Microbial Ecology

, Volume 54, Issue 2, pp 232–241 | Cite as

Effects of Experimental Lead Pollution on the Microbial Communities Associated with Sphagnum fallax (Bryophyta)

  • H. Nguyen-VietEmail author
  • D. Gilbert
  • E. A. D. Mitchell
  • P.-M. Badot
  • N. Bernard


Ecotoxicological studies usually focus on single microbial species under controlled conditions. As a result, little is known about the responses of different microbial functional groups or individual species to stresses. In an aim to assess the response of complex microbial communities to pollution in their natural habitat, we studied the effect of a simulated lead pollution on the microbial community (bacteria, cyanobacteria, protists, fungi, and micrometazoa) living on Sphagnum fallax. Mosses were grown in the laboratory with 0 (control), 625, and 2,500 μg L−1 of Pb2+ diluted in a standard nutrient solution and were sampled after 0, 6, 12, and 20 weeks. The biomasses of bacteria, microalgae, testate amoebae, and ciliates were dramatically and significantly decreased in both Pb addition treatments after 6, 12, and 20 weeks in comparison with the control. The biomass of cyanobacteria declined after 6 and 12 weeks in the highest Pb treatment. The biomasses of fungi, rotifers, and nematodes decreased along the duration of the experiment but were not significantly affected by lead addition. Consequently, the total microbial biomass was lower for both Pb addition treatments after 12 and 20 weeks than in the controls. The community structure was strongly modified due to changes in the densities of testate amoebae and ciliates, whereas the relative contribution of bacteria to the microbial biomass was stable. Differences in responses among the microbial groups suggest changes in the trophic links among them. The correlation between the biomass of bacteria and that of ciliates or testate amoebae increased with increasing Pb loading. We interpret this result as an effect on the grazing pathways of these predators and by the Pb effect on other potential prey (i.e., smaller protists). The community approach used here complements classical ecotoxicological studies by providing clues to the complex effect of pollutant-affecting organisms both directly and indirectly through trophic effects and could potentially find applications for pollution monitoring.


Microbial Community Microalgae Microbial Group Total Microbial Biomass Testate Amoeba 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Marie-Laure Toussaint for her assistance in Pb analysis, Stéphanie Nicopoulos for determining cyanobacterial species, and Dominique Rieffel for nematode measurement. We express our acknowledgements to Michael Coeurdassier, Jérôme Cortet, and Renaud Scheifler for giving comments to improve the experimental design and helpful discussion throughout the work. Jyrki Jauhianen (University of Helsinki, Finland), Catherine Rausch, and Sandrine Gombert (Muséum National d’Histoire Naturelle de Paris, France) are acknowledged for discussion on Sphagnum growth and supplying references on this issue. We thank the two anonymous reviewers for helpful comments on an earlier version of the manuscript. H. Nguyen-Viet has been supported by the University of Franche-Comté through a temporary lecturer contract (2004–2006) and by the European Science Foundation through an exchange grant (program RSTCB, ESF, 2006). E. Mitchell was at the University of Alaska Anchorage at the onset of this experiment and was later supported by the Swiss contribution to EU project RECIPE (no. EVK2-2002-00269).


