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In the present work, the relationships between plant consortia, consisting of 1–4 metallicolous pseudometallophytes with different metal-tolerance strategies (Thlaspi caerulescens: hyperaccumulator; Jasione montana: accumulator; Rumex acetosa: indicator; Festuca rubra: excluder), and their rhizosphere microbial communities were studied in a mine soil polluted with high levels of Cd, Pb and Zn. Physiological response and phytoremediation potential of the studied pseudometallophytes were also investigated. The studied metallicolous populations are tolerant to metal pollution and offer potential for the development of phytoextraction and phytostabilization technologies. T. caerulescens appears very tolerant to metal stress and most suitable for metal phytoextraction; the other three species enhance soil functionality. Soil microbial properties had a stronger effect on plant biomass rather than the other way around (35.2% versus 14.9%). An ecological understanding of how contaminants, ecosystem functions and biological communities interact in the long-term is needed for proper management of these fragile metalliferous ecosystems.
1. Materials and methods
1.1. Field characterization The study was carried out in a spontaneously revegetated abandoned mine, heavily polluted with Cd, Pb and Zn, located in Lanestosa, Biscay, northern Spain. Within the mine, an experimental area of approximately 300 m2 was chosen for this study based on the richness of plant species observed in that area. Initially, a systematic soil sampling (upper 0–10 cm) was carried out by means of dividing the experimental area into four quadrants and then, within each of them, 10 soil cores (diameter: 2.5 cm) were collected at random and mixed together to form a composite sample (4 composite samples: one per quadrant). Immediately after collection, soil samples were sieved to <2 mm, airdried t 30 _C, and subjected to physicochemical characterization according to standard methods. Total concentrations of heavy metals in soil samples were determined using flame atomic absorption spectrometry (AAS, Varian) following digestion with a mixture of HNO3/HClO4.
For the analysis of soil physicochemical parameters. Shoots from each plant species were harvested. Lipophilic antioxidants (carotenoids and tocopherols) and photosynthetic pigments [chlorophylls and b (Chl). Subsamples (0.3. R. R ¼ R. g. For each of the following combinations. J.4 g) of dried shoot tissue were digested with a mixture of HNO3/HClO4 (Zhao et al. rubra). Leaf samples were collected and kept in the dark for 12 h at room temperature (20– 22 C) to reduce the effects of diurnal variations in antioxidants and pigments.and a-tocopherols (Toc)] were extracted and measured by reversephase HPLC. antheraxanthin (A). organic C concentration was determined colorimetrically at 445 nm. J. montana. TR. metal indicator). Total concentrations of heavy metals in soil were determined as above. 1–5 consortia were collected: T.4 ml of substrate. taking into account that sampling points had to be at least 1 m apart from each other. 2 . was mixed with 0. (Brassicaceae. and F. Thirty-three (33) points were selected to study native consortia consisting of 1–4 of these plant species. metal excluder). violaxanthin (V). F ¼ F. RF.02 g FW leaf was collected. Soil microbial and physicochemical parameters. TJR. Fresh weights (FW) were recorded and. Then. carotenoids (Carot). & C. Blocks containing both aboveground plant consortia and belowground rhizosphere soil were carefully sampled and taken to the laboratory. caerulescens. 1994) and. For the analysis of microbial parameters. It has been reported that measurements of functional diversity are likely to provide information more relevant to the functioning of the soil ecosystem than species diversity. TJF. shoots were oven-dried at 70 C for 48 h to calculate dry weights (DW). acetosa L. Cd. finally. JR. For the estimation of metal bioavailability. frozen in liquid nitrogen and stored at 80 C until analysis. montana L. washed thoroughly with deionized water and gently dried with paper towels.38 was assumed). (2002): a moist sample. TF. Microbial biomass C was calculated as the difference between C concentration of the fumigated and unfumigated extracts (an extractability of 0.2. four metallicolous species with different metal-tolerance strategies were chosen: T. (Polygonaceae. The mixture was incubated at 25 C for 3 h and the reaction stopped with 8 ml of methanol. (Poaceae. (Campanulaceae. 2. as abovementioned. Rhizosphere soil was carefully sampled by collecting all the soil adhering to roots after gentle shaking.. J ¼ J. Were added to 2 ml of extract and incubated at 150 C for 60 min. R. F.4 ml of buffer and 0. Soil pH was measured following standard methods. soils were air-dried at 30 C for 48 h. caerulescens J. TRF.Water-soluble organic carbon (WSOC) was extracted by shaking soil (horizontal shaker at 175 rpm) with distilled water (1:5 w/v) for 1 h and then measured as described above for microbial biomass C. Presl. soils were sieved to < 2mm and stored fresh at 4 C until analysis. dehydrogenase activity was determined according to Taylor et al. sieved to < 2 mm and stored at 4 C until analysis. Pb and Zn were determined using AAS. Plant parameters For this study. subsequently. Regarding soil enzyme activities. acetosa. approximately 0. metal accumulator). JRF and TJRF (T ¼ T. zeaxanthin (Z). Finally.2. corresponding to 1 g DW soil. rubra L. metal hyperaccumulator).
