Skip to main content

Soil microbial respiration and PICT responses to an industrial and historic lead pollution: a field study

Abstract

We performed a field investigation to study the long-term impacts of Pb soil contamination on soil microbial communities and their catabolic structure in the context of an industrial site consisting of a plot of land surrounding a secondary lead smelter. Microbial biomass, catabolic profiles, and ecotoxicological responses (PICT) were monitored on soils sampled at selected locations along 110-m transects established on the site. We confirmed the high toxicity of Pb on respirations and microbial and fungal biomasses by measuring positive correlations with distance from the wall factory and negative correlation with total Pb concentrations. Pb contamination also induced changes in microbial and fungal catabolic structure (from carbohydrates to amino acids through carboxylic malic acid). Moreover, PICT measurement allowed to establish causal linkages between lead and its effect on biological communities taking into account the contamination history of the ecosystem at community level. The positive correlation between qCO2 (based on respiration and substrate use) and PICT suggested that the Pb stress-induced acquisition of tolerance came at a greater energy cost for microbial communities in order to cope with the toxicity of the metal. In this industrial context of long-term polymetallic contamination dominated by Pb in a field experiment, we confirmed impacts of this metal on soil functioning through microbial communities, as previously observed for earthworm communities.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biol Biochem 10:215–221

    Article  CAS  Google Scholar 

  2. Anderson JPE, Domsch KH (1985) Maintenance carbon requirements of actively-metabolizing microbial populations under in situ conditions. Soil Biol Biochem 17:197–203

    Article  CAS  Google Scholar 

  3. Anderson JPE, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25:393–395

    Article  Google Scholar 

  4. Anderson JAH, Hooper MJ, Zak JC, Cox SB (2009) Characterization of the structural and functional diversity of indigenous soil microbial communities in smelter-impacted and nonimpacted soils. Environ Toxicol Chem 28:534–541

    Article  CAS  Google Scholar 

  5. Azarbad H, Niklinska M, van Gestel CAM, van Straalen NM, Roling WFM, Laskowski R (2013) Microbial community structure and functioning along metal pollution gradients. Environ Toxicol Chem 32:1992–2002

    Article  CAS  Google Scholar 

  6. Baath E (1992) Measurement of heavy soil bacteria using thymidine incorporation into bacteria extracted after homogenization-centrifugation. Soil Biol Biochem 11:1167–1172

    Article  Google Scholar 

  7. Baath E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963

    Article  CAS  Google Scholar 

  8. Baath E, Dıaz-Ravina M, Bakken LR (2005) Microbial biomass, community structure and metal tolerance of a naturally Pb-enriched forest soil. Microb Ecol 50:496–505

    Article  CAS  Google Scholar 

  9. Banning NC, Lalor BM, Cookson WR, Grigg AH, Murphy DV (2012) Analysis of soil microbial community level physiological profiles in native and post-mining rehabilitation forest: which substrates discriminate? Appl Soil Ecol 56:27–34

    Article  Google Scholar 

  10. Bárcenas-Moreno G, Rousk J, Bååth E (2011) Fungal and bacterial recolonisation of acid and alkaline forest soils following artificial heat treatments. Soil Biol Biochem 43:1023–1033

    Article  Google Scholar 

  11. Ben Sassi M, Dolinger J, Renault P, Tlili A, Bérard A (2012) The FungiResp method: an application of the MicroResp™ method to assess fungi in microbial communities as soil biological indicators. Ecol Indic 23:482–490

    Article  Google Scholar 

  12. Bérard A, Dorigo U, Humbert JF, Leboulanger C, Seguin F (2002) PICT (Pollution-Induced Community Tolerance) concept applied to algal communities: a tool for real risk-assessment in aquatic sciences. Inter J Limnol 38:247–261

  13. Bérard A, Bouchet T, Sévenier G, Pablo AL, Gros R (2011) Resilience of soil microbial communities impacted by severe drought and high temperature in the context of Mediterranean heat waves. Eur J Soil Biol 47:333–342

