Skip to main content

Advertisement

Springer Nature Link
Log in

Soil Properties and Multi-Pollution Affect Taxonomic and Functional Bacterial Diversity in a Range of French Soils Displaying an Anthropisation Gradient

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The intensive industrial activities of the twentieth century have left behind highly contaminated wasteland soils. It is well known that soil parameters and the presence of pollutants shape microbial communities. But in such industrial waste sites, the soil multi-contamination with organic (polycyclic aromatic hydrocarbons, PAH) and metallic (Zn, Pb, Cd) pollutants and long-term exposure may induce a selection pressure on microbial communities that may modify soil functioning. The aim of our study was to evaluate the impact of long-term multi-contamination and soil characteristics on bacterial taxonomic and functional diversity as related to the carbon cycle. We worked on 10 soils from northeast of France distributed into three groups (low anthropised controls, slag heaps, and settling ponds) based on their physico-chemical properties (texture, C, N) and pollution level. We assessed bacterial taxonomic diversity by 16S rDNA Illumina sequencing, and functional diversity using Biolog® and MicroResp™ microtiter plate tools. Although taxonomic diversity at the phylum level was not different among the soil groups, many operational taxonomic units were influenced by metal or PAH pollution, and by soil texture and total nitrogen content. Functional diversity was not influenced by PAH contamination while metal pollution selected microbial communities with reduced metabolic functional diversity but more tolerant to zinc. Limited microbial utilisation of carbon substrates in metal-polluted soils was mainly due to the nitrogen content. Based on these two observations, we hypothesised that reduced microbial activity and lower carbon cycle–related functional diversity may have contributed to the accumulation of organic matter in the soils that exhibited the highest levels of metal pollution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  1. (2016) BASOL. http://basol.developpement-durable.gouv.fr/. Accessed 11 Sep 2017

  2. Rachwał M, Magiera T, Wawer M (2015) Coke industry and steel metallurgy as the source of soil contamination by technogenic magnetic particles, heavy metals and polycyclic aromatic hydrocarbons. Chemosphere 138:863–873. https://doi.org/10.1016/j.chemosphere.2014.11.077

    Article  CAS  PubMed  Google Scholar 

  3. Joimel S, Cortet J, Jolivet CC, Saby NPA, Chenot ED, Branchu P, Consalès JN, Lefort C, Morel JL, Schwartz C (2016) Physico-chemical characteristics of topsoil for contrasted forest, agricultural, urban and industrial land uses in France. Sci Total Environ 545:40–47. https://doi.org/10.1016/j.scitotenv.2015.12.035

    Article  CAS  PubMed  Google Scholar 

  4. Wilcke W (2000) SYNOPSIS polycyclic aromatic hydrocarbons (PAHs) in soil—a review. J Plant Nutr Soil Sci 163:229–248. https://doi.org/10.1002/1522-2624(200006)163:3<229::AID-JPLN229>3.0.CO;2-6

    Article  CAS  Google Scholar 

  5. Dhelft P (1994) Épuration du gaz de haut fourneau. Tech L’ingénieur Métaux Ferr Élabor Métal Prim TIB366DUO. (ref. article : m7422)

  6. Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84. https://doi.org/10.1016/j.envpol.2004.04.015

    Article  CAS  PubMed  Google Scholar 

  7. Janssen CR, Heijerick DG, De Schamphelaere KAC, Allen HE (2003) Environmental risk assessment of metals: tools for incorporating bioavailability. Environ Int 28:793–800. https://doi.org/10.1016/S0160-4120(02)00126-5

    Article  CAS  PubMed  Google Scholar 

  8. Kim R-Y, Yoon J-K, Kim T-S, Yang JE, Owens G, Kim KR (2015) Bioavailability of heavy metals in soils: definitions and practical implementation—a critical review. Environ Geochem Health 37:1041–1061. https://doi.org/10.1007/s10653-015-9695-y

    Article  CAS  PubMed  Google Scholar 

  9. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368. https://doi.org/10.1007/BF00129093

    Article  CAS  Google Scholar 

  10. Hatzinger PB, Alexander M (1995) Effect of aging of chemicals in soil on their biodegradability and extractability. Environ Sci Technol 29:537–545. https://doi.org/10.1021/es00002a033

    Article  CAS  PubMed  Google Scholar 

  11. Cébron A, Faure P, Lorgeoux C, Ouvrard S, Leyval C (1987) (2013) Experimental increase in availability of a PAH complex organic contamination from an aged contaminated soil: consequences on biodegradation. Environ Pollut Barking Essex 177:98–105. https://doi.org/10.1016/j.envpol.2013.01.043