galena. Pb and Zn concentrations usually found in nonpolluted soils of the Basque Country. (2000) and then analyzed by AAS. Finally.27%) and very low values of N. and quartz. In our study. 2. we employed variation partitioning procedures. probably due to the low number of species present in the 3 . In the studied soil. A considerable portion of the metals was found in the non CaCl2-extractable fraction. we measured how much of the variation in values of soil microbial properties could be attributed to the individual or joint effect of both soil physicochemical parameters and plant biomass data (influence of belowground physicochemical properties on belowground microbial properties as well as influence of aboveground plant biomass on belowground microbial properties).77 . calcite. plant composition. It is well-known that Pb usually appears in soil non-bioavailable fractions. Previous studies have shown that the composition of belowground soil microbial communities may depend on aboveground plant species composition.4.CaCl2-extractable (0. as heavy metals might affect biological mineralization cycles. Besides. but Cd and Zn frequently appear in more bioavailable fractions. Discussion The studied mine field was severely polluted with Cd. plant richness and abundance may also affect soil microbial communities. nonetheless. To explore the individual and shared effects of soil physicochemical and microbial properties to the revealed patterns in plant biomass data. Statistical analysis To study the influence of soil characteristics on biomass of each plant species (influence of belowground microbial and physicochemical properties on aboveground plant biomass). we quantified how much of the variability in the values of soil physicochemical properties could be attributed to the individual or joint effect of both soil microbial properties and plant biomass data (influence of belowground microbial properties on belowground physicochemical properties aswell as influence of aboveground plant biomass on belowground physicochemical properties). a considerable amount of Zn seems to be present in a hypogene assemblage consisting of sphalerite.0. surpassing by far. non-extractable metal fractions have been recently reported as plantavailable due to replenishment of more labile metal. Pb and Zn. as expected. On the other hand. the maximum Cd.01 M) metal fractions in soil were determined as described by Houba et al. dolomite. plant richness did not have any effect on soil microbial properties (or physicochemical properties). multivariate relationships between physicochemical and microbial soil properties and plant biomass were explored. mainly through the development of rhizobacteria induced by the release of specific sugars and amino acids into the rhizosphere. the high metal concentrations found in the mine soil could well be responsible for its relatively high values of OM content (4. pyrite. P and K content. 2. a form usually considered unavailable for plants. In the sameway.
99. Heavy metal contamination provides a strong pressure that selects for the recruitment of multiple resistance phenotypes that encode resistance to the predominant metals in the site. immobile forms using metal excluder plants). (2006). soil microbial parameters had a stronger effect on plant biomass rather than the other way round (35. The redundancy analysis suggested that the biomass of each plant species influenced in a different way soil microbial parameters. due to the extremely high levels of metals present in the experimental area. thus making it a good candidate for phytostabilization of soils heavily polluted with metals such as those from mining areas (phytostabilization is a phytoremediation method that converts soil metal pollutants into inert. None of the studied plants showed severe phytotoxic symptoms according to the values of photosynthetic pigments and antioxidant 4 . respiration) and soil pH was well characterized by linear or quadratic regression models with R values ranging from 0. the labile fraction of soil OM included inWSOC provides nutrients for the soil microbial community. a relationship between soil biological activities (alkaline phosphatase activity. reduced permeability. their environment and physicochemical conditions) that influence the balance of metal species between soluble and insoluble phases. Also. rubra.2% versus 14. positive effects of microbes on plant productivity are most common in nutrient poor ecosystems where they enhance the supply of growth limiting nutrients such as N and P to plants. R. Microorganisms can affect metal speciation thanks to their ability to effect and/or mediate mobilization or immobilization processes (the balance between mobilization and immobilization varies depending on the organisms involved.plant consortia (1–4) as well as the limited number of replicates per plant consortia found in the experimental area. Certainly. Microorganisms are intimately involved in metal biogeochemistry with a variety of processes determining mobility and bioavailability (Gadd. both soil pH and WSOC had a negative and positive influence on soil microbial properties. in bacteria. The influence of soil physicochemical properties (including metal concentrations) on soil microbial properties and vice versa is worth-mentioning.57 to 0. and extracellular detoxification. despite the elevated levels of soil metal pollution present in the mine soil.Unlike Cd and Pb. a metal excluder. respectively. it has been reported to be highly toxic at elevated concentrations. montana and R. Under such limiting conditions. 2004). up to 90% of the P and N for plant growth might be provided by soil microbes. An increasing body of evidence suggests that heavy metals have a strong impact on both bacterial and fungal communities. This population of R. extracellular sequestration. Indeed. but in the current study. no correlation between soil Zn concentration and shoot Zn concentration was observed. except for metal concentrations themselves. arylsulphatase activity. acetosa accumulated considerable amounts of Pb and Zn. can be grouped into five categories: intracellular sequestration. Both J.9%). Apart from that. acetosa has previously been reported to have great potential for Zn phytoextraction . The grass F. the four pseudometallophytes were able to spontaneously grow under such metalliferous conditions. Zn is an essential trace element. Nonetheless. In a study by Wang et al. Most importantly. nitrification potential. was able to tolerate the high levels of metal pollution by physiologically restricting the entry of heavy metals. acetosa is a species that usually behaves as a Zn indicator. emphasizing their importance for plant productivity in those areas. export. soil microorganisms have developed highly efficient systems for metal detoxification which. however.
3. confirming their adaptation to the harsh environmental conditions present in the mine. 5 . ecosystem functions and biological communities interact in the long-term is needed for proper management of these fragile metalliferous ecosystems. but not to plant richness. caerulescens suggest that this species is probably better protected against environmental stress than the others. physiological strategies used by metal-tolerant organisms. An ecological understanding of how contaminants. Conclusions The study of metalliferous environments is of great relevance since it can provide invaluable information on ecological impact of heavy metals on ecosystem function. The suitability of each species for phytoremediation is also different regarding the recovery of soil health. These particular features observed in T. caerulescens under field conditions and the interesting results obtained should encourage the scientific community to further study the physiology of this plant in order to better understand its peculiar behaviour. Soil microbial properties had a stronger effect on plant biomass rather than the other way round.metabolites. Soil microbial parameters are related to plant biomass. The studied pseudometallophytes are tolerant to metal pollution and offer potential for the development of phytoextraction and phytostabilization technologies. This is the first time that antioxidant metabolites are studied in T. and novel tools for remediation of metal-polluted sites.
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