Université Paris-Saclay, INRAE, AgroParisTech, UMR ECOSYSVersaillesFrance
  5. 5.Ecotox CentreLausanneSwitzerland
  6. 6.INRAE, UR HYCAR, Artemhys, Centre d’AntonyAntonyFrance

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