    Article  CAS  Google Scholar 

  12. Abdu N, Abdullahi AA, Abdulkadir A (2017) Heavy metals and soil microbes. Environ Chem Lett 15:65–84. https://doi.org/10.1007/s10311-016-0587-x

    Article  CAS  Google Scholar 

  13. Andreoni V, Cavalca L, Rao MA, Nocerino G, Bernasconi S, Dell’Amico E, Colombo M, Gianfreda L (2004) Bacterial communities and enzyme activities of PAHs polluted soils. Chemosphere 57:401–412. https://doi.org/10.1016/j.chemosphere.2004.06.013

    Article  CAS  PubMed  Google Scholar 

  14. Grant RJ, Muckian LM, Clipson NJW, Doyle EM (2007) Microbial community changes during the bioremediation of creosote-contaminated soil. Lett Appl Microbiol 44:293–300. https://doi.org/10.1111/j.1472-765X.2006.02066.x

    Article  CAS  PubMed  Google Scholar 

  15. Sawulski P, Clipson N, Doyle E (2014) Effects of polycyclic aromatic hydrocarbons on microbial community structure and PAH ring hydroxylating dioxygenase gene abundance in soil. Biodegradation 25:835–847. https://doi.org/10.1007/s10532-014-9703-4

    Article  CAS  PubMed  Google Scholar 

  16. Sutton NB, Maphosa F, Morillo JA, Abu al-Soud W, Langenhoff AAM, Grotenhuis T, Rijnaarts HHM, Smidt H (2013) Impact of long-term diesel contamination on soil microbial community structure. Appl Environ Microbiol 79:619–630. https://doi.org/10.1128/AEM.02747-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kelly JJ, Häggblom M, Tate RL (1999) Changes in soil microbial communities over time resulting from one time application of zinc: a laboratory microcosm study. Soil Biol Biochem 31:1455–1465. https://doi.org/10.1016/S0038-0717(99)00059-0

    Article  CAS  Google Scholar 

  18. Moffett BF, Nicholson FA, Uwakwe NC, Chambers BJ, Harris JA, Hill TCJ (2003) Zinc contamination decreases the bacterial diversity of agricultural soil. FEMS Microbiol Ecol 43:13–19. https://doi.org/10.1111/j.1574-6941.2003.tb01041.x

    Article  CAS  PubMed  Google Scholar 

  19. Cébron A, Norini M-P, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDα) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73:148–159. https://doi.org/10.1016/j.mimet.2008.01.009

    Article  CAS  PubMed  Google Scholar 

  20. Diaz-Ravina M, Baath E (1996) Development of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels. Appl Environ Microbiol 62:2970–2977

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 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 Int J 8:1003–1034. https://doi.org/10.1080/1080-700291905792

    Article  Google Scholar 

  22. Bourceret A, Cébron A, Tisserant E, Poupin P, Bauda P, Beguiristain T, Leyval C (2016) The bacterial and fungal diversity of an aged PAH- and heavy metal-contaminated soil is affected by plant cover and edaphic parameters. Microb Ecol 71:711–724. https://doi.org/10.1007/s00248-015-0682-8

    Article  CAS  PubMed  Google Scholar 

  23. Lindgren JF, Hassellöv I-M, Nyholm JR, Östin A, Dahllöf I (2017) Induced tolerance in situ to chronically PAH exposed ammonium oxidizers. Mar Pollut Bull 120:333–339. https://doi.org/10.1016/j.marpolbul.2017.05.044

    Article  CAS  PubMed  Google Scholar 

  24. Thavamani P, Malik S, Beer M, Megharaj M, Naidu R (2012) Microbial activity and diversity in long-term mixed contaminated soils with respect to polyaromatic hydrocarbons and heavy metals. J Environ Manage 99:10–17. https://doi.org/10.1016/j.jenvman.2011.12.030

    Article  CAS  PubMed  Google Scholar 

  25. Lu M, Xu K, Chen J (2013) Effect of pyrene and cadmium on microbial activity and community structure in soil. Chemosphere 91:491–497. https://doi.org/10.1016/j.chemosphere.2012.12.009

    Article  CAS  PubMed  Google Scholar 

  26. Markowicz A, Cycon M, Piotrowska-Seget Z (2016) Microbial community structure and diversity in long-term hydrocarbon and heavy metal contaminated soils. Int J Environ Res 10:321–332. https://doi.org/10.22059/ijer.2016.57792