  1. 1.
    Adams, SM, Greeley, MS (2000) Ecotoxicological indicators of water quality: using multi-response indicators to assess the health of aquatic ecosystems. Water, Air and Soil Pollution: Focus 123: 103–115CrossRefGoogle Scholar
  2. 2.
    Ashelford, KE, Fry, JC, Day, MJ, Hill, KE, Learner, MA, Marchesi, JR, Perkins, CD, Weightman, AJ (1997) Using microcosms to study gene transfer in aquatic habitats. FEMS Microbiol Ecol 23: 81–94CrossRefGoogle Scholar
  3. 3.
    Bååth, E, Díaz-Raviña, M, Bakken, LR (2005) Microbial biomass, community structure and metal tolerance of a naturally Pb-enriched forest soil. Microb Ecol 50: 496–505PubMedCrossRefGoogle Scholar
  4. 4.
    Borsheim, KY, Bratbak, G (1987) Cell volume to cell carbon conversion factors for bacteriovorous Monas sp. enriched from seawater. Mar Ecol Prog Ser 36: 171–175Google Scholar
  5. 5.
    Bratbak, G (1985) Bacterial biovolume and biomass estimations. Appl Environ Microbiol 46: 491–498Google Scholar
  6. 6.
    Charman, DJ, Warner, BG (1992) Relationship between testate amoebae (protozoa, rhizopoda) and microenvironmental parameters on a forested peatland in northeastern Ontario. Can J Zool Rev Can Zool 70: 2474–2482CrossRefGoogle Scholar
  7. 7.
    Clement, WH, Newman, MC (2003) Community Ecotoxicology. Wiley, New YorkGoogle Scholar
  8. 8.
    DePhilippis, R, Sili, C, Paperi, R, Vincenzini, M (2001) Expolysaccharide-producing cyanobacteria and their possible exploitation: a review. J Appl Phycol 13: 293–299CrossRefGoogle Scholar
  9. 9.
    Ekelund, F, Ronn, R, Christensen, S (2001) Distribution with depth of protozoa, bacteria and fungi in soil profiles from three Danish forest sites. Soil Biol Biochem 33: 475–481CrossRefGoogle Scholar
  10. 10.
    Epstein, SS, Shiaris, MP (1992) Size-selective grazing of coastal bacterioplankton by natural assemblages of pigmented flagellates, colorless flagellates, and ciliates. Microb Ecol 23: 211–225CrossRefGoogle Scholar
  11. 11.
    Fernandez-Leborans, G, Olalla Herrero, Y (2000) Toxicity and bioaccumulation of lead and cadmium in marine protozoan communities. Ecotoxicol Environ Saf 47: 266–276PubMedCrossRefGoogle Scholar
  12. 12.
    Foissner, W (1999) Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agric Ecosyst Environ 74: 95–112CrossRefGoogle Scholar
  13. 13.
    Gilbert, D, Amblard, C, Bourdier, G, Francez, AJ (1998) Short-term effect of nitrogen enrichment on the microbial communities of a peatland. Hydrobiologia 374: 111–119CrossRefGoogle Scholar
  14. 14.
    Gilbert, D, Amblard, C, Bourdier, G, Francez, A-J (1998) The microbial loop at the surface of a peatland: structure, function, and impact of nutrient input. Microb Ecol 35: 83–93PubMedCrossRefGoogle Scholar
  15. 15.
    Hallberg, KB, Johnson, DB (2005) Microbiology of a wetland ecosystem constructed to remediate mine drainage from a heavy metal mine. Sci Total Environ 338: 53–66PubMedCrossRefGoogle Scholar
  16. 16.
    Harithsa, S, Kerkarb, S, Loka Bharathi, PA (2002) Mercury and lead tolerance in hypersaline sulfate-reducing bacteria. Mar Pollut Bull 44: 726–732PubMedCrossRefGoogle Scholar
  17. 17.
    Kalin, M, Wheeler, WN, Meinrath, G (2004) The removal of uranium from mining waste water using algal/microbial biomass. J Environ Radioact 78: 151–177CrossRefGoogle Scholar
  18. 18.
    Kozdroj, J, van Elsas, JD (2001) Structural diversity of microbial communities in arable soils of a heavily industrialised area determined by PCR-DGGE fingerprinting and FAME profiling. Appl Soil Ecol 17: 31–42CrossRefGoogle Scholar
  19. 19.
    Lacroix, P, Moncorge, S (1999) Tourbière “Sur les Seignes” (Frambouhans, les Ecorces - 25): Espace Naturel Comtois Doub Nature Environnement. 47Google Scholar
  20. 20.
    Leborans, GF, Herrero, YO, Novillo, A (1998) Toxicity and bioaccumulation of lead in marine protozoa communities. Ecotoxicol Environ Saf 39: 172–178CrossRefGoogle Scholar
  21. 21.
    Madoni, P, Davoli, D, Gorbi, G, Vescovi, L (1996) Toxic effect of heavy metals on the activated sludge protozoan community. Water Res 30: 135–141CrossRefGoogle Scholar
  22. 22.
    Markert, BA, Breure, AM, Zechmeister, HG (2003) Bioindicators and Biomonitors: Principles, Concepts, and Applications. Elsevier 997, AmsterdamGoogle Scholar
  23. 23.
    Martin-Gonzalez, A, Borniquel, S, Diaz, S, Ortega, R, Gutierrez, JC (2005) Ultrastructural alterations in ciliated protozoa under heavy metal exposure. Cell Biol Int 29: 119–126PubMedCrossRefGoogle Scholar
  24. 24.
    Mitchell, EAD, Borcard, D, Buttler, AJ, Grosvernier, P, Gilbert, D, Gobat, JM (2000) Horizontal distribution patterns of testate amoebae (Protozoa) in a Sphagnum magellanicum carpet. Microb Ecol 39: 290–300PubMedGoogle Scholar
  25. 25.
    Mitchell, EAD, Gilbert, D, Buttler, A, Grosvernier, P, Amblard, C, Gobat, J-M (2003) Structure of microbial communities in Sphagnum peatlands and effect of atmospheric carbon dioxide enrichment. Microb Ecol 46: 187–199PubMedCrossRefGoogle Scholar
