Strain-specific bioaccumulation and intracellular distribution of Cd2+ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi

Environmental Science and Pollution Research, Sep 2014

Bioaccumulation of Cd2+ in soil bacteria might represent an important route of metal transfer to associated mycorrhizal fungi and plants and may have potential as a tool to accelerate Cd2+ extraction in the bioremediation of contaminated soils. The present study examined the bioaccumulation of Cd2+ in 15 bacterial strains representing three phyla (Firmicutes, Proteobacteria, and Bacteroidetes) that were isolated from the rhizosphere, ectomycorrhizae, and fruitbody of ectomycorrhizal fungi. The strains Pseudomonas sp. IV-111-14, Variovorax sp. ML3-12, and Luteibacter sp. II-116-7 displayed the highest biomass productivity at the highest tested Cd2+ concentration (2 mM). Microscopic analysis of the cellular Cd distribution revealed intracellular accumulation by strains Massilia sp. III–116-18, Pseudomonas sp. IV-111-14, and Bacillus sp. ML1-2. The quantities of Cd measured in the interior of the cells ranged from 0.87 to 1.31 weight % Cd. Strains originating from the rhizosphere exhibited higher Cd2+ accumulation efficiencies than strains from ectomycorrhizal roots or fruitbodies. The high Cd tolerances of Pseudomonas sp. IV-111-16 and Bacillus sp. ML1-2 were attributed to the binding of Cd2+ as cadmium phosphate. Furthermore, silicate binding of Cd2+ by Bacillus sp. ML1-2 was observed. The tolerance of Massilia sp. III-116-18 to Cd stress was attributed to a simultaneous increase in K+ uptake in the presence of Cd2+ ions. We conclude that highly Cd-tolerant and Cd-accumulating bacterial strains from the genera Massilia sp., Pseudomonas sp., and Bacillus sp. might offer a suitable tool to improve the bioremediation efficiency of contaminated soils.

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Strain-specific bioaccumulation and intracellular distribution of Cd2+ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi

Katarzyna Hrynkiewicz 0 1 2 Micha Zoch 0 1 2 Tomasz Kowalkowski 0 1 2 Christel Baum 0 1 2 Katarzyna Niedojado 0 1 2 Bogusaw Buszewski 0 1 2 0 Responsible editor: Robert Duran 1 K. Niedojado Department of Cell Biology, Institute of General and Molecular Biology, N. Copernicus University of Torun , Torun, Poland 2 C. Baum Department of Agricultural and Environmental Sciences, Soil Science, University of Rostock , Justus-von-Liebig-Weg 6, 18059 Rostock, Germany Bioaccumulation of Cd2+ in soil bacteria might represent an important route of metal transfer to associated mycorrhizal fungi and plants and may have potential as a tool to accelerate Cd2+ extraction in the bioremediation of contaminated soils. The present study examined the bioaccumulation of Cd2+ in 15 bacterial strains representing three phyla (Firmicutes, Proteobacteria, and Bacteroidetes) that were isolated from the rhizosphere, ectomycorrhizae, and fruitbody of ectomycorrhizal fungi. The strains Pseudomonas sp. IV-111-14, Variovorax sp. ML3-12, and Luteibacter sp. II-116-7 displayed the highest biomass productivity at the highest tested Cd2+ concentration (2 mM). Microscopic analysis of the cellular Cd distribution revealed intracellular accumulation by strains Massilia sp. III116-18, Pseudomonas sp. IV-111-14, and Bacillus sp. ML1-2. The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors. - Cadmium (Cd2+) is not involved in any known biological processes and is one of the most critical heavy metal pollutants due to its high solubility in water (Pinto et al. 2003), rapid accumulation in the food chain, severe toxic effects on living organisms, and mutagenic nature (Rani and Goel 2009; Farooq et al. 2010). Cd2+ exposure has numerous effects in humans, including kidney damage, high blood pressure, and bone fractures (Drasch 1983), and is acknowledged as a priority pollutant by the US Environmental Protection Agency (USEPA) (Krishnan and Anirudhan 2003). The European Chemicals Agency (ECHA) has placed Cd2+ on the Candidate List of Substances of Very High Concern for Authorisation (SVHC), and its content in products is subjected to rigorous restrictions [Regulation (EC) No. 1907/2006 of the European Parliament and of the Council, 2006]. Cd is commonly present in wastes from technological processes such as plastic manufacturing, galvanizing plating or pigments, and Cd/Ni battery production. Cd2+ is highly toxic in even relatively low concentrations; the World Health Organization (WHO) describes the highest permissible level of this element as 0.003 mg L1 (Cadmium in drinking water 2011). Cd2+ soil contamination can decrease crop yields by inhibiting photosynthesis, respiration, and nitrogen metabolism and by reducing water and mineral uptake (Tynecka et al. 1981). Microorganisms associated with plant roots can increase biomass production at sites polluted with heavy metals, affect metal mobilization in the soil, and protect the host plant from heavy metal toxicity (Hrynkiewicz and Baum 2012; 2013). Many bacteria are tolerant to high concentrations of Cd2+; however, this element generally causes reduced growth, long log phases, lower cell densities, and even bacterial death (Les and Walker 1984; Sinha and Mukherjee 2009). The presence of Cd2+ in the environment can affect the survival and composition of bacterial populations, thereby negatively affecting plant growth (Siripornadulsil and Siripornadulsil 2013) and impacting the entire ecosystem. Bacteria have developed several mechanisms for the detoxification of Cd2+, e.g., extracellular and intracellular sequestration (Hetzer et al. 2006), active efflux out of the cell (Teitzel and Parsek 2003), and biotransformation into less toxic forms (Khan et al. 2010), which allow these bacteria to tolerate increased concentrations of Cd2+ ions in the environment (Nies 1999). A fundamental strategy to avoid the toxic effects of Cd2+ ions that is widespread among bacterial species is to prevent the ions from entering the cell and to keep them away from the target sites (exclusion). This process may involve three different mechanisms: adsorption on the cell surface, secretion of high amounts of viscous slime outside the cells, and/or precipitation (Bruins et al. 2000; Zamil et al. 2008; Deb et al. 2013). The bacterial cell wall is the first component that interacts with heavy metal ions (Yun et al. 2011). Mechanisms of cell surface sorption are passive and based upon physicochemical interactions between the metal and the functional groups of the cell wall; this process occurs independently of cell metabolism (Oh et al. 2009). The negatively charged bacterial cell wall can bind high quantities of positively charged Cd2+ ions, thereby immobilizing the metal and inhibiting its intracellular toxic effects (Goulhen et al. 2006; Parungao et al. 2007). The carboxyl groups responsible for forming Cd-carboxyl complexes on the bacterial surface may be in (...truncated)


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Katarzyna Hrynkiewicz, Michał Złoch, Tomasz Kowalkowski, Christel Baum, Katarzyna Niedojadło, Bogusław Buszewski. Strain-specific bioaccumulation and intracellular distribution of Cd2+ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi, Environmental Science and Pollution Research, 2015, pp. 3055-3067, Volume 22, Issue 4, DOI: 10.1007/s11356-014-3489-0