Joynt J.*§, Konopka A.π, Nakatsu C.*
*Department of Agronomy, π Department of Biology, Purdue University, West Lafayette, Indiana, USA, 47907
Many scientific investigations have studied the effects of heavy metals and organic contaminants on microbial biomass and activities in soil. It remains unclear however, whether organic or metal contamination limit the bioremediation potential at a mixed waste site. We investigated the potentially selective factor limiting remediation by comparing the diversity of microbial populations present along a 21.6 m transect at a mixed waste site contaminated with lead, chromium and various organic compounds
Hazardous waste sites often contain both heavy
metal and organic contaminants in the soil.
Many reports have shown an acute effect of heavy metal stress is
decreased microbial biomass (Kandeler et
al., 1996; Knight et al., 1997),
and a chronic effect is decreased microbial metabolic activity (Bååth et al., 1991; Doelman and Haanstra,
1979; Insam et al., 1996). However,
these studies have also suggested that over time there is a gradual change in
the microbial composition towards a more metal tolerant community. If a tolerant community is able to develop
in soils, than the apparent decrease in biomass and activity that has been
reported may not be due to the toxicity of the heavy metal itself, but rather
due to an indirect effect of metals such as the lack of available organic
carbon in the soil. Bioremediation at a
mixed waste contaminated site may therefore, not be limited by the heavy metals
but by the toxicity and availability of the organics that are present.
By looking at the microbial community structure at a
long-term mixed waste site, the diversity of the community can be compared
between high and low metal and organic contaminant concentrations. If bacteria become tolerant and are able to
adapt to metal stress, then a relatively diverse community would be expected
irrespective of the metal concentrations present because the metals are not
inhibiting the bacteria. However, if the community cannot adapt to heavy metals
than fewer members would be expected to survive and diversity would be lowered
as metal concentrations increased.
The
objective of this study was to investigate how microbial community structure is
altered across high to low metal and organic gradients at a mixed waste
contaminated site. Bacterial DNA was extracted directly from soil samples, and
a fragment of the 16S rDNA gene was PCR amplified and separated using DGGE to
provide a picture of the community complexity and structure.
The sampling site was located at an Indiana
Department of Transportation (INDOT) property in Seymour, Indiana. Waste road
paint containing lead and chromium, and waste cleaning solvents containing
toluene, xylenes, ethylbenzene, methylene chloride and trichloroethylene were
dumped at the site and covered with backfill material since the late 1960's. In July, 1999 soil was sampled along a 21.6
m long and 0.5 m wide trench at the site. A total of twenty four samples were
collected along the transect taken at 0.9 m intervals alternating along the
north/south sides of the trench at a
0.6 to 0.9 m depth.
Soil was sent to Brookside Laboratories Inc. in New
Knoxville, Ohio for chemical and physical analysis. The following parameters were measured: pH, total organic carbon,
total lead, total chromium, nitrogen, phosphorous, potassium, volatile organic
carbon, texture, and cation exchange capacity.
Soil DNA was extracted in triplicate using the
FastDNA Spin Kitâ (Bio101) soil DNA
extraction kit following manufacturers instructions. DNA amplification was
carried out for subsequent use in DGGE using universal bacterial primers that
flank the V3 region of the 16S rDNA gene.
The primers (synthesized by Integrated DNA Technologies Inc.) are: 5’ AC
TCC TAC GGG AGG CAG CAG 3’ corresponding to position 338-358 in Escherichia coli, with a GC clamp
(5’-CGC CCG CCG CGC GCG GCG GGC GGG GCG GGG GCA CGG GGG G-3’) attached to the
5’ end, and reverse primer 5’-ATT ACC GCG GCT GCT GG-3’ corresponding to
position 534-518 in E. coli (Konopka et al., 1999). The GC clamp is present in order to stabilize the DNA in the DGGE
gel.
Denaturing gradient gel electrophoresis was carried
out as described previously (Konopka et
al., 1999). Briefly, PCR products
were resolved on an 8% (wt/vol) polyacrylamide gel (37.5:1
acrylamide:bisacrylamide) in 0.5X TAE (20 mM Tris-HCl, 10 mM acetate, 0.5 mM
EDTA) plus denaturant (100% denaturant contains 7M urea, 40% formamide in 0.5X
TAE). Electrophoresis was performed on a D-Gene apparatus (BioRad) at a
constant voltage of 20V for 15 minutes, followed by 200V for 4.5 hours. All gels were initially run using a 30-55%
denaturant gradient. Additionally, 30-70% denaturant gradients were used to
show bands with high G+C contents that migrated off the 30-55% gels.
Figure 1 shows the lead and chromium concentrations
across the site as well as total organic carbon for the north side of the
transect. Lead (Pb) and chromium (Cr)
concentrations in the soil ranged from 4 ppm to 17 000 ppm and 4 ppm to 3200
ppm respectively, and volatile organic concentrations ranged from 23 000 ppm to
<1 ppm in soil. Soil was mainly fill material, consisting largely of sand
(62-88.6%) with some pockets of high clay (37.6%). Total soil concentrations of
Pb and Cr were higher in samples that also contained high organic contaminants,
and had generally lower clay content.