    Article  Google Scholar 

  14. Bérard A, Mazzia C, Sappin-Didier V, Capowiez L, Capowiez Y (2014) Use of the MicroResp™ method to assess Pollution-Induced Community Tolerance in the context of metal soil contamination. Ecol Indic 40:27–33

    Article  Google Scholar 

  15. Blanck H (2002) A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Hum Ecol Risk Assess 8:1003–1034

    Article  Google Scholar 

  16. Blanck H, Wänkberg S-Å, Molander S (1988) Pollution-induced community tolerance - a new ecotoxicological tool. In: Cairs J Jr, Pratt JR (eds) Functional testing of aquatic biota for estimating hazards of chemicals. ASTM STP 988, Philadelphia, pp 219–230

    Chapter  Google Scholar 

  17. Boivin MEY, Breure AM, Posthuma L, Rutgers M (2002) Determination of field effects of contaminants—significance of Pollution-Induced Community Tolerance. Hum Ecol Risk Asses 8:1035–1055

    Article  Google Scholar 

  18. Boivin MEY, Greve GD, Kools SAE, van der Wurff AWG, Leeflang P, Smit E, Breure AM, Rutgers M, van Straalen NM (2006) Discriminating between effects of metals and natural variables in terrestrial bacterial communities. Appl Soil Ecol 34:103–113

    Article  Google Scholar 

  19. Brookes PC (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279

    Article  CAS  Google Scholar 

  20. Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69(6):3593–3599

    Article  CAS  Google Scholar 

  21. Chander K, Klein T, Eberhardt U, Joergensen RG (2002) Decomposition of carbon-14-labelled wheat straw in repeatedly fumigated and non-fumigated soils with different levels of heavy metal contamination. Biol Fertil Soils 35:86–91

    Article  CAS  Google Scholar 

  22. Chapman SJ, Campbell CD, Artz RE (2007) Assessing CLPPs using MicroResp™ - A comparison with biolog and multi-SIR. J Soil Sed 7(6):406–410

    Article  Google Scholar 

  23. Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package-I: one-table methods. R News 4:5–10

    Google Scholar 

  24. Clements WH, Rohr JR (2009) Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Crit Rev Environ Toxicol Chem 28:1789–1800

    Article  CAS  Google Scholar 

  25. Degens BP, Schipper LA, Sparling GP, Duncan LC, Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196

    Article  CAS  Google Scholar 

  26. Dilly O, Franke G, Nii-Annang S, Weber K, Freese D, Hüttl R-F (2008) Soil respiratory indicators including carbon isotope characteristics in response to copper. Geomicrob J 25:390–395

    Article  CAS  Google Scholar 

  27. Dumat C, Quenea K, Bermond A, Toinen S, Benedetti MF (2006) Study of the trace metal ion influence on the turnover of soil organic matter in cultivated contaminated soils. Environ Pollut 142:521–529. doi:10.1016/j.envpol.2005.10.027

    Article  CAS  Google Scholar 

  28. Flynn HC, Meharg AA, Bowyer PK, Paton GI (2003) Antimony bioavailability in mine soils. Environ Pollut 124:93–100

    Article  CAS  Google Scholar 

  29. Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 41:2031–2037

    Article  CAS  Google Scholar 

  30. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  Google Scholar 

  31. Jänsch S, Römbke J, Schallnaß H-J, Terytze K (2007) Derivation of Soil Values for the Path ‘Soil – Soil Organisms’ for Metals and Selected Organic Compounds Using Species Sensitivity Distributions. Env Sci Pollut Res 14(5):308–318

    Article  Google Scholar 

  32. Kizilkaya R, Aşkin T, Bayrakli B, Sağlam M (2004) Microbiological characteristics of soils contaminated by heavy metals. Eur J Soil Biol 40:95–102

