Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities

Abstract

Soil microorganisms drive critical functions in plant-soil systems. As such, various microbial properties have been proposed as indicators of soil functioning, making them potentially useful in evaluating the recovery of polluted soils via phytoremediation strategies. To evaluate microbial responses to metal phytoextraction using hyperaccumulators, a microcosm experiment was carried out to study the impacts of Zn and/or Cd pollution and Thlaspi caerulescens growth on key soil microbial properties: basal respiration; substrate-induced respiration (SIR); bacterial community structure as assessed by PCR-denaturing gradient gel electrophoresis (DGGE); community sizes of total bacteria, ammonia-oxidizing bacteria, and chitin-degrading bacteria as assessed by quantitative PCR (Q-PCR); and functional gene distributions as determined by functional gene arrays (GeoChip). T. caerulescens proved to be suitable for Zn and Cd phytoextraction: shoots accumulated up to 8,211 and 1,763 mg kg(-1) (dry weight [DW]) of Zn and Cd, respectively. In general, Zn pollution led to decreased levels of basal respiration and ammonia-oxidizing bacteria, while T. caerulescens growth increased the values of substrate-induced respiration (SIR) and total bacteria. In soils polluted with 1,000 mg Zn kg(-1) and 250 mg Cd kg(-1) (DW), soil bacterial community profiles and the distribution of microbial functional genes were most affected by the presence of metals. Metal-polluted and planted soils had the highest percentage of unique genes detected via the GeoChip (35%). It was possible to track microbial responses to planting with T. caerulescens and to gain insight into the effects of metal pollution on soilborne microbial communities.

FIG. 1.

Shoot and root metal concentrations at the end of the experiment in T. caerulescens plants subjected to different Zn (first value) and Cd (second value) soil concentrations (mg kg⁻¹ [DW]). Bars labeled with different letters are significantly different (P < 0.05) according to the Tukey-Kramer test (statistics are shown only when, according to two-way ANOVA, a significant interaction was found between soil Zn and Cd concentrations). Mean values (n = 4) and standard errors are shown.

FIG. 2.

Principal-component analysis of soil physicochemical and microbial properties in planted (P) and unplanted (UP) soils polluted with different Zn (first value) and Cd (second value) concentrations at the end of the experiment. Axis 1 and axis 2 account for 29 and 17% of the variance, respectively. Chit, group A bacterial chitinase gene abundance; Bac, total bacterial-gene abundance; BR, basal respiration; P, extractable phosphorus content; Amo, ammonia monooxygenase gene abundance; Ms, Medicago sativa growth; NO₃, nitrate content; N, total N content; K, extractable potassium content.

FIG. 3.

Number of gene variants detected in the GeoChip functional gene array in planted (P) and unplanted (UP) soils polluted with different Zn (first value) and Cd (second value) concentrations at the end of the experiment. Only those gene variants that were well represented (with a minimum of 5 gene variants) and that showed significant differences (P < 0.05) among treatments, according to ANOVA, are presented.