Skip to main content
Log in

The impact of increasing heavy metal stress on the diversity and structure of the bacterial and actinobacterial communities of metallophytic grassland soil

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

A study was undertaken to investigate the bacterial community found in metallophytic grassland soil contaminated with Zn and Pb. We hypothesised that such communities would be tolerant of additional heavy metal stress due to phylogenetic and functional adaptation. In microcosm experiments, lasting 51 days, denaturing gradient gel electrophoresis (DGGE) analyses was used to compare the total bacterial and actinobacterial communities in non-amended soils and those to which additional Pb and Zn concentrations were added. There was a decrease in total bacterial diversity with each addition of Pb and Zn; in contrast, the actinobacterial community diversity remained unaffected. The community structures were analysed using multivariate analyses of the DGGE profiles. Total bacterial community profiles showed two distinct groups sharing less than 80% similarity, irrespective of Pb and Zn addition. The first contained profiles sampled during the first 7 days of the experiment; the second contained those sampled from day 10 onwards. Actinobacterial profiles from those that were non-amended showed a similar distribution to those of the total bacterial community. However, in soil amended with fivefold additional Pb and Zn, all the profiles shared more than 80% similarity. Raup and Crick analyses suggested that total bacterial soil communities were subject deterministic selection becoming significantly similar as the experiment progressed, but this was inhibited by the highest concentration of additional Pb and Zn. Actinobacterial communities showed a similar response but were less affected by elevated Pb and Zn concentrations. These data indicate that the diversity of the actinobacterial community was not negatively affected by additional heavy metal stress in contrast to total bacterial community diversity.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Explore related subjects

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

References

  • Åkerblom S, Bååth E, Bringmark L, Bringmark E (2008) Experimentally induced effects of heavy metal on microbial activity and community structure of forest mor layers. Biol Fertil Soils 44:79–91 doi:10.1007/s00374-007-0181-2

    Article  Google Scholar 

  • Almås AR, Bakken LR, Mulder J (2004) Changes in tolerance of soil microbial communities in Zn and Cd contaminated soils. Soil Biol Biochem 36:805–813 doi:10.1016/j.soilbio.2004.01.010

    Article  Google Scholar 

  • Baxter J, Cummings SP (2006) The impact of bioaugmentation on metal cyanide degradation and soil bacteria community structure. Biodegradation 17:207–217 doi:10.1007/s10532-005-4219-6

    Article  PubMed  CAS  Google Scholar 

  • Baxter J, Garton NJ, Cummings SP (2006) The impact of acrylonitrile and bioaugmentation on the biodegradation activity and bacterial community structure of a topsoil. Folia Microbiol (Praha) 51:591–598

    Article  CAS  Google Scholar 

  • Brodie E, Edwards S, Clipson N (2003) Soil fungal community structure in a temperate upland grassland soil. FEMS Microbiol Ecol 45:105–114 doi:10.1016/S0168-6496(03)00126-0

    Article  CAS  Google Scholar 

  • DeGrood SH, Claassen VP, Scow KM (2005) Microbial community composition on native and drastically disturbed serpentine soils. Soil Biol Biochem 37:1427–1435 doi:10.1016/j.soilbio.2004.12.013

    Article  CAS  Google Scholar 

  • Duarte GF, Rosado AS, Seldin L, de Araujo W, van Elsas JD (2001) Analysis of bacterial community structure in sulphurous-oil-containing soils and detection of species carrying dibenzothiophene desulfurization (dsz) genes. Appl Environ Microbiol 67:1052–1062 doi:10.1128/AEM.67.3.1052-1062.2001

    Article  PubMed  CAS  Google Scholar 

  • Feris K, Ramsey P, Frazar C, Moore JN, Gannon JE, Holbert WE (2003) Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Appl Environ Microbiol 69:5563–5573 doi:10.1128/AEM.69.9.5563-5573.2003

    Article  PubMed  CAS  Google Scholar 

  • Frey B, Stemmer M, Widmer F, Luster JC, Sperisen C (2006) Microbial activity and community structure of a soil after heavy metal contamination in a model forest ecosystem. Soil Biol Biochem 38:1745–1756 doi:10.1016/j.soilbio.2005.11.032

    Article  CAS  Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390 doi:10.1126/science.1112665

    Article  PubMed  CAS  Google Scholar 

  • 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 doi:10.1016/S0038-0717(97)00270-8

    Article  CAS  Google Scholar 

  • Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907 doi:10.1046/j.1462-2920.2003.00484.x

    Article  PubMed  CAS  Google Scholar 

  • Griffiths BS, Bonkowski M, Roy J, Ritz K (2001) Functional stability, substrate utilisation and biological indicators of soils following environmental impacts. Appl Soil Ecol 16:49–61 doi:10.1016/S0929-1393(00)00081-0

    Article  Google Scholar 

  • Griffiths RI, Whitely AS, O’Donnell AG, Bailey MJ (2003) Influence of depth and sampling time on bacterial community structure in an upland grassland soil. FEMS Microbiol Ecol 43:35–43 doi:10.1111/j.1574-6941.2003.tb01043.x

    Article  CAS  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241

    PubMed  CAS  Google Scholar 

  • Hinojosa MB, Carreira JA, Garcia-Ruiz R, Dick RP (2005) Microbial response to heavy metal-polluted soils: Community analysis from phospholipid-linked fatty acids and ester-linked fatty acids extracts. J Environ Qual 34:1789–1800 doi:10.2134/jeq2004.0470

    Article  PubMed  CAS  Google Scholar 

  • Holmes AJ, Bowyer J, Holley MP, O’Donoghue M, Montgomery M, Gillings MR (2000) Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Microbiol Ecol 33:111–120 doi:10.1111/j.1574-6941.2000.tb00733.x