    Article  CAS  Google Scholar 

  33. Lalor BM, Cookson WR, Murphy DV (2007) Comparison of two methods that assess soil community level physiological profiles in a forest ecosystem. Soil Biol Biochem 39:454–462

    Article  CAS  Google Scholar 

  34. Lekfeldt JDS, Magid J, Holm PE, Nybroe O, Brandt KK (2014) Evaluation of the leucine incorporation technique for detection of pollution-induced community tolerance to copper in a long-term agricultural field trial with urban waste fertilizers. Environmental Pollution 194:78–85

    Article  CAS  Google Scholar 

  35. Lévêque T, Capowiez Y, Schreck E, Mazzia C, Auffan M, Foucault Y, Austruy A, Dumat C (2013) Assessing ecotoxicity and uptake of metals and metalloids in relation to two different earthworm species (Eiseina hortensis and Lumbricus terrestris). Environ Pollut 179:232–241. doi:10.1016/j.envpol.2013.03.066

    Article  Google Scholar 

  36. Lévêque T, Capowiez Y, Schreck E, Mombo S, Mazzia C, Foucault Y, Dumat C (2015) Effects of historic metal(loid) pollution on earthworm communities. STOTEN 511:738–746

    Google Scholar 

  37. Masto RE, Ahirwar R, George J, Ram LC, Selvi VA (2011) Soil biological and biochemical response to Cd exposure. Open J Soil Sci 1:8–15

    Article  CAS  Google Scholar 

  38. Nahmani J, Rossi JP (2003) Soil macro-invertebrates as indicators of pollution by heavy metals. Comptes Rendus Biologies 326:295–303

    Article  CAS  Google Scholar 

  39. Niu ZX, Xiaodong XD, Sun LN, Sun TH (2013) Dynamics of three organic acids (malic, acetic and succinic acid) in sunflower exposed to cadmium and lead. Internat J Phytoremed 15:690–702

    Article  CAS  Google Scholar 

  40. Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Engin 37:1889–1894

    Article  Google Scholar 

  41. Puglisi E, Hamon R, Vasileiadis S, Coppolecchia D, Trevisan M (2012) Adaptation of soil microorganisms to trace element contamination: a review of mechanisms, methodologies, and consequences for risk Assessment and remediation. Crit Rev Environ Sci Tech 42:2435–2470

    Article  Google Scholar 

  42. Quenea K, Lamy I, Winterton P, Bermond A, Dumat C (2009) Interactions between metals and soil organic matter in various particle size fractions of soil contaminated with waste water. Geoderma 149:217–223. doi:10.1016/j.geoderma.2008.11.037

    Article  CAS  Google Scholar 

  43. Rusk JA, Hamon RE, Stevens DP, McLaughlin MJ (2004) Adaptation of soil biological nitrification to heavy metals. Environ Sci Technol 38:3092–3097

    Article  CAS  Google Scholar 

  44. Schreck E, Foucault Y, Geret F, Pradere P, Dumat C (2011) Influence of soil ageing on bioavailability and ecotoxicity of lead carried by process waste metallic ultrafine particles. Chemosphere 85:1555–1562. doi:10.1016/j.chemosphere.2011.07.059

    Article  CAS  Google Scholar 

  45. Shahid M, Xiong T, Masood N, Lévêque T, Quenea K, Austruy A, Foucault Y, Dumat C (2014) Influence of plant species and phosphorus amendments on metal speciation and bio- availability in a smelter impacted soil: a case study of food chain contamination. J. Soils Sediments 14:655–65

    Article  Google Scholar 

  46. Sharma SS, Dietz K-J (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    Article  CAS  Google Scholar 

  47. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    Article  CAS  Google Scholar 

  48. Stefanowicz AM, Niklinska M, Laskowski R (2009) Pollution-induced tolerance of soil bacterial communities in meadow and forest ecosystems polluted with heavy metals. Eur J Soil Biol 45:363–369

