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Cadmium toxicity to Microcystis aeruginosa PCC 7806 and its microcystin-lacking mutant.

Huang B, Xu S, Miao AJ, Xiao L, Yang LY - PLoS ONE (2015)

Bottom Line: The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public.Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves.Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu Province, China.

ABSTRACT
The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public. Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves. One suggested function of MC is complexation, which may influence the bioaccumulation and toxicity of trace metals. To test this hypothesis, we examined Cd toxicity to wild-type Microcystis aeruginosa PCC 7806 (WT) and its MC-lacking mutant (MT) under nutrient-enriched (+NP), phosphorus-limited (-P), and nitrogen-limited (-N) conditions. The accumulation of Cd and the biochemical parameters associated with its detoxification [total phosphorus (TP), inorganic polyphosphate (Poly-P), and glutathione (GSH) in the cells as well as intra- and extra-cellular carbohydrates] were quantified. Although the -P cyanobacteria accumulated less Cd than their +NP and -N counterparts, the different nutrient-conditioned cyanobacteria were similarly inhibited by similar free ion concentration of Cd in the medium ([Cd2+]F). Such good toxicity predictability of [Cd2+]F was ascribed to the synchronous decrease in the intracellular concentrations of Cd and TP. Nevertheless, Cd toxicity was still determined by the intracellular Cd to phosphorus ratio (Cd/P), in accordance with what has been reported in the literature. On the other hand, the concentrations of TP, Poly-P, and carbohydrates went up, but GSH concentration dropped down with the enhancement of [Cd2+]F, indicating their association with Cd detoxification. Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity. These results suggest that MC cannot affect metal toxicity either by regulating metal accumulation or by altering the detoxification ability of the cyanobacteria. Other possible functions of MC need to be further investigated.

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Cellular concentration of glutathione ([GSH]cell) in treatments A-H of the (a) nutrient-enriched (+NP), (b) phosphorus-limited (-P), and (c) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
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pone.0116659.g005: Cellular concentration of glutathione ([GSH]cell) in treatments A-H of the (a) nutrient-enriched (+NP), (b) phosphorus-limited (-P), and (c) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)

Mentions: LMW thiols such as GSH and phytochelatins [(γ-Glu-Cys)n-Gly, n = 2–4] have been demonstrated to be involved in metal complexation and detoxification in eukaryotic phytoplankton [55]. As for WT and MT, their [GSH]cell decreased strikingly (e.g., as much as 86.6–89.4% under the—P condition) at higher levels of Cd (Fig. 5 and Figure D in S1 File). Such abrupt reduction might be explained by two possibilities. First, GSH could remove reactive oxygen species and thus more GSH was consumed at higher [Cd2+]F to alleviate the oxidative stresses caused by Cd [56]. Second, GSH might be transformed to other LMW thiols (e.g., phytochelatins), which could scavenge trace metals in the vacuoles of phytoplankton [57]. Although WT contained significantly (p < 0.05, two-way ANOVA, Table C in S1 File) more GSH than MT under the +NP condition, a reverse trend was observed when the cells were N or P limited, suggesting different extent of oxidative stresses for these two cyanobacterial strains under nutrient limitation. On the other hand, phytochelatins were below the detection limit in present study suggesting that M. aeruginosa was unable to synthesize these thiols in appreciable amounts. Our finding further supports the previous opinion that cyanobacteria lack the phytochelatin synthase gene observed in eukaryotes [58]. Although suspicious genes with similar functions were reported in cyanobacteria, one of the proteins (Alr0975), encoded in the genes of the cyanobacterium Nostoc sp. does not possess the phytochelatin synthase ability [59].


Cadmium toxicity to Microcystis aeruginosa PCC 7806 and its microcystin-lacking mutant.