    Article  CAS  Google Scholar 

  27. Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108. https://doi.org/10.1016/0038-0717(94)90131-7

    Article  Google Scholar 

  28. 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 69:3593–3599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Boshoff M, De Jonge M, Dardenne F et al (2014) The impact of metal pollution on soil faunal and microbial activity in two grassland ecosystems. Environ Res 134:169–180. https://doi.org/10.1016/j.envres.2014.06.024

    Article  CAS  PubMed  Google Scholar 

  30. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci 103:626–631. https://doi.org/10.1073/pnas.0507535103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schöning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000. https://doi.org/10.1371/journal.pone.0017000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bissett A, Richardson AE, Baker G, Thrall PH (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51:66–78. https://doi.org/10.1016/j.apsoil.2011.08.010

    Article  Google Scholar 

  33. Baize D (2000) Teneurs totales en « métaux lourds » dans les sols français : résultats généraux du programme ASPITET. Courr Environ Inra 39

  34. Cennerazzo J, de Junet A, Audinot J-N, Leyval C (2017) Dynamics of PAHs and derived organic compounds in a soil-plant mesocosm spiked with 13C-phenanthrene. Chemosphere 168:1619–1627. https://doi.org/10.1016/j.chemosphere.2016.11.145

    Article  CAS  PubMed  Google Scholar 

  35. Reid BJ, Stokes JD, Jones KC, Semple KT (2000) Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ Sci Technol 34:3174–3179. https://doi.org/10.1021/es990946c

    Article  CAS  Google Scholar 

  36. Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999. https://doi.org/10.1016/j.soilbio.2005.08.012

    Article  CAS  Google Scholar 

  37. Thomas F, Cébron A (2016) Short-term rhizosphere effect on available carbon sources, phenanthrene degradation, and active microbiome in an aged-contaminated industrial soil. Syst Microbiol 92. https://doi.org/10.3389/fmicb.2016.00092

  38. Lueders T, Wagner B, Claus P, Friedrich MW (2004) Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol 6:60–72. https://doi.org/10.1046/j.1462-2920.2003.00535.x

    Article  CAS  PubMed  Google Scholar 

  39. Felske A, Akkermans ADL, Vos WMD (1998) Quantification of 16S rRNAs in complex bacterial communities by multiple competitive reverse transcription-PCR in temperature gradient gel electrophoresis fingerprints. Appl Environ Microbiol 64:4581–4587

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Cébron A, Beguiristain T, Bongoua-Devisme J, Denonfoux J, Faure P, Lorgeoux C, Ouvrard S, Parisot N, Peyret P, Leyval C (2015) Impact of clay mineral, wood sawdust or root organic matter on the bacterial and fungal community structures in two aged PAH-contaminated soils. Environ Sci Pollut Res Int 22:13724–13738. https://doi.org/10.1007/s11356-015-4117-3

    Article  CAS  PubMed  Google Scholar 

  41. Thion C, Cebron A, Beguiristain T, Leyval C (2012) Long-term in situ dynamics of the fungal communities in a multi-contaminated soil are mainly driven by plants. Fems Microbiol Ecol 82:169–181. https://doi.org/10.1111/j.1574-6941.2012.01414.x

    Article  CAS  PubMed  Google Scholar 

  42. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522. https://doi.org/10.1073/pnas.1000080107

    Article  PubMed  Google Scholar 

  44. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinforma Oxf Engl 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  Google Scholar 

  47. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11. https://doi.org/10.1111/j.1574-6941.2003.tb01040.x

    Article  CAS  PubMed  Google Scholar 

  48. Oksanen J, Blanchet FG, Friendly M, et al (2017) Vegan: community ecology package. R package version 1.17–2. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  49. Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04

    Article  Google Scholar 

  50. Wold S, Ruhe A, Wold H, Dunn IW (1984) The collinearity problem in linear regression. The partial least squares (PLS) approach to generalized inverses. SIAM J Sci Stat Comput 5:735–743. https://doi.org/10.1137/0905052

    Article  Google Scholar 

  51. Wold S, Sjöström M, Eriksson L (2001) PLS-regression: a basic tool of chemometrics. Chemom Intell Lab Syst 58:109–130. https://doi.org/10.1016/S0169-7439(01)00155-1

