Bacterial Activity, Community Structure, and Centimeter-Scale Spatial Heterogeneity in Contaminated Soil

In an anthropogenically disturbed soil (88% sand, 8% silt, 4% clay), 150-mg samples were studied to examine the fine-scale relationship of bacterial activity and community structure to heavy metal contaminants. The soils had been contaminated for over 40 years with aromatic solvents, Pb, and Cr. Samples from distances of <1, 5, 15, and 50 cm over a depth range of 40–90 cm underwent a sequential analysis to determine metabolic potential (from 14C glucose mineralization), bacterial community structure [using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE)], and total extractable Pb and Cr levels. Metabolic potential varied by as much as 10,000-fold in samples <1 cm apart; log–log plots of metal concentration and microbial metabolic potential showed no correlation with each other. Overall, metal concentrations ranged from 9 to 29,000 mg kg−1 for Pb and from 3 to 8500 mg kg−1 for Cr with small zones of high contamination present. All regions exhibited variable metal concentrations, with some soil samples having 30-fold differences in metal concentration in sites <1 cm apart. Geostatistical analysis revealed a strong spatial dependence for all three parameters tested (metabolic activity, Pb, and Cr levels) with a range up to 30 cm. Kriging maps showed that in zones of high metal, the corresponding metabolic activity was low suggesting that metals negatively impacted the microbial community. PCR-DGGE analysis revealed that diverse communities were present in the soils with a random distribution of phylotypes throughout the sampling zones. These results suggest the presence of spatially isolated microbial communities within the soil profile.

[1]  C. Chenu,et al.  Spatial variability of 2,4-dichlorophenoxyacetic acid (2,4-D) mineralisation potential at a millimetre scale in soil , 2003 .

[2]  T. Barkay,et al.  Molecular Evidence for the Evolution of Metal Homeostasis Genes by Lateral Gene Transfer in Bacteria from the Deep Terrestrial Subsurface , 2004, Applied and Environmental Microbiology.

[3]  A. Felske,et al.  Spatial Homogeneity of Abundant Bacterial 16S rRNA Molecules in Grassland Soils , 1998, Microbial Ecology.

[4]  L. Forney,et al.  Spatial Distribution of Rhodopseudomonas palustris Ecotypes on a Local Scale , 2003, Applied and Environmental Microbiology.

[5]  L. Ranjard,et al.  Shifts in Diversity and Microscale Distribution of the Adapted Bacterial Phenotypes due to Hg(II) Spiking in Soil , 2003, Microbial Ecology.

[6]  Hahn,et al.  Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. , 1999, FEMS microbiology ecology.

[7]  D. Wardle,et al.  Spatial soil ecology , 2002 .

[8]  A. Fliessbach,et al.  SOIL MICROBIAL BIOMASS AND MICROBIAL ACTIVITY IN SOILS TREATED WITH HEAVY METAL CONTAMINATED SEWAGE SLUDGE , 1994 .

[9]  P. Hobbs,et al.  Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil , 2000, Biology and Fertility of Soils.

[10]  R. Franklin,et al.  Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. , 2003, FEMS microbiology ecology.

[11]  M. Sliwinski,et al.  Spatial Heterogeneity of Crenarchaeal Assemblages within Mesophilic Soil Ecosystems as Revealed by PCR-Single-Stranded Conformation Polymorphism Profiling , 2004, Applied and Environmental Microbiology.

[12]  D. R. Nielsen,et al.  Spatial and Temporal Statistics - Sampling Field Soils and Their Vegetation , 2003 .

[13]  Jizhong Zhou,et al.  Microbial Diversity and Heterogeneity in Sandy Subsurface Soils , 2004, Applied and Environmental Microbiology.

[14]  H. Fritze,et al.  Phospholipid Fatty Acid Composition and Heavy Metal Tolerance of Soil Microbial Communities along Two Heavy Metal-Polluted Gradients in Coniferous Forests , 1996, Applied and environmental microbiology.

[15]  A. Konopka,et al.  Long-term effects of chromium and lead upon the activity of soil microbial communities , 2002 .

[16]  Grundmann,et al.  Geostatistical analysis of the distribution of NH(4)(+) and NO(2)(-)-oxidizing bacteria and serotypes at the millimeter scale along a soil transect. , 2000, FEMS microbiology ecology.

[17]  T. Parkin,et al.  Spatial Variability of Microbial Processes in Soil—A Review , 1993 .

[18]  Anthony V. Palumbo,et al.  Spatial and Resource Factors Influencing High Microbial Diversity in Soil , 2002, Applied and Environmental Microbiology.

[19]  R. Franklin,et al.  A geostatistical analysis of small-scale spatial variability in bacterial abundance and community structure in salt marsh creek bank sediments. , 2002, FEMS microbiology ecology.

[20]  J. Kelly,et al.  Changes in soil microbial communities over time resulting from one time application of zinc: a laboratory microcosm study , 1999 .

[21]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[22]  J. Tiedje,et al.  A Two-Species Test of the Hypothesis That Spatial Isolation Influences Microbial Diversity in Soil , 2002, Microbial Ecology.