Bands in the DGGE profile correspond to 16S rDNA
fragments that differ in their nucleotide sequences, and as a result migrate to
different positions in the gel. DGGE analysis of soils along the transect is
shown in Figure 2. Comparison of the
bacterial communities from each of the samples shows distinctly different profiles
from left to right across the gel. Samples
HN1, HN2 and HN3 appear to have similar banding profiles, whereas samples HN6
to HN12 also have a similar profile. These samples correspond to samples with
high and low metals respectively.
Sample HN4 and HN5 have bands common to both sets of communities and
appear to be transition samples.
Several populations with high G+C contents were found only in samples
HN1 to HN3, which have high volatile organic concentrations. Not all of these populations can be seen in
Figure 2, but are discernable when the denaturant is extended to 70% (data not
shown). Two bands were present in all samples irrespective of metal or organic
concentrations. There were more unique
bands however, than common bands across the site.
In this study the primary interest was investigating
the bacterial community structure and diversity at a metal and organic
contaminated site using DGGE. The DGGE
profile shown in Figure 3 demonstrates that the community across the site has several
different populations of bacteria present in both high and low Pb and Cr soil
concentrations as indicated by the number of bands present in each sample. This supports the inference that a bacterial
community is able to adapt to a heavy metal environment. The separation of the profile patterns into
two distinct groups (HN1to HN3 and HN6 to HN12) coincides with the presence of
high levels of organic contamination in one set (HN1 to HN3) and the absence of
organic contamination in the other (HN6 to HN12). Both sets of profiles have high levels of Pb and Cr. However, in the profiles for HN6 to 12,
sample HN10 has a Pb concentration of 351 ppm, and sample HN11 has a Pb
concentration of 3.73 ppm, yet the profiles remain consistent irrespective of
the metal concentration. These results suggest the organics rather than metals
at the site may predominantly influence the community composition in the
present study. Recently, Konopka et al., 1999 investigated microbial
diversity by DGGE at a lead contaminated site, and found that lead soils in
that study were more comparable to an agricultural soil with a smear of bands,
than the organic contaminated soil in which the diversity was severely
reduced. The soils in the present study
showed a diverse community, although they did not produce a smear of bands as
reported in Konopka et al., 1999,
which may be attributable to the organic contaminant influence. However, if the
community composition was solely influenced by the organics, than soils with
low organic contamination should have a greater diversity than soils with high
organic contamination. This was not the case.
Two reasons may explain this.
First, soil chemical data at the site show trace levels of organics
contaminants present in the HN6-HN12 samples which indicates organics were
present in these locations at some point.
These samples may therefore have reduced diversity as a result of these
previous contaminants. Second, soil
properties such as texture and CEC differ between the two profile sets, which
may be influencing the community structure.
In conclusion, it can be seen that lead chromium and
organic contamination are influencing the microbial community structure present
at the site, although the extent of their influence is not known. More work must be done to determine the
dominant selective pressure on the community.
Future work entails nucleotide sequence determination of the dominant
bands present in distinct sample profiles, and monitoring of community shifts
with metal and organic and both added to the soil.
Acknowledgements: Funding was provided by the
DOE-NABIR Program, grant #DE-FG02-98ER62681
REFERENCES:
Bååth E, Arnebrandt K, Nordgren A (1991) Bull
Environ Contam Tox. 47:278-282.
Bååth E, Diaz-Ravina M, Frostegård Å, Campbell C
(1998) Appl Environ Micrbiol. 64:1:238-245.
Doelman P, Haanstra L (1979) Soil Biol Biochem.
11:475-479.
Insam H, Hutchinson T, Reber H (1996) Soil Biol
Biochem. 28:4/5:691-694.
Kandeler E, Kampichler C, Horak O (1996) Biol Fert
Soils. 23:299-306.
Knight B, McGrath S, Chaudri A (1997) Appl Environ
Microbiol. 63:39-43.
Konopka A, Zakharova T, Bischoff M, Oliver L,
Nakatsu C, Turco R (1999) Appl Environ Microbiol. 65:5:2256-2259.
Vallaeys T, Topp E, Muyzer G, Macheret V, Laguerre G, Rigaud A, Soulas G (1997) FEMS Microbiol Ecol. 24:279-285.
Figure 1:
Total lead, chromium and total organic carbon concentrations along the north
side of the transect.

Figure 2: Samples HN1 to HN12 across the
site transect. Samples were
extracted from soil and a section of the V3 region of 16S rDNA gene was PCR amplified, then run on a 30-55% DGGE gel. Bands at different positions in the gel
represent different bacterial populations. Samples in figure start with a
marker lane, followed by samples HN1 to HN12 consecutively.