    Article  CAS  Google Scholar 

  52. Lê Cao KA, Rohart F, Gonzalez I, et al (2017) mixOmics: Omics Data Integration Project. Available from: https://CRAN.R-project.org/package=mixOmics Accessed 1 Jun 2018

  53. Rohart F, Gautier B, Singh A, Cao K-AL (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLOS Comput Biol 13:e1005752. https://doi.org/10.1371/journal.pcbi.1005752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116. https://doi.org/10.1111/j.1365-2389.2010.01314.x

    Article  CAS  Google Scholar 

  55. Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348. https://doi.org/10.3389/fmicb.2012.00348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. https://doi.org/10.1046/j.1351-0754.2003.0556.x

    Article  Google Scholar 

  57. Yin B, Crowley D, Sparovek G, de Melo WJ, Borneman J (2000) Bacterial functional redundancy along a soil reclamation gradient. Appl Environ Microbiol 66:4361–4365. https://doi.org/10.1128/AEM.66.10.4361-4365.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596. https://doi.org/10.1128/AEM.02775-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Reis MP, Barbosa FAR, Chartone-Souza E, Nascimento AMA (2013) The prokaryotic community of a historically mining-impacted tropical stream sediment is as diverse as that from a pristine stream sediment. Extremophiles 17:301–309. https://doi.org/10.1007/s00792-013-0517-9

    Article  CAS  PubMed  Google Scholar 

  60. Gillan DC, Danis B, Pernet P, Joly G, Dubois P (2005) Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Appl Environ Microbiol 71:679–690. https://doi.org/10.1128/AEM.71.2.679-690.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Azarbad H, Niklińska M, Laskowski R, van Straalen NM, van Gestel CAM, Zhou J, He Z, Wen C, Röling WFM (2015) Microbial community composition and functions are resilient to metal pollution along two forest soil gradients. FEMS Microbiol Ecol 91:1–11. https://doi.org/10.1093/femsec/fiu003

    Article  CAS  PubMed  Google Scholar 

  62. Niklińska M, Chodak M, Stefanowicz A (2004) Community level physiological profiles of microbial communities from forest humus polluted with different amounts of Zn, Pb, and Cd—preliminary study with BIOLOG ecoplates. Soil Sci Plant Nutr 50:941–944. https://doi.org/10.1080/00380768.2004.10408558

    Article  Google Scholar 

  63. Nordgren A, Bååth E, Söderström B (1988) Evaluation of soil respiration characteristics to assess heavy metal effects on soil microorganisms using glutamic acid as a substrate. Soil Biol Biochem 20:949–954. https://doi.org/10.1016/0038-0717(88)90109-5

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  65. Stazi SR, Moscatelli MC, Papp R, Crognale S, Grego S, Martin M, Marabottini R (2017) A multi-biological assay approach to assess microbial diversity in arsenic (as) contaminated soils. Geomicrobiol J. 34:183–192. https://doi.org/10.1080/01490451.2016.1189015

    Article  CAS  Google Scholar 

  66. Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2(8):805–814

    Article  CAS  PubMed  Google Scholar 

  67. Rajapaksha RMCP, Tobor-Kapłon MA, Bååth E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70(5):2966–2973. https://doi.org/10.1128/AEM.70.5.2966-2973.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Sullivan TS, McBride MB, Thies JE (2013) Rhizosphere microbial community and Zn uptake by willow (Salix purpurea L.) depend on soil sulfur concentrations in metalliferous peat soils. Appl Soil Ecol 67:53–60. https://doi.org/10.1016/j.apsoil.2013.02.003

    Article  Google Scholar 

  69. Ni C, Horton DJ, Rui J, Henson MW, Jiang Y, Huang X, Learman DR (2016) High concentrations of bioavailable heavy metals impact freshwater sediment microbial communities. Ann Microbiol 66:1003–1012. https://doi.org/10.1007/s13213-015-1189-8

    Article  CAS  Google Scholar 

  70. Epelde L, Lanzén A, Blanco F, Urich T, Garbisu C (2015) Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine. FEMS Microbiol Ecol 91:1–11. https://doi.org/10.1093/femsec/fiu007

    Article  CAS  PubMed  Google Scholar 

  71. Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. https://doi.org/10.1038/nrmicro.2017.87

    Article  CAS  PubMed  Google Scholar 

  72. Sprocati AR, Alisi C, Tasso F, Fiore A, Marconi P, Langella F, Haferburg G, Nicoara A, Neagoe A, Kothe E (2014) Bioprospecting at former mining sites across Europe: microbial and functional diversity in soils. Environ Sci Pollut Res Int 21:6824–6835. https://doi.org/10.1007/s11356-013-1907-3