    Article  PubMed  CAS  Google Scholar 

  • Intawongse M, Dean JR (2008) Use of the physiologically-based extraction test to assess the oral bioaccessibility of metals in vegetable plants grown in contaminated soil. Environ Poll 152:60–72

    Article  CAS  Google Scholar 

  • Joynt J, Bischoff M, Turco R, Konopka A, Nakatsu CH (2006) Microbial community analysis of soils contaminated with lead, chromium and petroleum hydrocarbons. Microb Ecol 51:209–219 doi:10.3354/ame01202

    Article  PubMed  CAS  Google Scholar 

  • Kelly JJ, Häggblom MM, 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 doi:10.1016/S0038-0717(99)00059-0

    Article  CAS  Google Scholar 

  • Kuan HL, Fenwick C, Glover LA, Griffiths BS, Ritz K (2006) Functional resilience of microbial communities from perturbed upland grassland soils to further persistent or transient stresses. Soil Biol Biochem 38:2300–2306 doi:10.1016/j.soilbio.2006.02.013

    Article  CAS  Google Scholar 

  • Li ZJ, Xu JM, Tang CX, Wu JJ, Muhammad A, Wang HZ (2006) Application of 16S rDNA-PCR amplification and DGGE fingerprinting for detection of shift in microbial community diversity in Cu-, Zn-, and Cd-contaminated paddy soils. Chemosph 62:1374–1380 doi:10.1016/j.chemosphere.2005.07.050

    Article  CAS  Google Scholar 

  • Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P et al (2006) Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biol Biochem 38:1430–1437 doi:10.1016/j.soilbio.2005.10.020

    Article  CAS  Google Scholar 

  • Mummey DL, Stahl PD (2004) Analysis of soil whole- and inner-microaggregate bacterial communities. Microb Ecol 48:41–50 doi:10.1007/s00248-003-1000-4

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Odum EP (1981) The effects of stress on the trajectory of ecological succession. In: Barrett GW, Rosenburg R (eds) Stress effects on natural ecosystems. Wiley, London, pp 43–47

    Google Scholar 

  • Ogino A, Koshikawa H, Nakahara T, Uchiyama H (2001) Succession of microbial communities during a biostimulation process as evaluated by DGGE and clone library analyses. J Appl Microbiol 91:625–635 doi:10.1046/j.1365-2672.2001.01424.x

    Article  PubMed  CAS  Google Scholar 

  • Quevauviller P (1998) Operationally defined extraction procedures for soil and sediment analysis—II. Certified reference materials. Trends Analyt Chem 17:632–642 doi:10.1016/S0165-9936(98)00078-8

    Article  CAS  Google Scholar 

  • Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160 doi:10.1111/j.1574-6941.2007.00375.x

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen DL, Sørensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36:1–9 doi:10.1111/j.1574-6941.2001.tb00820.x

    Article  PubMed  CAS  Google Scholar 

  • Renella G, Chaudri AM, Brookes PC (2002) Fresh additions of heavy metals do not model long-term effects on microbial biomass and activity. Soil Biol Biochem 34:121–124 doi:10.1016/S0038-0717(01)00150-X

    Article  CAS  Google Scholar 

  • Renella G, Chaudri AM, Falloon CM, Landi L, Nannipieri P, Brookes PC (2007) Effects of Cd, Zn, or both on soil microbial biomass and activity in a clay loam soil. Biol Fertil Soils 43:751–758 doi:10.1007/s00374-006-0159-5

    Article  CAS  Google Scholar 

  • Rowan AK, Snape JR, Fearnside D, Barer MR, Curtis TP, Head IM (2003) Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. FEMS Microbiol Ecol 43:195–206 doi:10.1111/j.1574-6941.2003.tb01059.x

    Article  CAS  Google Scholar 

  • Sandaa RA, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251 doi:10.1111/j.1574-6941.1999.tb00652.x

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Haferburg G, Sineriz M, Merten D, Buchel G, Kothe E (2005) Heavy metal resistance mechanisms in Actinobacteria for survival in AMD contaminated soils. Chem Erde-Geochem 65:131–144 doi:10.1016/j.chemer.2005.06.006

    Article  CAS  Google Scholar 

  • Sigler WV, Turco RF (2002) The impact of chlorothalonil application on soil bacterial and fungal populations as assessed by denaturing gradient gel electrophoresis. Appl Soil Ecol 21:107–118 doi:10.1016/S0929-1393(02)00088-4

    Article  Google Scholar 

  • Tobor-Kaplon M, Bloem AJ, Romkens P, de Ruiter PC (2005) Functional stability of microbial communities in contaminated soils. Oikos 111:119–129 doi:10.1111/j.0030-1299.2005.13512.x

    Article  CAS  Google Scholar 

  • Wu SC, Luo YM, Cheung KC, Wong MH (2006) Influence of bacteria on Pb and Zn speciation, mobility and bioavailability in soil: a laboratory study. Environ Pollut 144:765–773 doi:10.1016/j.envpol.2006.02.022

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank BIONET, the Sustainable Cities Institute, Northumbria University and the Centre for Excellence in Life Sciences, Newcastle-upon-Tyne for financial support for this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen P. Cummings.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bamborough, L., Cummings, S.P. The impact of increasing heavy metal stress on the diversity and structure of the bacterial and actinobacterial communities of metallophytic grassland soil. Biol Fertil Soils 45, 273–280 (2009). https://doi.org/10.1007/s00374-008-0323-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-008-0323-1

Keyword