    Article  CAS  Google Scholar 

  49. Stefanowicz AM, Niklinska M, Kapusta P, Szarek-Łukaszewska G (2010) Pine forest and grassland differently influuence the response of soil microbial communities to metal contamination. Sci Total Environ 408:6134–6141

    Article  CAS  Google Scholar 

  50. Tlili A, Marechal M, Montuelle B, Volat B, Dorigo U, Bérard A (2011a) Use of the MicroResp™ method to assess pollution-induced community tolerance to metals for lotic biofilms. Environ Pollut 15:18–24

    Article  Google Scholar 

  51. Tlili A, Marechal M, Bérard A, Volat B, Montuelle B (2011b) Enhanced co-tolerance and co-sensitivity from long-term metal exposures of heterotrophic and autotrophic components of fluvial biofilms. Sci Total Environ 409(20):4335–4343

    Article  CAS  Google Scholar 

  52. Tlili A, Bérard A, Blanck H, Bouchez A, Cassio F, Eriksson Km, Morin S, Montuelle B, Navarro E, Pascoal C, Pesce S, Schmitt-Jansen M, Behra R (2015) Pollution-induced community tolerance (PICT): towards an ecologically relevant risk assessment of chemicals in aquatic systems, Freswater Biol. online: 8 APR 2015. http://dx.doi.org/10.1111/fwb.12558

  53. Wakelin S, Gerard E, Black A, Hamonts K, Condron L, Yuan T, van Nostrand J, Zhou J, O’Callaghan M (2014) Mechanisms of pollution induced community tolerance in a soil microbial community exposed to Cu. Environ Poll 190:1–9

    Article  CAS  Google Scholar 

  54. Wang F, Yaoa J, Sia Y, Chena H, Russela M, Chena K, Qiana Y, Zarayb G, Bramantic E (2010) Short-time effect of heavy metals upon microbial community activity. J Hazard Mater 173:510–516

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge ADEME (French Agency of the Environment and Energy) as well as the company STCM (Société de Traitements Chimiques des Métaux) for their technical help and financial support. This work was also supported by the INSU-EC2CO program (Biotuba Project). We thank G. Sévenier for his technical support. The text was language-edited by ATT (an ISO 9001:2008-certified technical and scientific translation and editing services company).

Compliance with ethical standards

The reported work in this paper submitted for publication in the journal “Environmental Science and Pollution Research” is an original one and has not been submitted for publication elsewhere.

The consent of all the authors of this paper has been obtained for submitting the paper to the journal “Environmental Science and Pollution Research”.

Conflict of interest

Annette Bérard declares that she has no conflict of interest

Line Capowiez declares that she has no conflict of interest

Stéphane Mombo declares that he has no conflict of interest

Eva Schreck declares that she has no conflict of interest

Camille Dumat declares that she has no conflict of interest

Frédéric Deola declares that she has no conflict of interest

Yvan Capowiez declares that he has no conflict of interest

This article does not contain any studies with human or animal subjects.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Annette Bérard.

Additional information

Research highlights

-PICT-assays with FungiResp technique to assess metal impact on soil microbial communities

-PICT observed in a long-term field study with high-Pb soil contamination gradient

-Long-term metal contamination induced a shift in catabolic structure

-Metabolic quotient increased with pollution-induced community tolerance

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PPTX 132 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bérard, A., Capowiez, L., Mombo, S. et al. Soil microbial respiration and PICT responses to an industrial and historic lead pollution: a field study. Environ Sci Pollut Res 23, 4271–4281 (2016). https://doi.org/10.1007/s11356-015-5089-z

Download citation

Keywords

  • Microbial ecotoxicology
  • Soil microbial communities
  • Microbial physiological traits
  • Pollution-induced community tolerance
  • Substrate-induced respiration
  • Heavy metals
  • Lead
  • MicroResp™