    Article  CAS  PubMed  Google Scholar 

  73. Ellis RJ, Morgan P, Weightman AJ, Fry JC (2003) Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl Environ Microbiol 69:3223–3230. https://doi.org/10.1128/AEM.69.6.3223-3230.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414. https://doi.org/10.1016/S0038-0717(97)00270-8

    Article  CAS  Google Scholar 

  75. Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu L, Barua S, Barry K, Tringe SG, Watson DB, He Z, Hazen TC, Tiedje JM, Rubin EM, Zhou J (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4:660–672. https://doi.org/10.1038/ismej.2009.154

    Article  CAS  PubMed  Google Scholar 

  76. Chander K, Joergensen RG (2001) Decomposition of 14C glucose in two soils with different amounts of heavy metal contamination. Soil Biol Biochem 33:1811–1816. https://doi.org/10.1016/S0038-0717(01)00108-0

    Article  CAS  Google Scholar 

  77. Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles—a critique. FEMS Microbiol Ecol 42:1–14. https://doi.org/10.1016/S0168-6496(02)00324-0

    Article  CAS  PubMed  Google Scholar 

  78. Lock K (1987) Janssen CR (2005) Influence of soil zinc concentrations on zinc sensitivity and functional diversity of microbial communities. Environ Pollut Barking Essex 136:275–281. https://doi.org/10.1016/j.envpol.2004.12.038

    Article  CAS  Google Scholar 

  79. Ni N, Wang F, Song Y, Shi R, Jia M, Bian Y, Jiang X (2017) Effects of cationic surfactant on the bioaccumulation of polycyclic aromatic hydrocarbons in rice and the soil microbial community structure. RSC Adv 7:41444–41451. https://doi.org/10.1039/C7RA07124H

    Article  CAS  Google Scholar 

  80. Ren G, Teng Y, Ren W, Dai S, Li Z (2016) Pyrene dissipation potential varies with soil type and associated bacterial community changes. Soil Biol Biochem 103:71–85. https://doi.org/10.1016/j.soilbio.2016.08.007

    Article  CAS  Google Scholar 

  81. Padmanabhan P, Padmanabhan S, DeRito C, Gray A, Gannon D, Snape JR, Tsai CS, Park W, Jeon C, Madsen EL (2003) Respiration of 13C-labeled substrates added to soil in the field and subsequent 16S rRNA gene analysis of 13C-labeled soil DNA. Appl Environ Microbiol 69:1614–1622. https://doi.org/10.1128/AEM.69.3.1614-1622.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Trzesicka-Mlynarz D, Ward OP (1995) Degradation of polycyclic aromatic hydrocarbons (PAHs) by a mixed culture and its component pure cultures, obtained from PAH-contaminated soil. Can J Microbiol 41:470–476

    Article  CAS  PubMed  Google Scholar 

  83. Viñas M, Sabaté J, Espuny MJ, Solanas AM (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Appl Environ Microbiol 71:7008–7018. https://doi.org/10.1128/AEM.71.11.7008-7018.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Martirani-Von Abercron S, Marín P, Solsona-Ferraz M et al (2017) Naphthalene biodegradation under oxygen-limiting conditions: community dynamics and the relevance of biofilm-forming capacity. Microb Biotechnol 10:1781–1796. https://doi.org/10.1111/1751-7915.12842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Cébron A, Beguiristain T, Faure P et al (2009) Influence of vegetation on the in situ bacterial community and polycyclic aromatic hydrocarbon (PAH) degraders in aged PAH-contaminated or thermal-desorption-treated soil. Appl Environ Microbiol 75:6322–6330. https://doi.org/10.1128/AEM.02862-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. https://doi.org/10.1038/ismej.2010.58

    Article  PubMed  Google Scholar 

  87. Brewer TE, Handley KM, Carini P, Gilbert JA, Fierer N (2017) Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus. Nat Microbiol 2:16198. https://doi.org/10.1038/nmicrobiol.2016.198

    Article  CAS  Google Scholar 

  88. Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224. https://doi.org/10.1128/AEM.67.9.4215-4224.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Franzluebbers AJ, Haney RL, Hons FM, Zuberer DA (1996) Active fractions of organic matter in soils with different texture. Soil Biol Biochem 28:1367–1372. https://doi.org/10.1016/S0038-0717(96)00143-5