Huang B, Xu S, Miao AJ, Xiao L, Yang LY - PLoS ONE (2015)

Cellular concentration of glutathione ([GSH]cell) in treatments A-H of the (a) nutrient-enriched (+NP), (b) phosphorus-limited (-P), and (c) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4295860&req=5

pone.0116659.g005: Cellular concentration of glutathione ([GSH]cell) in treatments A-H of the (a) nutrient-enriched (+NP), (b) phosphorus-limited (-P), and (c) nitrogen-limited (-N) toxicity tests for Microcystis aeruginosa PCC 7806 (WT, black bar) and its MC-lacking mutant (MT, white bar).All values were normalized to levels (100% as represented by the dashed lines) detected in the WT strain at the lowest respective Cd concentration (Treatment A). Cd concentration in treatments A-H ([Cd]T, 1.00×10-8—9.95×10-6 M; [Cd2+]F, 1.00×10-13—1.21×10-8 M) is listed in Table B of S1 File. Data are mean ± standard error (n = 2)
Mentions: LMW thiols such as GSH and phytochelatins [(γ-Glu-Cys)n-Gly, n = 2–4] have been demonstrated to be involved in metal complexation and detoxification in eukaryotic phytoplankton [55]. As for WT and MT, their [GSH]cell decreased strikingly (e.g., as much as 86.6–89.4% under the—P condition) at higher levels of Cd (Fig. 5 and Figure D in S1 File). Such abrupt reduction might be explained by two possibilities. First, GSH could remove reactive oxygen species and thus more GSH was consumed at higher [Cd2+]F to alleviate the oxidative stresses caused by Cd [56]. Second, GSH might be transformed to other LMW thiols (e.g., phytochelatins), which could scavenge trace metals in the vacuoles of phytoplankton [57]. Although WT contained significantly (p < 0.05, two-way ANOVA, Table C in S1 File) more GSH than MT under the +NP condition, a reverse trend was observed when the cells were N or P limited, suggesting different extent of oxidative stresses for these two cyanobacterial strains under nutrient limitation. On the other hand, phytochelatins were below the detection limit in present study suggesting that M. aeruginosa was unable to synthesize these thiols in appreciable amounts. Our finding further supports the previous opinion that cyanobacteria lack the phytochelatin synthase gene observed in eukaryotes [58]. Although suspicious genes with similar functions were reported in cyanobacteria, one of the proteins (Alr0975), encoded in the genes of the cyanobacterium Nostoc sp. does not possess the phytochelatin synthase ability [59].

Bottom Line: The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public.Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves.Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu Province, China.

ABSTRACT
The adverse effects of microcystin (MC) produced by cyanobacteria have drawn considerable attention from the public. Yet it remains unclear whether MC confers any benefits to the cyanobacteria themselves. One suggested function of MC is complexation, which may influence the bioaccumulation and toxicity of trace metals. To test this hypothesis, we examined Cd toxicity to wild-type Microcystis aeruginosa PCC 7806 (WT) and its MC-lacking mutant (MT) under nutrient-enriched (+NP), phosphorus-limited (-P), and nitrogen-limited (-N) conditions. The accumulation of Cd and the biochemical parameters associated with its detoxification [total phosphorus (TP), inorganic polyphosphate (Poly-P), and glutathione (GSH) in the cells as well as intra- and extra-cellular carbohydrates] were quantified. Although the -P cyanobacteria accumulated less Cd than their +NP and -N counterparts, the different nutrient-conditioned cyanobacteria were similarly inhibited by similar free ion concentration of Cd in the medium ([Cd2+]F). Such good toxicity predictability of [Cd2+]F was ascribed to the synchronous decrease in the intracellular concentrations of Cd and TP. Nevertheless, Cd toxicity was still determined by the intracellular Cd to phosphorus ratio (Cd/P), in accordance with what has been reported in the literature. On the other hand, the concentrations of TP, Poly-P, and carbohydrates went up, but GSH concentration dropped down with the enhancement of [Cd2+]F, indicating their association with Cd detoxification. Although the inactivation of MC peptide synthetase gene had some nutrient and Cd concentration dependent effects on the parameters above, both cyanobacterial strains showed the same Cd accumulation ability and displayed similar Cd sensitivity. These results suggest that MC cannot affect metal toxicity either by regulating metal accumulation or by altering the detoxification ability of the cyanobacteria. Other possible functions of MC need to be further investigated.

Show MeSH
Related in: MedlinePlus