Strain-specific bioaccumulation and intracellular distribution of Cd2+ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi
Katarzyna Hrynkiewicz
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Micha Zoch
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Tomasz Kowalkowski
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Christel Baum
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Katarzyna Niedojado
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Bogusaw Buszewski
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Responsible editor: Robert Duran
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K. Niedojado Department of Cell Biology, Institute of General and Molecular Biology, N. Copernicus University of Torun
, Torun,
Poland
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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.
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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)