  26. 26.
    Mitsch, WJ, Gosselink, JG (2000) Wetlands, 3rd edn. Wiley, New YorkGoogle Scholar
  27. 27.
    Muhammad, A, Xu, J, Li, Z, Wang, H, Yao, H (2005) Effects of lead and cadmium nitrate on biomass and substrate utilization pattern of soil microbial communities. Chemosphere 60: 508–514PubMedCrossRefGoogle Scholar
  28. 28.
    Nguyen-Viet, H, Bernard, N, Mitchell, EAD, Cortet, J, Badot, P-M, Gilbert, D Relationship between testate amoeba (Protist) communities and atmospheric heavy metals accumulated in Barbula indica (Bryophyta) in Vietnam. Microb Ecol,
  29. 29.
    Nguyen-Viet, H, Gilbert, D, Bernard, N, Mitchell, EAD, Badot, PM (2004) Relationship between atmospheric pollution characterized by NO2 concentrations and testate amoebae abundance and diversity. Acta Protozool 43: 233–329Google Scholar
  30. 30.
    Nicolau, A, Martins, MJ, Mota, M, Lima, N (2005) Effect of copper in the protistan community of activated sludge. Chemosphere 58: 605–614PubMedCrossRefGoogle Scholar
  31. 31.
    Patterson, RT, Barker, T, Burbidge, SM (1996) Arcellaceans (thecamoebians) as proxies of arsenic and mercury contamination in northeastern Ontario lakes. J Foraminifer Res 26: 172–183CrossRefGoogle Scholar
  32. 32.
    Paulin, JJ (1996) Morphology and cytology in ciliates. In: Hausmann, K, Bradbury, PC (Eds.) Ciliates. Cells as Organisms, Gustav Fischer, Stuttgart, pp 1–40Google Scholar
  33. 33.
    Pennanen, T (2001) Microbial communities in boreal coniferous forest humus exposed to heavy metals and changes in soil pH—a summary of the use of phospholipid fatty acids, Biolog(R) and 3H-thymidine incorporation methods in field studies. Geoderma 100: 91–126CrossRefGoogle Scholar
  34. 34.
    Piccinni, E, Albergoni, V (1996) Cadmium detoxification in protists. Comp Biochem Physiol C 113: 141–147Google Scholar
  35. 35.
    Reinhardt, EG, Dalby, AP, Kumar, A, Patterson, RT (1998) Arcellaceans as pollution indicators in mine tailing contaminated lakes near Cobalt, Ontario, Canada. Micropaleontology 44: 131–148CrossRefGoogle Scholar
  36. 36.
    Rudolph, H, Kirchhoff, M, Gliesmann, G (1988) Sphagnum culture techniques. In: Glime JM (Ed.) Methods in Bryology. Proceedings of the Bryological Methods Workshop, Mainz, Hattori Botanical Laboratory, Nichinan, pp 25–34Google Scholar
  37. 37.
    Shi, W, Becker, J, Bischoff, M, Turco, RF, Konopka, AE (2002) Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination. Appl Environ Microbiol 68: 3859–3866PubMedCrossRefGoogle Scholar
  38. 38.
    Slaveykova, VI, Wilkinson, KJ (2002) Physicochemical aspects of lead bioaccumulation by Chlorella vulgaris. Environ Sci Technol 36: 969–975PubMedCrossRefGoogle Scholar
  39. 39.
    Sugiura, K (1996) The use of an aquatic microcosm for pollution effects assessment. Water Res 30: 1801–1812CrossRefGoogle Scholar
  40. 40.
    Suhadolc, M, Schroll, R, Gattinger, A, Schloter, M, Munch, JC, Lestan, D (2004) Effects of modified Pb-, Zn-, and Cd-availability on the microbial communities and on the degradation of isoproturon in a heavy metal contaminated soil. Soil Biol Biochem 36: 1943–1954CrossRefGoogle Scholar
  41. 41.
    Traunspurger, W, Schafer, H, Remde, A (1996) Comparative investigation on the effect of a herbicide on aquatic organisms in single species tests and aquatic microcosms. Chemosphere 33: 1129–1141CrossRefGoogle Scholar
  42. 42.
    Turpeinen, R, Kairesalo, T, Haggblom, MM (2004) Microbial community structure and activity in arsenic, chromium and copper contaminated soils. FEMS Microbiol Ecol 47: 39–50CrossRefPubMedGoogle Scholar
  43. 43.
    Utermölh, H (1958) Zur vervollkommnung der quantative phytoplankton-methodik. Mitteilungen aus Institut Verhein Limnologie 9: 1–38Google Scholar
  44. 44.
    Van den Brink, PJ, Ter Braak, CJF (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18: 138–148CrossRefGoogle Scholar
  45. 45.
    Weisse, T, Muller, H, Pinto-Coelho, RM, Schweizer, A, Springmann, D, Baldringer, G (1990) Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnol Oceanogr 35: 781–794CrossRefGoogle Scholar
  46. 46.
    Wu, L (2004) Review of 15 years of research on ecotoxicology and remediation of land contaminated by agricultural drainage sediment rich in selenium. Ecotoxicol Environ Saf 57: 257–269PubMedCrossRefGoogle Scholar
  47. 47.
    Yeates, GW, Foissner, W (1995) Testate amebas as predators of nematodes. Biol Fertil Soils 20: 1–7CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • H. Nguyen-Viet
    • 1
    Email author
  • D. Gilbert
    • 1
  • E. A. D. Mitchell
    • 2
  • P.-M. Badot
    • 1
  • N. Bernard
    • 1
  1. 1.Laboratory of Environmental Biology, USC INRA, EA 3184University of Franche-ComtéBesançonFrance
  2. 2.Department of Public Health and EpidemiologySwiss Tropical InstituteBaselSwitzerland

Personalised recommendations