    Article  CAS  Google Scholar 

  90. Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensics 12:333–341. https://doi.org/10.1080/15275922.2011.622348

    Article  CAS  Google Scholar 

  91. Kandeler F, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306. https://doi.org/10.1007/BF00335958

    Article  CAS  Google Scholar 

  92. Valsecchi G, Gigliotti C, Farini A (1995) Microbial biomass, activity, and organic matter accumulation in soils contaminated with heavy metals. Biol Fertil Soils 20:253–259. https://doi.org/10.1007/BF00336086

    Article  CAS  Google Scholar 

  93. Chew I, Obbard JP, Stanforth RR (2001) Microbial cellulose decomposition in soils from a rifle range contaminated with heavy metals. Environ Pollut 111:367–375. https://doi.org/10.1016/S0269-7491(00)00094-4

    Article  CAS  PubMed  Google Scholar 

  94. McEnroe NA, Helmisaari H-S (2001) Decomposition of coniferous forest litter along a heavy metal pollution gradient, south-west Finland. Environ Pollut 113:11–18. https://doi.org/10.1016/S0269-7491(00)00163-9

    Article  CAS  PubMed  Google Scholar 

  95. Lucisine P, Lecerf A, Danger M, Felten V, Aran D, Auclerc A, Gross EM, Huot H, Morel JL, Muller S, Nahmani J, Maunoury-Danger F (2015) Litter chemistry prevails over litter consumers in mediating effects of past steel industry activities on leaf litter decomposition. Sci Total Environ 537:213–224. https://doi.org/10.1016/j.scitotenv.2015.07.112

    Article  CAS  PubMed  Google Scholar 

  96. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol Rev 67:321–358. https://doi.org/10.1111/j.1469-185X.1992.tb00728.x

    Article  Google Scholar 

  97. Johnson D, Leake JR, Lee JA, Campbell CD (1998) Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands. Environ Pollut 103:239–250. https://doi.org/10.1016/S0269-7491(98)00115-8

    Article  CAS  Google Scholar 

  98. Kuperman RG, Carreiro MM (1997) Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biol Biochem 29:179–190. https://doi.org/10.1016/S0038-0717(96)00297-0

    Article  CAS  Google Scholar 

  99. Moore A, Becking J (1963) Nitrogen fixation by Bacillus strains isolated from Nigerian soils. Nature 198:915–916. https://doi.org/10.1038/198915a0

    Article  CAS  Google Scholar 

  100. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. https://doi.org/10.1038/ismej.2011.159

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Arcelor Mittal, EPFL, GISFI, ONF, and LTO of Montiers (ANDRA/INRA, M.P. Turpault and S. Uroz) for giving us access to the different sampling sites. We would like to thank G. Kitzinger and D. Billet (LIEC, Nancy, France) as well as J. Marchand (PTEF, INRA Champenoux, France) for technical assistance and A. Meyer (LIEC, Metz, France) for statistical analysis support.

Funding

This study was supported by the Agence Nationale de la Recherche (RhizOrg project ANR-13-JSV7-000701), the French national program EC2CO (Ecobios project), and the OSU-OteLo (TraitMic project).

Author information

Authors and Affiliations

  1. Université de Lorraine, CNRS, LIEC, 54000, Nancy, France

    Florian Lemmel, Andrea Fanesi, Corinne Leyval & Aurélie Cébron

  2. Université de Lorraine, CNRS, LIEC, 57000, Metz, France

    Florence Maunoury-Danger

Authors
  1. Florian Lemmel
    View author publications

    Search author on:PubMed Google Scholar

  2. Florence Maunoury-Danger
    View author publications

    Search author on:PubMed Google Scholar

  3. Andrea Fanesi
    View author publications

    Search author on:PubMed Google Scholar

  4. Corinne Leyval
    View author publications

    Search author on:PubMed Google Scholar

  5. Aurélie Cébron
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Aurélie Cébron.

Electronic supplementary material

ESM 1

(XLSX 13 kb)

ESM 2

(XLSX 9 kb)

FIGURE S1

(PNG 2230 kb)

High Resolution Image (TIF 52987 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lemmel, F., Maunoury-Danger, F., Fanesi, A. et al. Soil Properties and Multi-Pollution Affect Taxonomic and Functional Bacterial Diversity in a Range of French Soils Displaying an Anthropisation Gradient. Microb Ecol 77, 993–1013 (2019). https://doi.org/10.1007/s00248-018-1297-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-018-1297-7

Keywords