[23]  L. Ranjard,et al.  Response of soil bacteria to Hg(II) in relation to soil characteristics and cell location , 1997 .

[24]  E. Bååth,et al.  Development of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels , 1996, Applied and environmental microbiology.

[25]  D. Mummey,et al.  Analysis of Soil Whole- and Inner-Microaggregate Bacterial Communities , 2004, Microbial Ecology.

[26]  S. Sørensen,et al.  The Effect of Longterm Exposure to Mercury on the Bacterial Community in Marine Sediment , 1998, Current Microbiology.

[27]  J. Crawford,et al.  In Situ Spatial Patterns of Soil Bacterial Populations, Mapped at Multiple Scales, in an Arable Soil , 2002, Microbial Ecology.

[28]  G. Grundmann,et al.  Spatial Modeling of Nitrifier Microhabitats in Soil , 2001 .

[29]  G. Zerbi,et al.  Bioavailability and effects of heavy metals on soil microbial biomass survival during laboratory incubation , 1995, Biology and Fertility of Soils.

[30]  L. Øvreås,et al.  Prokaryotic Diversity--Magnitude, Dynamics, and Controlling Factors , 2002, Science.

[31]  David J. Mulla,et al.  Geostatistical Tools for Modeling and Interpreting Ecological Spatial Dependence , 1992 .

[32]  L. Ranjard,et al.  Sequencing Bands of Ribosomal Intergenic Spacer Analysis Fingerprints for Characterization and Microscale Distribution of Soil Bacterium Populations Responding to Mercury Spiking , 2000, Applied and Environmental Microbiology.

[33]  B. Griffiths,et al.  Community DNA hybridisation and %G+C profiles of microbial communities from heavy metal polluted soils , 1997 .

[34]  E. Bååth,et al.  Phospholipid Fatty Acid Composition, Biomass, and Activity of Microbial Communities from Two Soil Types Experimentally Exposed to Different Heavy Metals , 1993, Applied and environmental microbiology.

[35]  J. D. Elsas,et al.  Structural diversity of microbial communities in arable soils of a heavily industrialised area determined by PCR-DGGE fingerprinting and FAME profiling , 2001 .

[36]  Jianming Xu,et al.  Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils , 2003 .

[37]  E. Bååth,et al.  Multiple Heavy Metal Tolerance of Soil Bacterial Communities and Its Measurement by a Thymidine Incorporation Technique , 1994, Applied and environmental microbiology.

[38]  P. Normand,et al.  Microscale Diversity of the GenusNitrobacter in Soil on the Basis of Analysis of Genes Encoding rRNA , 2000, Applied and Environmental Microbiology.

[39]  C. D. Clegg,et al.  Spatial structure in soil chemical and microbiological properties in an upland grassland. , 2004, FEMS microbiology ecology.

[40]  W. Holben,et al.  Differences in Hyporheic-Zone Microbial Community Structure along a Heavy-Metal Contamination Gradient , 2003, Applied and Environmental Microbiology.

[41]  L. Ranjard,et al.  Quantitative and qualitative microscale distribution of bacteria in soil. , 2001, Research in microbiology.

[42]  M. Meadows.  The Unified Theory of Biodiversity and Biogeography BY STEPHEN P. HUBBELL xiv + 375 pp., 21.5 × 14 × 2.2 cm, ISBN 0 691 02128 7 paperback, US$ 29.95/GB£ 19.95, Princeton, NJ, USA/Woodstock, UK: Princeton University Press, 2001 , 2002, Environmental Conservation.

[43]  E. Bååth,et al.  Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals , 1996 .

[44]  Linet,et al.  A soil microscale study to reveal the heterogeneity of Hg(II) impact on indigenous bacteria by quantification of adapted phenotypes and analysis of community DNA fingerprints. , 2000, FEMS microbiology ecology.

[45]  M. Rillig,et al.  Determining Rates of Change and Evaluating Group-Level Resiliency Differences in Hyporheic Microbial Communities in Response to Fluvial Heavy-Metal Deposition , 2004, Applied and Environmental Microbiology.

[46]  T. Kairesalo,et al.  Microbial community structure and activity in arsenic-, chromium- and copper-contaminated soils. , 2004, FEMS microbiology ecology.

[47]  J. Scullion,et al.  Effect of soil on microbial responses to metal contamination. , 2000, Environmental pollution.

[48]  E. Kandeler,et al.  Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment , 2001, Applied and Environmental Microbiology.

[49]  S. Morris.  Spatial distribution of fungal and bacterial biomass in southern Ohio hardwood forest soils: fine scale variability and microscale patterns , 1999 .

[50]  J. Amador,et al.  Spatial and temporal patterns of soil biological activity in a forest and an old field , 1998 .

[51]  E. Bååth,et al.  Response of soil bacterial communities pre-exposed to different metals and reinoculated in an unpolluted soil , 2001 .

[52]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[53]  R. Sandaa,et al.  Influence of long-term heavy-metal contamination on microbial communities in soil , 2001 .

[54]  E. Bååth,et al.  Spatial variation and patterns of soil microbial community structure in a mixed spruce-birch stand. , 2000 .